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Default mode network

Default mode network
medial prefrontal cortex, the posterior cingulate cortex, the precuneus and the angular gyrus
Anatomical terminology]
Default mode network connectivity. This image shows main regions of the default mode network (yellow) and connectivity between the regions color-coded by structural traversing direction (xyz → rgb).[1][2]

In

medial prefrontal cortex, posterior cingulate cortex, precuneus and angular gyrus. It is best known for being active when a person is not focused on the outside world and the brain is at wakeful rest, such as during daydreaming and mind-wandering. It can also be active during detailed thoughts related to external task performance.[3] Other times that the DMN is active include when the individual is thinking about others, thinking about themselves, remembering the past, and planning for the future.[4][5]

The DMN was originally noticed to be deactivated in certain goal-oriented tasks and was sometimes referred to as the task-negative network,[6] in contrast with the task-positive network. This nomenclature is now widely considered misleading, because the network can be active in internal goal-oriented and conceptual cognitive tasks.[7][8][9][10] The DMN has been shown to be negatively correlated with other networks in the brain such as attention networks.[11]

Evidence has pointed to disruptions in the DMN of people with

autism spectrum disorder.[4]

History

electroencephalogram, was the first to propose the idea that the brain is constantly busy. In a series of papers published in 1929, he showed that the electrical oscillations detected by his device do not cease even when the subject is at rest. However, his ideas were not taken seriously, and a general perception formed among neurologists that only when a focused activity is performed does the brain (or a part of the brain) become active.[12]

But in the 1950s,

In the 1990s, with the advent of positron emission tomography (PET) scans, researchers began to notice that when a person is involved in perception, language, and attention tasks, the same brain areas become less active compared to passive rest, and labeled these areas as becoming "deactivated".[4]

In 1995, Bharat Biswal, a graduate student at the Medical College of Wisconsin in Milwaukee, discovered that the human sensorimotor system displayed "resting-state connectivity," exhibiting synchronicity in functional magnetic resonance imaging (fMRI) scans while not engaged in any task.[14][15]

Later, experiments by neurologist Marcus E. Raichle's lab at Washington University School of Medicine and other groups[16] showed that the brain's energy consumption is increased by less than 5% of its baseline energy consumption while performing a focused mental task. These experiments showed that the brain is constantly active with a high level of activity even when the person is not engaged in focused mental work. Research thereafter focused on finding the regions responsible for this constant background activity level.[12]

Raichle coined the term "default mode" in 2001 to describe resting state brain function;[17] the concept rapidly became a central theme in neuroscience.[18] Around this time the idea was developed that this network of brain areas is involved in internally directed thoughts and is suspended during specific goal-directed behaviors. In 2003, Greicius and colleagues examined resting state fMRI scans and looked at how correlated different sections in the brain are to each other. Their correlation maps highlighted the same areas already identified by the other researchers.[19] This was important because it demonstrated a convergence of methods all leading to the same areas being involved in the DMN. Since then other networks have been identified, such as visual, auditory, and attention networks. Some of them are often anti-correlated with the default mode network.[11]

Until the mid-2000s, researchers labeled the default mode network as the "task-negative network" because it was deactivated when participants had to perform external goal-directed tasks.[6] DMN was thought to only be active during passive rest and inactive during tasks. However, more recent studies have demonstrated the DMN to be active in certain internal goal-directed tasks such as social working memory and autobiographical tasks.[7]

Around 2007, the number of papers referencing the default mode network skyrocketed.[20] In all years prior to 2007, there were 12 papers published that referenced "default mode network" or "default network" in the title; however, between 2007 and 2014 the number increased to 1,384 papers. One reason for the increase in papers was the robust effect of finding the DMN with resting-state scans and independent component analysis (ICA).[16][21] Another reason was that the DMN could be measured with short and effortless resting-state scans, meaning they could be performed on any population including young children, clinical populations, and nonhuman primates.[4] A third reason was that the role of the DMN had been expanded to more than just a passive brain network.[4]

Anatomy

Graphs of the dynamic development of correlations between brain networks. (A) In children the regions are largely local and are organized by their physical location; the frontal regions are highlighted in light blue. (B) In adults the networks become highly correlated despite their physical distance; the default network is highlighted in light red.[22] This result is now believed to have been confounded by artifactual processes attributable to the tendency of younger subjects to move more during image acquisition, which preferentially inflates estimates of connectivity between physically proximal regions (Power 2012, Satterthwaite 2012).

The default mode network is an interconnected and anatomically defined[4] set of brain regions. The network can be separated into hubs and subsections:

Functional hubs:[23] Information regarding the self

  • Posterior cingulate cortex (PCC) & precuneus: Combines bottom-up (not controlled) attention with information from memory and perception. The ventral (lower) part of PCC activates in all tasks which involve the DMN including those related to the self, related to others, remembering the past, thinking about the future, and processing concepts plus spatial navigation. The dorsal (upper) part of PCC involves involuntary awareness and arousal. The precuneus is involved in visual, sensorimotor, and attentional information.
  • Medial prefrontal cortex
    (mPFC)
    : Decisions about self-processing such as personal information, autobiographical memories, future goals and events, and decision making regarding those personally very close such as family. The ventral (lower) part is involved in positive emotional information and internally valued reward.
  • Angular gyrus: Connects perception, attention, spatial cognition, and action and helps with parts of recall of episodic memories.

Dorsal medial subsystem:[23] Thinking about others

Medial temporal subsystem:[23] Autobiographical memory and future simulations

The default mode network is most commonly defined with

posterior cingulate cortex and examining which other brain areas most correlate with this area.[19] The DMN can also be defined by the areas deactivated during external directed tasks compared to rest.[17] Independent component analysis (ICA) robustly finds the DMN for individuals and across groups, and has become the standard tool for mapping the default network.[16][21]

It has been shown that the default mode network exhibits the highest overlap in its structural and functional connectivity, which suggests that the structural architecture of the brain may be built in such a way that this particular network is activated by default.[1] Recent evidence from a population brain-imaging study of 10,000 UK Biobank participants further suggests that each DMN node can be decomposed into subregions with complementary structural and functional properties. It has been a widespread practice in DMN research to treat its constituent nodes to be functionally homogeneous, but the distinction between subnodes within each major DMN node has mostly been neglected. However, the close proximity of subnodes that propagate hippocampal space-time outputs and subnodes that describe the global network architecture may enable default functions, such as autobiographical recall or internally-orientated thinking.[25]

In the infant's brain, there is limited evidence of the default network, but default network connectivity is more consistent in children aged 9–12 years, suggesting that the default network undergoes developmental change.[11]

Functional connectivity analysis in monkeys shows a similar network of regions to the default mode network seen in humans.[4] The PCC is also a key hub in monkeys; however, the mPFC is smaller and less well connected to other brain regions, largely because human's mPFC is much larger and well developed.[4]

Diffusion MRI imaging shows white matter tracts connecting different areas of the DMN together.[20] The structural connections found from diffusion MRI imaging and the functional correlations from resting state fMRI show the highest level of overlap and agreement within the DMN areas.[1] This provides evidence that neurons in the DMN regions are linked to each other through large tracts of axons and this causes activity in these areas to be correlated with one another. From the point of view of effective connectivity, many studies have attempted to shed some light using dynamic causal modeling, with inconsistent results. However, directionality from the medial prefrontal cortex towards the posterior cingulate gyrus seems confirmed in multiple studies, and the inconsistent results appear to be related to small sample size analysis.[26]

Function

The default mode network is thought to be involved in several different functions:

It is potentially the neurological basis for the self:[20]

  • Autobiographical information: Memories of collection of events and facts about one's self
  • Self-reference: Referring to traits and descriptions of one's self
  • Emotion of one's self: Reflecting about one's own emotional state

Thinking about others:[20]

  • Theory of mind: Thinking about the thoughts of others and what they might or might not know
  • Emotions of others: Understanding the emotions of other people and empathizing with their feelings
  • Moral reasoning: Determining a just and an unjust result of an action
  • Social evaluations: Good-bad attitude judgements about social concepts
  • Social categories: Reflecting on important social characteristics and status of a group
  • Social isolation: A perceived lack of social interaction[27]

Remembering the past and thinking about the future:[20]

  • Remembering the past: Recalling events that happened in the past
  • Imagining the future: Envisioning events that might happen in the future
  • Episodic memory: Detailed memory related to specific events in time
  • Story comprehension: Understanding and remembering a narrative
  • Replay: Consolidating recently acquired memory traces[28]

The default mode network is active during passive rest and mind-wandering[4] which usually involves thinking about others, thinking about one's self, remembering the past, and envisioning the future rather than the task being performed.[20] Recent work, however, has challenged a specific mapping between the default mode network and mind-wandering, given that the system is important in maintaining detailed representations of task information during working memory encoding.[29] Electrocorticography studies (which involve placing electrodes on the surface of a subject's cerebral cortex) have shown the default mode network becomes activated within a fraction of a second after participants finish a task.[30] Additionally, during attention demanding tasks, sufficient deactivation of the default mode network at the time of memory encoding has been shown to result in more successful long-term memory consolidation.[31]

Studies have shown that when people watch a movie,[32] listen to a story,[33][34] or read a story,[35] their DMNs are highly correlated with each other. DMNs are not correlated if the stories are scrambled or are in a language the person does not understand, suggesting that the network is highly involved in the comprehension and the subsequent memory formation of that story.[34] The DMN is shown to even be correlated if the same story is presented to different people in different languages,[36] further suggesting the DMN is truly involved in the comprehension aspect of the story and not the auditory or language aspect.

The default mode network is deactivated during some external goal-oriented tasks such as visual attention or cognitive working memory tasks.[6] However, with internal goal-oriented tasks, such as social working memory or autobiographical tasks, the DMN is positively activated with the task and correlates with other networks such as the network involved in executive function.[7] Regions of the DMN are also activated during cognitively demanding tasks that require higher-order conceptual representations.[9] The DMN shows higher activation when behavioral responses are stable, and this activation is independent of self-reported mind wandering.[37]

Tsoukalas (2017) links theory of mind to immobilization, and suggests that the default network is activated by the immobilization inherent in the testing procedure (the patient is strapped supine on a stretcher and inserted by a narrow tunnel into a massive metallic structure). This procedure creates a sense of entrapment and, not surprisingly, the most commonly reported side-effect is claustrophobia.[38]

Gabrielle et al. (2019) suggests that the DMN is related to the perception of beauty, in which the network becomes activated in a generalized way to aesthetically moving domains such as artworks, landscapes, and architecture. This would explain a deep inner feeling of pleasure related to aesthetics, interconnected with the sense of personal identity, due to the network functions related to the self.[39]

Clinical significance

The default mode network has been hypothesized to be relevant to disorders including Alzheimer's disease, autism, schizophrenia, major depressive disorder (MDD), chronic pain, post-traumatic stress disorder (PTSD) and others.[4][40] In particular, the DMN has also been reported to show overlapping yet distinct neural activity patterns across different mental health conditions, such as when directly comparing attention deficit hyperactivity disorder (ADHD) and autism.[41]

People with Alzheimer's disease show a reduction in glucose (energy use) within the areas of the default mode network.[4] These reductions start off as slight decreases in patients with mild symptoms and continue to large reductions in those with severe symptoms. Surprisingly, disruptions in the DMN begin even before individuals show signs of Alzheimer's disease.[4] Plots of the peptide amyloid-beta, which is thought to cause Alzheimer's disease, show the buildup of the peptide is within the DMN.[4] This prompted Randy Buckner and colleagues to propose the high metabolic rate from continuous activation of DMN causes more amyloid-beta peptide to accumulate in these DMN areas.[4] These amyloid-beta peptides disrupt the DMN and because the DMN is heavily involved in memory formation and retrieval, this disruption leads to the symptoms of Alzheimer's disease.

DMN is thought to be disrupted in individuals with autism spectrum disorder.[4][42] These individuals are impaired in social interaction and communication which are tasks central to this network. Studies have shown worse connections between areas of the DMN in individuals with autism, especially between the mPFC (involved in thinking about the self and others) and the PCC (the central core of the DMN).[43][44] The more severe the autism, the less connected these areas are to each other.[43][44] It is not clear if this is a cause or a result of autism, or if a third factor is causing both (confounding).

Although it is not clear whether the DMN connectivity is increased or decreased in psychotic bipolar disorder and schizophrenia, several genes correlated with altered DMN connectivity are also risk genes for mood and psychosis disorders.[45]

Rumination, one of the main symptoms of major depressive disorder, is associated with increased DMN connectivity and dominance over other networks during rest.[46][47] Such DMN hyperconnectivity has been observed in first-episode depression[48] and chronic pain.[49] Altered DMN connectivity may change the way a person perceives events and their social and moral reasoning, thus increasing their susceptibility to depressive symptoms.[50]

Lower connectivity between brain regions was found across the default network in people who have experienced long-term trauma, such as childhood abuse or neglect, and is associated with dysfunctional attachment patterns. Among people experiencing PTSD, lower activation was found in the posterior cingulate gyrus compared to controls, and severe PTSD was characterized by lower connectivity within the DMN.[40][51]

Adults and children with ADHD show reduced anticorrelation between the DMN and other brain networks.[52][53] The cause may be a lag in brain maturation.[54] More generally, competing activation between the DMN and other networks during memory encoding may result in poor long-term memory consolidation, which is a symptom of not only ADHD but also depression, anxiety, autism, and schizophrenia.[31]

Modulation

The default mode network (DMN) may be modulated by the following interventions and processes:

Criticism

Some have argued the brain areas in the default mode network only show up together because of the vascular coupling of large arteries and veins in the brain near these areas, not because these areas are actually functionally connected to each other. Support for this argument comes from studies that show changing in breathing alters oxygen levels in the blood which in turn affects DMN the most.[4] These studies however do not explain why the DMN can also be identified using PET scans by measuring glucose metabolism which is independent of vascular coupling[4] and in electrocorticography studies[72] measuring electrical activity on the surface of the brain, and in MEG by measuring magnetic fields associated with electrophysiological brain activity that bypasses the hemodynamic response.[73]

The idea of a "default network" is not universally accepted.[74] In 2007 the concept of the default mode was criticized as not being useful for understanding brain function, on the grounds that a simpler hypothesis is that a resting brain actually does more processing than a brain doing certain "demanding" tasks, and that there is no special significance to the intrinsic activity of the resting brain.[75]

Nomenclature

The default mode network has also been called the language network, semantic system, or limbic network.[10] Even though the dichotomy is misleading,[7] the term task-negative network is still sometimes used to contrast it against other more externally-oriented brain networks.[53]

In 2019, Uddin et al. proposed that medial frontoparietal network (M-FPN) be used as a standard anatomical name for this network.[10]

See also

References

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  26. ^ Silchenko, Alexander N.; Hoffstaedter, Felix; Eickhoff, Simon B. (2023). "Impact of sample size and regression of tissue-specific signals on effective connectivity within the core default mode network". Human Brain Mapping.
  27. PMID 33319780.{{cite journal}}: CS1 maint: multiple names: authors list (link
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  46. . Retrieved 6 June 2014.
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  49. ^ Sambataro, Fabio; Wolf, Nadine; Giusti, Pietro; Vasic, Nenad; Wolf, Robert (October 2013). "Default mode network in depression: A pathway to impaired affective cognition?" (PDF). Clinical Neuralpyschiatry. 10: 212–216. Archived from the original (PDF) on 29 August 2017. Retrieved 28 September 2017.
  50. ^ Dr. Ruth Lanius, Brain Mapping conference, London, November 2010
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External links


Electrocorticography

Electrocorticography
Intracranial electrode grid for electrocorticography.
SynonymsIntracranial electroencephalography
Purposerecord electrical activity from the cerebral cortex.(invasive)

Electrocorticography (ECoG), a type of intracranial electroencephalography (iEEG), is a type of electrophysiological monitoring that uses electrodes placed directly on the exposed surface of the brain to record electrical activity from the cerebral cortex. In contrast, conventional electroencephalography (EEG) electrodes monitor this activity from outside the skull. ECoG may be performed either in the operating room during surgery (intraoperative ECoG) or outside of surgery (extraoperative ECoG). Because a craniotomy (a surgical incision into the skull) is required to implant the electrode grid, ECoG is an invasive procedure.

History

ECoG was pioneered in the early 1950s by

Montreal Neurological Institute.[1] The two developed ECoG as part of their groundbreaking Montreal procedure, a surgical protocol used to treat patients with severe epilepsy. The cortical potentials recorded by ECoG were used to identify epileptogenic zones – regions of the cortex that generate epileptic seizures. These zones would then be surgically removed from the cortex during resectioning, thus destroying the brain tissue where epileptic seizures had originated. Penfield and Jasper also used electrical stimulation during ECoG recordings in patients undergoing epilepsy surgery under local anesthesia.[2]
This procedure was used to explore the functional anatomy of the brain, mapping speech areas and identifying the somatosensory and somatomotor cortex areas to be excluded from surgical removal. A doctor named Robert Galbraith Heath was also an early researcher of the brain at the Tulane University School of Medicine.[3][4]

Electrophysiological basis

ECoG signals are composed of synchronized postsynaptic potentials (

skull, where potentials rapidly attenuate due to the low conductivity of bone. For this reason, the spatial resolution of ECoG is much higher than EEG, a critical imaging advantage for presurgical planning.[5] ECoG offers a temporal resolution of approximately 5 ms and spatial resolution as low as 1-100 μm.[6]

Using depth electrodes, the

action potentials.[8] In which case the spatial resolution is down to individual neurons, and the field of view of an individual electrode is approximately 0.05–0.35 mm.[7]

Procedure

The ECoG recording is performed from electrodes placed on the exposed cortex. In order to access the cortex, a surgeon must first perform a craniotomy, removing a part of the skull to expose the brain surface. This procedure may be performed either under

Platinum-iridium alloy or gold ball electrodes, each mounted on a ball and socket joint for ease in positioning. These electrodes are attached to an overlying frame in a "crown" or "halo" configuration.[9] Subdural strip and grid electrodes are also widely used in various dimensions, having anywhere from 4 to 256[10] electrode contacts. The grids are transparent, flexible, and numbered at each electrode contact. Standard spacing between grid electrodes is 1 cm; individual electrodes are typically 5 mm in diameter. The electrodes sit lightly on the cortical surface, and are designed with enough flexibility to ensure that normal movements of the brain do not cause injury. A key advantage of strip and grid electrode arrays is that they may be slid underneath the dura mater into cortical regions not exposed by the craniotomy. Strip electrodes and crown arrays may be used in any combination desired. Depth electrodes may also be used to record activity from deeper structures such as the hippocampus
.

DCES

Direct cortical electrical stimulation (DCES), also known as cortical stimulation mapping, is frequently performed in concurrence with ECoG recording for functional mapping of the cortex and identification of critical cortical structures.[9] When using a crown configuration, a handheld wand bipolar stimulator may be used at any location along the electrode array. However, when using a subdural strip, stimulation must be applied between pairs of adjacent electrodes due to the nonconductive material connecting the electrodes on the grid. Electrical stimulating currents applied to the cortex are relatively low, between 2 and 4 mA for somatosensory stimulation, and near 15 mA for cognitive stimulation.[9] The stimulation frequency is usually 60 Hz in North America and 50 Hz in Europe, and any charge density more than 150 μC/cm2 causes tissue damage.[11][12]

The functions most commonly mapped through DCES are primary motor, primary sensory, and language. The patient must be alert and interactive for mapping procedures, though patient involvement varies with each mapping procedure. Language mapping may involve naming, reading aloud, repetition, and oral comprehension; somatosensory mapping requires that the patient describe sensations experienced across the face and extremities as the surgeon stimulates different cortical regions.[9]

Clinical applications

Since its development in the 1950s, ECoG has been used to localize epileptogenic zones during presurgical planning, map out cortical functions, and to predict the success of epileptic surgical resectioning. ECoG offers several advantages over alternative diagnostic modalities:

  • Flexible placement of recording and stimulating electrodes[2]
  • Can be performed at any stage before, during, and after a surgery
  • Allows for direct electrical stimulation of the brain, identifying critical regions of the cortex to be avoided during surgery
  • Greater precision and sensitivity than an EEG scalp recording – spatial resolution is higher and signal-to-noise ratio is superior due to closer proximity to neural activity

Limitations of ECoG include:

  • Limited sampling time – seizures (
    ictal
    events) may not be recorded during the ECoG recording period
  • Limited field of view – electrode placement is limited by the area of exposed cortex and surgery time, sampling errors may occur
  • Recording is subject to the influence of anesthetics, narcotic analgesics, and the surgery itself[2]

Intractable epilepsy

Epilepsy is currently ranked as the third most commonly diagnosed neurological disorder, afflicting approximately 2.5 million people in the United States alone.[13] Epileptic seizures are chronic and unrelated to any immediately treatable causes, such as toxins or infectious diseases, and may vary widely based on etiology, clinical symptoms, and site of origin within the brain. For patients with intractable epilepsy – epilepsy that is unresponsive to anticonvulsants – surgical treatment may be a viable treatment option. Partial epilepsy[14] is the common intractable epilepsy and the partial seizure is difficult to locate.Treatment for such epilepsy is limited to attachment of vagus nerve stimulator. Epilepsy surgery is the cure for partial epilepsy provided that the brain region generating seizure is carefully and accurately removed.

Extraoperative ECoG

Before a patient can be identified as a candidate for resectioning surgery, MRI must be performed to demonstrate the presence of a structural lesion within the cortex, supported by EEG evidence of epileptogenic tissue.

interictal
epileptiform activity (IEA), brief bursts of neuronal activity recorded between epileptic events. ECoG is also performed following the resectioning surgery to detect any remaining epileptiform activity, and to determine the success of the surgery. Residual spikes on the ECoG, unaltered by the resection, indicate poor seizure control, and incomplete neutralization of the epileptogenic cortical zone. Additional surgery may be necessary to completely eradicate seizure activity. Extraoperative ECoG is also used to localize functionally-important areas (also known as eloquent cortex) to be preserved during epilepsy surgery. [17] Motor, sensory, cognitive tasks during extraoperative ECoG are reported to increase the amplitude of high-frequency activity at 70–110 Hz in areas involved in execution of given tasks.[17][18][19] Task-related high-frequency activity can animate 'when' and 'where' cerebral cortex is activated and inhibited in a 4D manner with a temporal resolution of 10 milliseconds or below and a spatial resolution of 10 mm or below.[18][19]

Intraoperative ECoG

The objective of the resectioning surgery is to remove the epileptogenic tissue without causing unacceptable neurological consequences. In addition to identifying and localizing the extent of epileptogenic zones, ECoG used in conjunction with DCES is also a valuable tool for functional cortical mapping. It is vital to precisely localize critical brain structures, identifying which regions the surgeon must spare during resectioning (the "eloquent cortex") in order to preserve sensory processing, motor coordination, and speech. Functional mapping requires that the patient be able to interact with the surgeon, and thus is performed under local rather than general anesthesia. Electrical stimulation using cortical and acute depth electrodes is used to probe distinct regions of the cortex in order to identify centers of speech, somatosensory integration, and somatomotor processing. During the resectioning surgery, intraoperative ECoG may also be performed to monitor the epileptic activity of the tissue and ensure that the entire epileptogenic zone is resectioned.

Although the use of extraoperative and intraoperative ECoG in resectioning surgery has been an accepted clinical practice for several decades, recent studies have shown that the usefulness of this technique may vary based on the type of epilepsy a patient exhibits. Kuruvilla and Flink reported that while intraoperative ECoG plays a critical role in tailored temporal lobectomies, in multiple subpial transections (MST), and in the removal of malformations of cortical development (MCDs), it has been found impractical in standard resection of medial temporal lobe epilepsy (TLE) with MRI evidence of mesial temporal sclerosis (MTS).[2] A study performed by Wennberg, Quesney, and Rasmussen demonstrated the presurgical significance of ECoG in frontal lobe epilepsy (FLE) cases.[20]

Research applications

ECoG has recently emerged as a promising recording technique for use in

brain-computer interfaces (BCI).[21] BCIs are direct neural interfaces that provide control of prosthetic, electronic, or communication devices via direct use of the individual's brain signals. Brain signals may be recorded either invasively, with recording devices implanted directly into the cortex, or noninvasively, using EEG scalp electrodes. ECoG serves to provide a partially invasive compromise between the two modalities – while ECoG does not penetrate the blood–brain barrier like invasive recording devices, it features a higher spatial resolution and higher signal-to-noise ratio than EEG.[21] ECoG has gained attention recently for decoding imagined speech or music, which could lead to "literal" BCIs[22] in which users simply imagine words, sentences, or music that the BCI can directly interpret.[23][24]

In addition to clinical applications to localize functional regions to support neurosurgery, real-time functional brain mapping with ECoG has gained attention to support research into fundamental questions in neuroscience. For example, a 2017 study explored regions within face and color processing areas and found that these subregions made highly specific contributions to different aspects of vision.[25] Another study found that high-frequency activity from 70 to 200 Hz reflected processes associated with both transient and sustained decision-making.[26] Other work based on ECoG presented a new approach to interpreting brain activity, suggesting that both power and phase jointly influence instantaneous voltage potential, which directly regulates cortical excitability.[27] Like the work toward decoding imagined speech and music, these research directions involving real-time functional brain mapping also have implications for clinical practice, including both neurosurgery and BCI systems. The system that was used in most of these real-time functional mapping publications, "CortiQ". has been used for both research and clinical applications.

Recent advances

The electrocorticogram is still considered to be the "gold standard" for defining epileptogenic zones; however, this procedure is risky and highly invasive. Recent studies have explored the development of a noninvasive cortical imaging technique for presurgical planning that may provide similar information and resolution of the invasive ECoG.

In one novel approach, Lei Ding et al.[28] seek to integrate the information provided by a structural MRI and scalp EEG to provide a noninvasive alternative to ECoG. This study investigated a high-resolution subspace source localization approach, FINE (first principle vectors) to image the locations and estimate the extents of current sources from the scalp EEG. A thresholding technique was applied to the resulting tomography of subspace correlation values in order to identify epileptogenic sources. This method was tested in three pediatric patients with intractable epilepsy, with encouraging clinical results. Each patient was evaluated using structural MRI, long-term video EEG monitoring with scalp electrodes, and subsequently with subdural electrodes. The ECoG data were then recorded from implanted subdural electrode grids placed directly on the surface of the cortex. MRI and computed tomography images were also obtained for each subject.

The epileptogenic zones identified from preoperative EEG data were validated by observations from postoperative ECoG data in all three patients. These preliminary results suggest that it is possible to direct surgical planning and locate epileptogenic zones noninvasively using the described imaging and integrating methods. EEG findings were further validated by the surgical outcomes of all three patients. After surgical resectioning, two patients are seizure-free and the third has experienced a significant reduction in seizures. Due to its clinical success, FINE offers a promising alternative to preoperative ECoG, providing information about both the location and extent of epileptogenic sources through a noninvasive imaging procedure.

See also

References


Brain–computer interface

A brain–computer interface (BCI), sometimes called a brain–machine interface (BMI), is a direct communication link between the

ECoG and endovascular) to invasive (microelectrode array), based on how physically close electrodes are to brain tissue.[2]

Research on BCIs began in the 1970s by Jacques Vidal at the University of California, Los Angeles (UCLA) under a grant from the National Science Foundation, followed by a contract from DARPA.[3][4] Vidal's 1973 paper introduced the expression brain–computer interface into scientific literature.

Due to the

neuroprosthetic
devices were implanted in humans in the mid-1990s.

Studies in

human-computer interaction via the application of machine learning to statistical temporal features extracted from the frontal lobe (EEG brainwave) data has achieved success in classifying mental states (relaxed, neutral, concentrating),[6] mental emotional states (negative, neutral, positive),[7] and thalamocortical dysrhythmia.[8]

History

The history of brain-computer interfaces (BCIs) starts with Hans Berger's discovery of the brain's electrical activity and the development of electroencephalography (EEG). In 1924 Berger was the first to record human brain activity utilizing EEG. Berger was able to identify oscillatory activity, such as the alpha wave (8–13 Hz), by analyzing EEG traces.

Berger's first recording device was rudimentary. He inserted

voltages
as small as 10-4 volt, led to success.

Berger analyzed the interrelation of alternations in his EEG wave diagrams with

brain diseases
. EEGs permitted completely new possibilities for brain research.

Although the term had not yet been coined, one of the earliest examples of a working brain-machine interface was the piece Music for Solo Performer (1965) by American composer

alpha waves and thereby "playing" the various instruments via loudspeakers that are placed near or directly on the instruments.[9]

Vidal coined the term "BCI" and produced the first peer-reviewed publications on this topic.[3][4] He is widely recognized as the inventor of BCIs.[10][11][12] A review pointed out that Vidal's 1973 paper stated the "BCI challenge"[13] of controlling external objects using EEG signals, and especially use of Contingent Negative Variation (CNV) potential as a challenge for BCI control. Vidal's 1977 experiment was the first application of BCI after his 1973 BCI challenge. It was a noninvasive EEG (actually Visual Evoked Potentials (VEP)) control of a cursor-like graphical object on a computer screen. The demonstration was movement in a maze.[14]

1988 was the first demonstration of noninvasive EEG control of a physical object, a robot. The experiment demonstrated EEG control of multiple start-stop-restart cycles of movement, along an arbitrary trajectory defined by a line drawn on a floor. The line-following behavior was the default robot behavior, utilizing autonomous intelligence and an autonomous energy source.[15][16][17][18]

In 1990, a report was given on a closed loop, bidirectional, adaptive BCI controlling a computer buzzer by an anticipatory brain potential, the Contingent Negative Variation (CNV) potential.[19][20] The experiment described how an expectation state of the brain, manifested by CNV, used a feedback loop to control the S2 buzzer in the S1-S2-CNV paradigm. The resulting cognitive wave representing the expectation learning in the brain was termed Electroexpectogram (EXG). The CNV brain potential was part of Vidal's 1973 challenge.

Studies in the 2010s suggested neural stimulation's potential to restore functional connectivity and associated behaviors through modulation of molecular mechanisms.[21][22] This opened the door for the concept that BCI technologies may be able to restore function.

Beginning in 2013, DARPA funded BCI technology through the BRAIN initiative, which supported work out of teams including University of Pittsburgh Medical Center,[23] Paradromics,[24] Brown,[25] and Synchron.[26]

Neuroprosthetics

Neuroprosthetics is an area of

pacemaker
.

The terms are sometimes used interchangeably. Neuroprosthetics and BCIs seek to achieve the same aims, such as restoring sight, hearing, movement, ability to communicate, and even

cognitive function.[1]
Both use similar experimental methods and surgical techniques.

Animal research

Several laboratories have managed to read signals from monkey and rat

computer cursors and commanded robotic arms to perform simple tasks simply by thinking about the task and seeing the results, without motor output.[28] In May 2008 photographs that showed a monkey at the University of Pittsburgh Medical Center operating a robotic arm by thinking were published in multiple studies.[29]
Sheep have also been used to evaluate BCI technology including Synchron's Stentrode.

In 2020, Elon Musk's Neuralink was successfully implanted in a pig.[30] In 2021, Musk announced that the company had successfully enabled a monkey to play video games using Neuralink's device.[31]

Early work

Monkey operating a robotic arm with brain–computer interfacing (Schwartz lab, University of Pittsburgh)

In 1969 operant conditioning studies by Fetz et.al. at the Regional Primate Research Center and Department of Physiology and Biophysics, University of Washington School of Medicine showed that monkeys could learn to control the deflection of a biofeedback arm with neural activity.[32] Similar work in the 1970s established that monkeys could learn to control the firing rates of individual and multiple neurons in the primary motor cortex if they were rewarded accordingly.[33]

neurons, which control movement, date back to the 1970s. In the 1980s, Georgopoulos at Johns Hopkins University found a mathematical relationship between the electrical responses of single motor cortex neurons in rhesus macaque monkeys and the direction in which they moved their arms. He also found that dispersed groups of neurons, in different areas of the monkey's brains, collectively controlled motor commands. He was able to record the firings of neurons in only one area at a time, due to equipment limitations.[34]

Several groups have been able to capture complex brain motor cortex signals by recording from

neural ensembles (groups of neurons) and using these to control external devices.[citation needed
]

Research

Kennedy and Yang Dan

Phillip Kennedy (Neural Signals founder (1987) and colleagues built the first intracortical brain–computer interface by implanting neurotrophic-cone

electrodes into monkeys.[citation needed]

Yang Dan and colleagues' recordings of cat vision using a BCI implanted in the lateral geniculate nucleus (top row: original image; bottom row: recording)

In 1999, Yang Dan et.al. at University of California, Berkeley decoded neuronal firings to reproduce images from cats. The team used an array of electrodes embedded in the thalamus (which integrates the brain's sensory input). Researchers targeted 177 brain cells in the thalamus lateral geniculate nucleus area, which decodes signals from the retina. Neuron firings were recorded from watching eight short movies. Using mathematical filters, the researchers decoded the signals to reconstruct recognizable scenes and moving objects.[35]

Nicolelis

Duke University professor Miguel Nicolelis advocates using multiple electrodes spread over a greater area of the brain to obtain neuronal signals.

After initial studies in rats during the 1990s, Nicolelis and colleagues developed BCIs that decoded brain activity in

owl monkeys
and used the devices to reproduce monkey movements in robotic arms. Monkeys' advanced reaching and grasping abilities and hand manipulation skills, made them good test subjects.

By 2000, the group succeeded in building a BCI that reproduced owl monkey movements while the monkey operated a joystick or reached for food.[36] The BCI operated in real time and could remotely control a separate robot. But the monkeys received no feedback (open-loop BCI).

rhesus monkeys

Later experiments on

rhesus monkeys included feedback and reproduced monkey reaching and grasping movements in a robot arm. Their deeply cleft and furrowed brains made them better models for human neurophysiology than owl monkeys. The monkeys were trained to reach and grasp objects on a computer screen by manipulating a joystick while corresponding movements by a robot arm were hidden.[37][38] The monkeys were later shown the robot and learned to control it by viewing its movements. The BCI used velocity predictions to control reaching movements and simultaneously predicted gripping force
.

In 2011 O'Doherty and colleagues showed a BCI with sensory feedback with rhesus monkeys. The monkey controlled the position of an avatar arm while receiving sensory feedback through direct intracortical stimulation (ICMS) in the arm representation area of the sensory cortex.[39]

Donoghue, Schwartz, and Andersen

BCIs are a core focus of the Carney Institute for Brain Science at Brown University.

Other laboratories that have developed BCIs and algorithms that decode neuron signals include

Caltech
. These researchers produced working BCIs using recorded signals from far fewer neurons than Nicolelis (15–30 neurons versus 50–200 neurons).

The Carney Institute reported training rhesus monkeys to use a BCI to track visual targets on a computer screen (closed-loop BCI) with or without a joystick.[40] The group created a BCI for three-dimensional tracking in virtual reality and reproduced BCI control in a robotic arm.[41] The same group demonstrated that a monkey could feed itself pieces of fruit and marshmallows using a robotic arm controlled by the animal's brain signals.[42][43][44]

Andersen's group used recordings of premovement activity from the posterior parietal cortex, including signals created when experimental animals anticipated receiving a reward.[45]

Other research

In addition to predicting

electromyographic or electrical activity of the muscles of primates are in process.[46]
Such BCIs could restore mobility in paralyzed limbs by electrically stimulating muscles.

Nicolelis and colleagues demonstrated that large neural ensembles can predict arm position. This work allowed BCIs to read arm movement intentions and translate them into actuator movements. Carmena and colleagues[37] programmed a BCI that allowed a monkey to control reaching and grasping movements by a robotic arm. Lebedev and colleagues argued that brain networks reorganize to create a new representation of the robotic appendage in addition to the representation of the animal's own limbs.[38]

In 2019, a study reported a BCI that had the potential to help patients with speech impairment caused by neurological disorders. Their BCI used high-density

anarthric patient who had been unable to speak for over 15 years.[49][50]

The biggest impediment to BCI technology is the lack of a sensor modality that provides safe, accurate and robust access to brain signals. The use of a better sensor expands the range of communication functions that can be provided using a BCI.

Development and implementation of a BCI system is complex and time-consuming. In response to this problem, Gerwin Schalk has been developing BCI2000, a general-purpose system for BCI research, since 2000.[51]

A new 'wireless' approach uses

transfected cells in the somatosensory cortex influenced decision-making in mice.[52]

BCIs led to a deeper understanding of neural networks and the central nervous system. Research has reported that despite neuroscientists' inclination to believe that neurons have the most effect when working together, single neurons can be conditioned through the use of BCIs to fire in a pattern that allows primates to control motor outputs. BCIs led to development of the single neuron insufficiency principle that states that even with a well-tuned firing rate, single neurons can only carry limited information and therefore the highest level of accuracy is achieved by recording ensemble firings. Other principles discovered with BCIs include the neuronal multitasking principle, the neuronal mass principle, the neural degeneracy principle, and the plasticity principle.[53]

BCIs are proposed to be applied by users without disabilities. Passive BCIs allow for assessing and interpreting changes in the user state during Human-Computer Interaction (

HCI). In a secondary, implicit control loop, the system adapts to its user, improving its usability.[54]

BCI systems can potentially be used to encode signals from the periphery. These sensory BCI devices enable real-time, behaviorally-relevant decisions based upon closed-loop neural stimulation.[55]

The BCI Award

The BCI Research Award is awarded annually in recognition of innovative research. Each year, a renowned research laboratory is asked to judge projects. The jury consists of BCI experts recruited by that laboratory. The jury selects twelve nominees, then chooses a first, second, and third-place winner, who receive awards of $3,000, $2,000, and $1,000, respectively.

Human research

Invasive BCIs

Invasive BCI requires surgery to implant electrodes under the scalp for accessing brain signals. The main advantage is to increase accuracy. Downsides include side effects from the surgery, including scar tissue that can obstruct brain signals or the body may not accept the implanted electrodes.[56]

Vision

Invasive BCI research has targeted repairing damaged sight and providing new functionality for people with paralysis. Invasive BCIs are implanted directly into the grey matter of the brain during neurosurgery. Because they lie in the grey matter, invasive devices produce the highest quality signals of BCI devices but are prone to scar-tissue build-up, causing the signal to weaken, or disappear, as the body reacts to the foreign object.[57]

In

phosphenes, the sensation of seeing light. The system included cameras mounted on glasses to send signals to the implant. Initially, the implant allowed Jerry to see shades of grey in a limited field of vision at a low frame-rate. This also required him to be hooked up to a mainframe computer, but shrinking electronics and faster computers made his artificial eye more portable and now enable him to perform simple tasks unassisted.[58]

Dummy unit illustrating the design of a BrainGate interface

In 2002, Jens Naumann, also blinded in adulthood, became the first in a series of 16 paying patients to receive Dobelle's second generation implant, one of the earliest commercial uses of BCIs. The second generation device used a more sophisticated implant enabling better mapping of phosphenes into coherent vision. Phosphenes are spread out across the visual field in what researchers call "the starry-night effect". Immediately after his implant, Jens was able to use his imperfectly restored vision to drive an automobile slowly around the parking area of the research institute.[59] Dobelle died in 2004 before his processes and developments were documented, leaving no one to continue his work.[60] Subsequently, Naumann and the other patients in the program began having problems with their vision, and eventually lost their "sight" again.[61][62]

Movement

BCIs focusing on motor neuroprosthetics aim to restore movement in individuals with paralysis or provide devices to assist them, such as interfaces with computers or robot arms.

Kennedy and Bakay were first to install a human brain implant that produced signals of high enough quality to simulate movement. Their patient, Johnny Ray (1944–2002), developed '

brain aneurysm.[63]

Tetraplegic Matt Nagle became the first person to control an artificial hand using a BCI in 2005 as part of the first nine-month human trial of Cyberkinetics's BrainGate chip-implant. Implanted in Nagle's right precentral gyrus (area of the motor cortex for arm movement), the 96-electrode implant allowed Nagle to control a robotic arm by thinking about moving his hand as well as a computer cursor, lights and TV.[64] One year later, Jonathan Wolpaw received the Altran Foundation for Innovation prize for developing a Brain Computer Interface with electrodes located on the surface of the skull, instead of directly in the brain.[65]

Research teams led by the BrainGate group and another at University of Pittsburgh Medical Center, both in collaborations with the United States Department of Veterans Affairs (VA), demonstrated control of prosthetic limbs with many degrees of freedom using direct connections to arrays of neurons in the motor cortex of tetraplegia patients.[66][67]

Communication

In May 2021, a Stanford University team reported a successful proof-of-concept test that enabled a quadraplegic participant to produce English sentences at about 86 characters per minute and 18 words per minute. The participant imagined moving his hand to write letters, and the system performed handwriting recognition on electrical signals detected in the motor cortex, utilizing

recurrent neural networks.[68][69]

A 2021 study reported that a paralyzed patient was able to communicate 15 words per minute using a brain implant that analyzed vocal tract motor neurons.[70][49]

In a review article, authors wondered whether human information transfer rates can surpass that of language with BCIs. Language research has reported that information transfer rates are relatively constant across many languages. This may reflect the brain's information processing limit. Alternatively, this limit may be intrinsic to language itself, as a modality for information transfer.[71]

In 2023 two studies used BCIs with recurrent neural network to decode speech at a record rate of 62 words per minute and 78 words per minute.[72][73][74]

Technical challenges

There exist a number of technical challenges to recording brain activity with invasive BCIs. Advances in

Hodgkin-Huxley model.[76][77]

Electronic limitations to invasive BCIs have been an active area of research in recent decades. While

foreign-body reaction by means of matching the Young's modulus of the electrode closer to that of brain tissue.[88]

Partially invasive BCIs

Partially invasive BCI devices are implanted inside the skull but rest outside the brain rather than within the grey matter. They produce higher resolution signals than non-invasive BCIs where the bone tissue of the cranium deflects and deforms signals and have a lower risk of forming scar-tissue in the brain than fully invasive BCIs. Preclinical demonstration of intracortical BCIs from the stroke perilesional cortex has been conducted.[90]

Endovascular

A systematic review published in 2020 detailed multiple clinical and non-clinical studies investigating the feasibility of endovascular BCIs.[91]

In 2010, researchers affiliated with University of Melbourne began developing a BCI that could be inserted via the vascular system. Australian neurologist

Thomas Oxley conceived the idea for this BCI, called Stentrode, earning funding from DARPA. Preclinical studies evaluated the technology in sheep.[2]

Stentrode is a monolithic stent electrode array, is designed to be delivered via an intravenous catheter under image-guidance to the superior sagittal sinus, in the region which lies adjacent to the motor cortex.[92] This proximity enables Stentrode to measure neural activity. The procedure is most similar to how venous sinus stents are placed for the treatment of idiopathic intracranial hypertension.[93] Stentrode communicates neural activity to a battery-less telemetry unit implanted in the chest, which communicates wirelessly with an external telemetry unit capable of power and data transfer. While an endovascular BCI benefits from avoiding a craniotomy for insertion, risks such as clotting and venous thrombosis
exist.

Human trials with Stentrode were underway as of 2021.

amyotrophic lateral sclerosis were able to wirelessly control an operating system to text, email, shop, and bank using direct thought using Stentrode,[94] marking the first time a brain-computer interface was implanted via the patient's blood vessels, eliminating the need for brain surgery. In January 2023, researchers reported no serious adverse events during the first year for all four patients, who could use it to operate computers.[95][96]

Electrocorticography

Electrocorticography (ECoG) measures brain electrical activity from beneath the skull in a way similar to non-invasive electroencephalography, using electrodes embedded in a thin plastic pad placed above the cortex, beneath the dura mater.[97] ECoG technologies were first trialled in humans in 2004 by Eric Leuthardt and Daniel Moran from Washington University in St. Louis. In a later trial, the researchers enabled a teenage boy to play Space Invaders.[98] This research indicates that control is rapid, requires minimal training, balancing signal fidelity and level of invasiveness.[note 1]

Signals can be either subdural or epidural, but are not taken from within the brain parenchyma. Patients are required to have invasive monitoring for localization and resection of an epileptogenic focus.[citation needed]

ECoG offers higher spatial resolution, better signal-to-noise ratio, wider frequency range, and less training requirements than scalp-recorded EEG, and at the same time has lower technical difficulty, lower clinical risk, and may have superior long-term stability than intracortical single-neuron recording.[100] This feature profile and evidence of the high level of control with minimal training requirements shows potential for real world application for people with motor disabilities.[101][102]

UCSF reported that ECoG signals could be used to decode speech from epilepsy patients implanted with high-density ECoG arrays over the peri-Sylvian cortices.[103][104] They reported word error rates of 3% (a marked improvement from prior efforts) utilizing an encoder-decoder neural network
, which translated ECoG data into one of fifty sentences composed of 250 unique words.

Non-invasive BCIs

Human experiments have used

interfaces. The majority of published BCI research involves noninvasive EEG-based BCIs. EEG-based technologies and interfaces have been used for the broadest variety of applications. Although EEG-based interfaces are easy to wear and do not require surgery, they have relatively poor spatial resolution and cannot effectively use higher-frequency signals because the skull interferes, dispersing and blurring the electromagnetic waves created by the neurons. EEG-based interfaces also require some time and effort prior to each usage session, while others require no prior-usage training. The choice of a specific BCI for a patient depends on numerous factors.

Functional near-infrared spectroscopy

In 2014 and 2017, a BCI using

amyotrophic lateral sclerosis (ALS) was able to restore basic ability to communicate.[105][106]

Electroencephalography (EEG)-based brain-computer interfaces

electroencephalogram

After Vidal stated the BCI challenge, the initial reports on non-invasive approaches included control of a cursor in 2D using VEP,[107] control of a buzzer using CNV,[108] control of a physical object, a robot, using a brain rhythm (alpha),[109] control of a text written on a screen using P300.[110][111]

In the early days of BCI research, another substantial barrier to using EEG was that extensive training ws required. For example, in experiments beginning in the mid-1990s, Niels Birbaumer at the University of Tübingen in Germany trained paralysed people to self-regulate the slow cortical potentials in their EEG to such an extent that these signals could be used as a binary signal to control a computer cursor. (Birbaumer had earlier trained epileptics to prevent impending fits by controlling this low voltage wave.) The experiment trained ten patients to move a computer cursor. The process was slow, requiring more than an hour for patients to write 100 characters with the cursor, while training often took months. The slow cortical potential approach has fallen away in favor of approaches that require little or no training, are faster and more accurate, and work for a greater proportion of users.[112]

Another research parameter is the type of

New York State University they focused on developing technology that would allow users to choose the brain signals they found easiest to operate a BCI, including mu and beta rhythms.[citation needed
]

A further parameter is the method of feedback used as shown in studies of

P300 signals. Patterns of P300 waves are generated involuntarily (stimulus-feedback) when people see something they recognize and may allow BCIs to decode categories of thoughts without training.[citation needed
]

A 2005 study reported EEG emulation of digital control circuits, using a CNV flip-flop.

Advances by

hemodynamic signals.[117] Refined by a neuroimaging approach and a training protocol, They fashioned a non-invasive EEG based brain-computer interface to control the flight of a virtual helicopter in 3-dimensional space, based upon motor imagination.[118] In June 2013 they announced a technique to guide a remote-control helicopter through an obstacle course.[119] They also solved the EEG inverse problem and then used the resulting virtual EEG for BCI tasks. Well-controlled studies suggested the merits of such a source analysis-based BCI.[120]

A 2014 study reported that severely motor-impaired patients could communicate faster and more reliably with non-invasive EEG BCI than with muscle-based communication channels.[121]

A 2019 study reported that the application of evolutionary algorithms could improve EEG mental state classification with a non-invasive Muse device, enabling classification of data acquired by a consumer-grade sensing device.[122]

In a 2021 systematic review of

randomized controlled trials using BCI for post-stroke upper-limb rehabilitation, EEG-based BCI was reported to have efficacy in improving upper-limb motor function compared to control therapies. More specifically, BCI studies that utilized band power features, motor imagery, and functional electrical stimulation were reported to be more effective than alternatives.[123] Another 2021 systematic review focused on post-stroke robot-assisted EEG-based BCI for hand rehabilitation. Improvement in motor assessment scores was observed in three of eleven studies.[124]

Dry active electrode arrays

In the early 1990s Babak Taheri, at University of California, Davis demonstrated the first single and multichannel dry active electrode arrays.[125] The arrayed electrode was demonstrated to perform well compared to silver/silver chloride electrodes. The device consisted of four sensor sites with integrated electronics to reduce noise by impedance matching. The advantages of such electrodes are:

  • no electrolyte used,
  • no skin preparation,
  • significantly reduced sensor size,
  • compatibility with EEG monitoring systems.

The active electrode array is an integrated system containing an array of capacitive sensors with local integrated circuitry packaged with batteries to power the circuitry. This level of integration was required to achieve the result.

The electrode was tested on a test bench and on human subjects in four modalities, namely:

  • spontaneous EEG,
  • sensory event-related potentials,
  • brain stem potentials,
  • cognitive event-related potentials.

Performance compared favorably with that of standard wet electrodes in terms of skin preparation, no gel requirements (dry), and higher signal-to-noise ratio.[126]

In 1999 Hunter Peckham and others at

quadriplegic. As he concentrated on simple but opposite concepts like up and down. A basic pattern was identified in his beta-rhythm EEG output and used to control a switch: Above average activity was interpreted as on, below average off. The signals were also used to drive nerve controllers embedded in his hands, restoring some movement.[127]

SSVEP mobile EEG BCIs

In 2009, the NCTU Brain-Computer-Interface-headband was reported. Those researchers also engineered silicon-based

microelectro-mechanical system (MEMS) dry electrodes designed for application to non-hairy body sites. These electrodes were secured to the headband's DAQ board with snap-on electrode holders. The signal processing module measured alpha activity and transferred it over Bluetooth to a phone that assessed the patients' alertness and cognitive capacity. When the subject became drowsy, the phone sent arousing feedback to the operator to rouse them.[128]

In 2011, researchers reported a cellular based BCI that could cause phone to ring. The wearable system was composed of a four channel bio-signal acquisition/amplification module, a communication module, and a Bluetooth phone. The electrodes were placed to pick up steady state visual evoked potentials (SSVEPs).[129] SSVEPs are electrical responses to flickering visual stimuli with repetition rates over 6 Hz[129] that are best found in the parietal and occipital scalp regions of the visual cortex.[130][131][132] It was reported that all study participants were able to initiate the phone call with minimal practice in natural environments.[133]

The scientists reported that a single channel

canonical correlation analysis (CCA) algorithm can support mobile BCIs.[129][134] The CCA algorithm has been applied in experiments investigating BCIs with claimed high accuracy and speed.[135] Cellular BCI technology can reportedly be translated for other applications, such as picking up sensorimotor mu/beta rhythms to function as a motor-imagery based BCI.[129]

In 2013, comparative tests performed on Android cell phone, tablet, and computer based BCIs, analyzed the power spectrum density of resultant EEG SSVEPs. The stated goals of this study were to "increase the practicability, portability, and ubiquity of an SSVEP-based BCI, for daily use". It was reported that the stimulation frequency on all mediums was accurate, although the phone's signal was not stable. The amplitudes of the SSVEPs for the laptop and tablet were reported to be larger than those of the cell phone. These two qualitative characterizations were suggested as indicators of the feasibility of using a mobile stimulus BCI.[134]

One of the difficulties with EEG readings is susceptibility to motion artifacts.

fMRI
fusion.

Prosthesis and environment control

Non-invasive BCIs have been applied to prosthetic upper and lower extremity devices in people with paralysis. For example, Gert Pfurtscheller of

orthosis to regain basic ambulation.[139][140] In 2009 independent researcher Alex Blainey used the Emotiv EPOC to control a 5 axis robot arm.[141] He made several demonstrations of mind controlled wheelchairs and home automation
.

Magnetoencephalography and fMRI

ATR Labs' reconstruction of human vision using fMRI (top row: original image; bottom row: reconstruction from mean of combined readings)

Magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) have both been used as non-invasive BCIs.[142] In a widely reported experiment, fMRI allowed two users to play Pong in real-time by altering their haemodynamic response or brain blood flow through biofeedback.[143]

fMRI measurements of haemodynamic responses in real time have also been used to control robot arms with a seven-second delay between thought and movement.[144]

In 2008 research developed in the Advanced Telecommunications Research (ATR)

pixels.[145]

A 2011 study reported second-by-second reconstruction of videos watched by the study's subjects, from fMRI data.[146] This was achieved by creating a statistical model relating videos to brain activity. This model was then used to look up 100 one-second video segments, in a database of 18 million seconds of random YouTube videos, matching visual patterns to brain activity recorded when subjects watched a video. These 100 one-second video extracts were then combined into a mash-up image that resembled the video.[147][148][149]

BCI control strategies in neurogaming

Motor imagery

Bio/neurofeedback for passive BCI designs

Biofeedback can be used to monitor a subject's mental relaxation. In some cases, biofeedback does not match EEG, while parameters such as

galvanic skin resistance (GSR), and heart rate variability (HRV) can do so. Many biofeedback systems treat disorders such as attention deficit hyperactivity disorder (ADHD), sleep problems in children, teeth grinding, and chronic pain. EEG biofeedback systems typically monitor four brainwave bands (theta: 4–7 Hz, alpha:8–12 Hz, SMR: 12–15 Hz, beta: 15–18 Hz) and challenge the subject to control them. Passive BCI uses BCI to enrich human–machine interaction with information on the user's mental state, for example, simulations that detect when users intend to push brakes during emergency vehicle braking.[54] Game developers using passive BCIs understand that through repetition of game levels the user's cognitive state adapts. During the first play of a given level, the player reacts differently than during subsequent plays: for example, the user is less surprised by an event that they expect.[150]

Visual evoked potential (VEP)

A VEP is an electrical potential recorded after a subject is presented with a visual stimuli. The types of VEPs include SSVEPs and P300 potential.

Steady-state visually evoked potentials (SSVEPs) use potentials generated by exciting the retina, using visual stimuli modulated at certain frequencies. SSVEP stimuli are often formed from alternating checkerboard patterns and at times use flashing images. The frequency of the phase reversal of the stimulus used can be distinguished by EEG; this makes detection of SSVEP stimuli relatively easy. SSVEP is used within many BCI systems. This is due to several factors. The signal elicited is measurable in as large a population as the transient VEP and blink movement. Electrocardiographic artefacts do not affect the frequencies monitored. The SSVEP signal is robust; the topographic organization of the primary visual cortex is such that a broader area obtains afferents from the visual field's central or fovial region. SSVEP comes with problems. As SSVEPs use flashing stimuli to infer user intent, the user must gaze at one of the flashing or iterating symbols in order to interact with the system. It is, therefore, likely that the symbols become irritating and uncomfortable during longer play sessions.

Another type of VEP is the P300 potential. This potential is a positive peak in the EEG that occurs roughly 300 ms after the appearance of a target stimulus (a stimulus for which the user is waiting or seeking) or oddball stimuli. P300 amplitude decreases as the target stimuli and the ignored stimuli grow more similar. P300 is thought to be related to a higher level attention process or an orienting response. Using P300 requires fewer training sessions. The first application to use it was the P300 matrix. Within this system, a subject chooses a letter from a 6 by 6 grid of letters and numbers. The rows and columns of the grid flashed sequentially and every time the selected "choice letter" was illuminated the user's P300 was (potentially) elicited. However, the communication process, at approximately 17 characters per minute, was slow. P300 offers a discrete selection rather than continuous control. The advantage of P300 within games is that the player does not have to learn how to use a new control system, requiring only short training instances to learn gameplay mechanics and the basic BCI paradigm.[150]

Non-brain-based human–computer interface (physiological computing)

Human-computer interaction can exploit other recording modalities, such as electrooculography and eye-tracking. These modalities do not record brain activity and therefore do not qualify as BCIs.[153]

Electrooculography (EOG)

In 1989, a study reported control of a mobile robot by eye movement using electrooculography signals. A mobile robot was driven to a goal point using five EOG commands, interpreted as forward, backward, left, right, and stop.[154]

Pupil-size oscillation

A 2016 article described a new non-EEG-based HCI that required no

visual fixation, or ability to move the eyes.[155] The interface is based on covert interest
; directing attention to a chosen letter on a virtual keyboard, without the need to look directly at the letter. Each letter has its own (background) circle which micro-oscillates in brightness differently from the others. Letter selection is based on best fit between unintentional pupil-size oscillation and the background circle's brightness oscillation pattern. Accuracy is additionally improved by the user's mental rehearsal of the words 'bright' and 'dark' in synchrony with the brightness transitions of the letter's circle.

Brain-to-brain communication

In the 1960s a researcher after training used EEG to create Morse code using alpha waves.[156] On 27 February 2013 Miguel Nicolelis's group at Duke University and IINN-ELS connected the brains of two rats, allowing them to share information, in the first-ever direct brain-to-brain interface.[157][158][159]

Gerwin Schalk reported that ECoG signals can discriminate vowels and consonants embedded in spoken and imagined words, shedding light on the mechanisms associated with their production and could provide a basis for brain-based communication using imagined speech.[102][160]

In 2002 Kevin Warwick had an array of 100 electrodes fired into his nervous system in order to link his nervous system to the Internet. Warwick carried out a series of experiments. Electrodes were implanted into his wife's nervous system, allowing them to conduct the first direct electronic communication experiment between the nervous systems of two humans.[161][162][163][164]

Other researchers achieved brain-to-brain communication between at a distance using non-invasive technology attached to the participants' scalps. The words were encoded in binary streams by the cognitive motor input of the person sending the information. Pseudo-random bits of the information carried encoded words "hola" ("hi" in Spanish) and "ciao" ("goodbye" in Italian) and were transmitted mind-to-mind.[165]

Cell-culture BCIs

Researchers have built devices to interface with neural cells and entire neural networks in vitro. Experiments on cultured neural tissue focused on building problem-solving networks, constructing basic computers and manipulating robotic devices. Research into techniques for stimulating and recording individual neurons grown on semiconductor chips is neuroelectronics or neurochips.[166]

Development of the first neurochip was claimed by a Caltech team led by Jerome Pine and Michael Maher in 1997.[167] The Caltech chip had room for 16 neurons.

In 2003 a team led by Theodore Berger, at the University of Southern California, worked on a neurochip designed to function as an artificial or prosthetic hippocampus. The neurochip was designed for rat brains. The hippocampus was chosen because it is thought to be the most structured and most studied part of the brain. Its function is to encode experiences for storage as long-term memories elsewhere in the brain.[168]

In 2004 Thomas DeMarse at the

aircraft simulator. After collection, the cortical neurons were cultured in a petri dish and reconnected themselves to form a living neural network. The cells were arranged over a grid of 60 electrodes and used to control the pitch and yaw functions of the simulator. The study's focus was on understanding how the human brain performs and learns computational tasks at a cellular level.[169]

Collaborative BCIs

The idea of combining/integrating brain signals from multiple individuals was introduced at Humanity+ @Caltech, in December 2010, by Adrian Stoica, who referred to the concept as multi-brain aggregation.[170][171][172] A patent was applied for in 2012.[173][174][175] Stoica's first paper on the topic appeared in 2012, after the publication of his patent application.[176]

Ethical considerations

BCIs present significant ethical questions, including concerns about privacy, autonomy, consent, and the consequences of merging human cognition with external devices. Exploring these ethical considerations highlights the complex interplay between advancing technology and preserving fundamental human rights and values. The concerns can be broadly categorized into user-centric issues and legal and social issues.

Concerns center on the safety and long-term effects on users. These include obtaining informed consent from individuals with communication difficulties, the impact on patients' and families' quality of life, health-related side effects, misuse of therapeutic applications, safety risks, and the non-reversible nature of some BCI-induced changes. Additionally, questions arise about access to maintenance, repair, and spare parts, particularly in the event of a company's bankruptcy[177]

The legal and social aspects of BCIs complicate mainstream adoption. Concerns include issues of accountability and responsibility, such as claims that BCI influence overrides free will and control over actions, inaccurate translation of cognitive intentions, personality changes resulting from deep-brain stimulation, and the blurring of the line between human and machine.[178] Other concerns involve the use of BCIs in advanced interrogation techniques, unauthorized access ("brain hacking"),[179] social stratification through selective enhancement, privacy issues related to mind-reading, tracking and "tagging" systems, and the potential for mind, movement, and emotion control.[180] Researchers have also theorized that BCIs could exacerbate existing social inequalities.

In their current form, most BCIs are more akin to corrective therapies that engage few of such ethical issues. Bioethics is well-equipped to address the challenges posed by BCI technologies, with Clausen suggesting in 2009 that "BCIs pose ethical challenges, but these are conceptually similar to those that bioethicists have addressed for other realms of therapy."[181] Haselager and colleagues highlighted the importance of managing expectations and value.[182] Standard protocols can ensure ethically sound informed-consent procedures for locked-in patients.

The evolution of BCIs mirrors that of pharmaceutical science, which began as a means to address impairments and now enhances focus and reduces the need for sleep. As BCIs progress from therapies to enhancements, the BCI community is working to create consensus on ethical guidelines for research, development, and dissemination.[183][184] Ensuring equitable access to BCIs will be crucial in preventing generational inequalities that could hinder the right to human flourishing.

Low-cost systems

Various companies are developing inexpensive BCIs for research and entertainment. Toys such as the NeuroSky and Mattel MindFlex have seen some commercial success.

  • In 2006, Sony patented a neural interface system allowing radio waves to affect signals in the neural cortex.[185]
  • In 2007, NeuroSky released the first affordable consumer based EEG along with the game NeuroBoy. It was the first large scale EEG device to use dry sensor technology.[186]
  • In 2008,
    OCZ Technology developed a device for use in video games relying primarily on electromyography.[187]
  • In 2008, Final Fantasy developer Square Enix announced that it was partnering with NeuroSky to create Judecca, a game.[188][189]
  • In 2009, Mattel partnered with NeuroSky to release Mindflex, a game that used an EEG to steer a ball through an obstacle course. It was by far the best selling consumer based EEG at the time.[188][190]
  • In 2009,
    Uncle Milton Industries partnered with NeuroSky to release the Star Wars Force Trainer, a game designed to create the illusion of possessing the Force.[188][191]
  • In 2009, Emotiv released the EPOC, a 14 channel EEG device that can read 4 mental states, 13 conscious states, facial expressions, and head movements. The EPOC was the first commercial BCI to use dry sensor technology, which can be dampened with a saline solution for a better connection.[192]
  • In November 2011, Time magazine selected "necomimi" produced by Neurowear as one of the year's best inventions.[193]
  • In February 2014, They Shall Walk (a nonprofit organization fixed on constructing exoskeletons, dubbed LIFESUITs, for paraplegics and quadriplegics) began a partnership with James W. Shakarji on the development of a wireless BCI.[194]
  • In 2016, a group of hobbyists developed an open-source BCI board that sends neural signals to the audio jack of a smartphone, dropping the cost of entry-level BCI to £20.[195] Basic diagnostic software is available for Android devices, as well as a text entry app for Unity.[196]
  • In 2020, NextMind released a dev kit including an EEG headset with dry electrodes at $399.[197][198] The device can run various visual-BCI demonstration applications or developers can create their own. It was later acquired by Snap Inc. in 2022.[199]

Future directions

Brain-computer interface

A consortium of 12 European partners completed a roadmap to support the European Commission in their funding decisions for the

Horizon 2020 framework program. The project was funded by the European Commission. It started in November 2013 and published a roadmap in April 2015.[200] A 2015 publication describes this project, as well as the Brain-Computer Interface Society.[201]
It reviewed work within this project that further defined BCIs and applications, explored recent trends, discussed ethical issues, and evaluated directions for new BCIs.

Other recent publications too have explored future BCI directions for new groups of disabled users.[10][202]

Disorders of consciousness (DOC)

Some people have a

disorder of consciousness (DOC). This state is defined to include people in a coma and those in a vegetative state (VS) or minimally conscious state (MCS). BCI research seeks to address DOC. A key initial goal is to identify patients who can perform basic cognitive tasks, which would change their diagnosis, and allow them to make important decisions (such as whether to seek therapy, where to live, and their views on end-of-life decisions regarding them). Patients incorrectly diagnosed may die as a result of end-of-life decisions made by others. The prospect of using BCI to communicate with such patients is a tantalizing prospect.[203][204]

Many such patients cannot use BCIs based on vision. Hence, tools must rely on auditory and/or vibrotactile stimuli. Patients may wear headphones and/or vibrotactile stimulators placed on responsive body parts. Another challenge is that patients may be able to communicate only at unpredictable intervals. Home devices can allow communications when the patient is ready.

Automated tools can ask questions that patients can easily answer, such as "Is your father named George?" or "Were you born in the USA?" Automated instructions inform patients how to coney yes or no, for example by focusing their attention on stimuli on the right vs. left wrist. This focused attention produces reliable changes in EEG patterns that can help determine whether the patient is able to communicate.[205][206][207]

Motor recovery

People may lose some of their ability to move due to many causes, such as stroke or injury. Research in recent years has demonstrated the utility of EEG-based BCI systems in aiding motor recovery and neurorehabilitation in patients who have had a stroke.[208][209][210][211] Several groups have explored systems and methods for motor recovery that include BCIs.[212][213][214][215] In this approach, a BCI measures motor activity while the patient imagines or attempts movements as directed by a therapist. The BCI may provide two benefits: (1) if the BCI indicates that a patient is not imagining a movement correctly (non-compliance), then the BCI could inform the patient and therapist; and (2) rewarding feedback such as functional stimulation or the movement of a virtual avatar also depends on the patient's correct movement imagery.

So far, BCIs for motor recovery have relied on the EEG to measure the patient's motor imagery. However, studies have also used fMRI to study different changes in the brain as persons undergo BCI-based stroke rehab training.[216][217][218] Imaging studies combined with EEG-based BCI systems hold promise for investigating neuroplasticity during motor recovery post-stroke.[218] Future systems might include the fMRI and other measures for real-time control, such as functional near-infrared, probably in tandem with EEGs. Non-invasive brain stimulation has also been explored in combination with BCIs for motor recovery.[219] In 2016, scientists out of the University of Melbourne published preclinical proof-of-concept data related to a potential brain-computer interface technology platform being developed for patients with paralysis to facilitate control of external devices such as robotic limbs, computers and exoskeletons by translating brain activity.[220][221][222]

Functional brain mapping

In 2014, some 400,000 people underwent brain mapping during neurosurgery. This procedure is often required for people who do not respond to medication.[223] During this procedure, electrodes are placed on the brain to precisely identify the locations of structures and functional areas. Patients may be awake during neurosurgery and asked to perform tasks, such as moving fingers or repeating words. This is necessary so that surgeons can remove the desired tissue while sparing other regions. Removing too much brain tissue can cause permanent damage, while removing too little can mandate additional neurosurgery.[citation needed]

Researchers explored ways to improve neurosurgical mapping. This work focuses largely on high gamma activity, which is difficult to detect non-invasively. Results improved methods for identifying key functional areas.[224]

Flexible devices

microelectromechanical systems (MEMS).[citation needed
]

Flexible neural interfaces may minimize brain tissue trauma related to mechanical mismatch between electrode and tissue.[227]

Neural dust

Neural dust is millimeter-sized devices operated as wirelessly powered nerve sensors that were proposed in a 2011 paper from the University of California, Berkeley Wireless Research Center.[228][229] In one model, local field potentials could be distinguished from action potential "spikes", which would offer greatly diversified data vs conventional techniques.[228]

See also

Notes

  1. ^ These electrodes had not been implanted in the patient with the intention of developing a BCI. The patient had had severe epilepsy and the electrodes were temporarily implanted to help his physicians localize seizure foci; the BCI researchers simply took advantage of this.[99]

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Further reading

External links