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1.  Single-Cell Responses to Face Adaptation in the Human Medial Temporal Lobe 
Neuron  2014;84(2):363-369.
Summary
We used a face adaptation paradigm to bias the perception of ambiguous images of faces and study how single neurons in the human medial temporal lobe (MTL) respond to the same images eliciting different percepts. The ambiguous images were morphs between the faces of two familiar individuals, chosen because at least one MTL neuron responded selectively to one but not to the other face. We found that the firing of MTL neurons closely followed the subjects’ perceptual decisions—i.e., recognizing one person or the other. In most cases, the response to the ambiguous images was similar to the one obtained when showing the pictures without morphing. Altogether, these results show that many neurons in the medial temporal lobe signal the subjects’ perceptual decisions rather than the visual features of the stimulus.
Highlights
•We used a face adaptation paradigm to bias the perception of ambiguous images•Neurons in the human MTL fired according to the subjects’ perceptual decisions•In most cases, ambiguous images triggered similar responses as the original pictures•MTL neurons follow subjective perception rather than visual inputs
Using an adaptation paradigm to bias the perception of morphed faces, Quian Quiroga et al. show how single neurons in the human medial temporal lobe follow the subjective perception by the subjects rather than the visual features of the stimulus.
doi:10.1016/j.neuron.2014.09.006
PMCID: PMC4210637  PMID: 25263754
2.  Coding of Information in the Phase of Local Field Potentials within Human Medial Temporal Lobe 
Neuron  2013;79(3):10.1016/j.neuron.2013.06.001.
Summary
There is increasing evidence that the phase of ongoing oscillations plays a role in neural coding, but its relative importance throughout the brain has yet to be understood. We assessed single-trial phase coding in four temporal lobe and four frontal lobe regions of the human brain using local field potentials (LFPs) recorded during a card-matching task. In the temporal lobe, classification of correct/incorrect matches based on LFP phase was significantly better than classification based on amplitude and comparable to the full LFP signal. Surprisingly, in these regions, the correct/incorrect mean phases became aligned to one another before they diverged and coded for trial outcome. Neural responses in the amygdala were consistent with a mechanism of phase resetting, while parahippocampal gyrus activity was indicative of evoked potentials. These findings highlight the importance of phase coding in human MTL and suggest that different brain regions may represent information in diverse ways.
doi:10.1016/j.neuron.2013.06.001
PMCID: PMC3835725  PMID: 23932002
3.  Timing of Single-Neuron and Local Field Potential Responses in the Human Medial Temporal Lobe 
Current biology : CB  2014;24(3):299-304.
Summary
The relationship between the firing of single cells and local field potentials (LFPs) has received increasing attention, with studies in animals [1-11] and humans [12-14]. Recordings in the human medial temporal lobe (MTL) have demonstrated the existence of neurons with selective and invariant responses [15], with a relatively late but precise response onset around 300 ms after stimulus presentation [16-18] and firing only upon conscious recognition of the stimulus [19]. This represents a much later onset than expected from direct projections from inferotemporal cortex [16, 18]. The neural mechanisms underlying this onset remain unclear. To address this issue, we performed a joint analysis of single-cell and LFP responses during a visual recognition task. Single-neuron responses were preceded by a global LFP deflection in the theta range. In addition, there was a local and stimulus-specific increase in the single-trial gamma power. These LFP responses correlated with conscious recognition. The timing of the neurons’ firing was phase locked to these LFP responses. We propose that whereas the gamma phase locking reflects the activation of local networks encoding particular recognized stimuli, the theta phase locking reflects a global activation that provides a temporal window for processing consciously perceived stimuli in the MTL.
doi:10.1016/j.cub.2013.12.004
PMCID: PMC3963414  PMID: 24462002
4.  Direct recordings of grid-like neuronal activity in human spatial navigation 
Nature neuroscience  2013;16(9):1188-1190.
Grid cells in the entorhinal cortex appear to represent spatial location via a triangular coordinate system. Such cells, which have been identified in rats, bats, and monkeys, are believed to support a wide range of spatial behaviors. By recording neuronal activity from neurosurgical patients performing a virtual-navigation task we identified cells exhibiting grid-like spiking patterns in the human brain, suggesting that humans and simpler animals rely on homologous spatial-coding schemes.
doi:10.1038/nn.3466
PMCID: PMC3767317  PMID: 23912946
5.  Timing of Single-Neuron and Local Field Potential Responses in the Human Medial Temporal Lobe 
Current Biology  2014;24(3):299-304.
Summary
The relationship between the firing of single cells and local field potentials (LFPs) has received increasing attention, with studies in animals [1–11] and humans [12–14]. Recordings in the human medial temporal lobe (MTL) have demonstrated the existence of neurons with selective and invariant responses [15], with a relatively late but precise response onset around 300 ms after stimulus presentation [16–18] and firing only upon conscious recognition of the stimulus [19]. This represents a much later onset than expected from direct projections from inferotemporal cortex [16, 18]. The neural mechanisms underlying this onset remain unclear. To address this issue, we performed a joint analysis of single-cell and LFP responses during a visual recognition task. Single-neuron responses were preceded by a global LFP deflection in the theta range. In addition, there was a local and stimulus-specific increase in the single-trial gamma power. These LFP responses correlated with conscious recognition. The timing of the neurons’ firing was phase locked to these LFP responses. We propose that whereas the gamma phase locking reflects the activation of local networks encoding particular recognized stimuli, the theta phase locking reflects a global activation that provides a temporal window for processing consciously perceived stimuli in the MTL.
Highlights
•Global theta LFP increases immediately precede MTL single-cell responses•Gamma power reflects activations of local networks encoding specific stimuli•The timing of the neurons’ firing is phase locked to LFP responses•LFP responses give a temporal window for processing consciously perceived stimuli
Rey et al. show that, in human medial temporal lobe (MTL), single-cell responses triggered by consciously perceived stimuli are locked to global theta and local gamma LFP responses; the latter reflects local activations, but the former shortly precedes the spike responses and may provide a window for stimulus processing in the MTL.
doi:10.1016/j.cub.2013.12.004
PMCID: PMC3963414  PMID: 24462002
6.  Human hypocretin and melanin concentrating hormone levels are linked to emotion and social interaction 
Nature communications  2013;4:1547.
The neurochemical changes underlying human emotions and social behavior are largely unknown. Here we report on the changes in the levels of two hypothalamic neuropeptides, hypocretin-1 (Hcrt-1) and melanin concentrating hormone (MCH), measured in the human amygdala. We show that Hcrt-1 levels are maximal during positive emotion, social interaction, and anger, behaviors that induce cataplexy in human narcoleptics. In contrast, MCH levels are minimal during social interaction, but are increased after eating. Both peptides are at minimal levels during periods of postoperative pain despite high levels of arousal. MCH levels increase at sleep onset, consistent with a role in sleep induction, whereas Hcrt-1 levels increase at wake onset, consistent with a role in wake induction. Levels of these two peptides in humans are not simply linked to arousal, but rather to specific emotions and state transitions. Other arousal systems may be similarly emotionally specialized.
doi:10.1038/ncomms2461
PMCID: PMC3595130  PMID: 23462990
7.  Ensembles of human MTL neurons “jump back in time” in response to a repeated stimulus 
Hippocampus  2012;22(9):1833-1847.
Episodic memory, which depends critically on the integrity of the medial temporal lobe (MTL), has been described as “mental time travel” in which the rememberer “jumps back in time.” The neural mechanism underlying this ability remains elusive. Mathematical and computational models of performance in episodic memory tasks provide a specific hypothesis regarding the computation that supports such a jump back in time. The models suggest that a representation of temporal context, a representation that changes gradually over macroscopic periods of time, is the cue for episodic recall. According to these models, a jump back in time corresponds to a stimulus recovering a prior state of temporal context. In vivo single-neuron recordings were taken from the human MTL while epilepsy patients distinguished novel from repeated images in a continuous recognition memory task. The firing pattern of the ensemble of MTL neurons showed robust temporal autocorrelation over macroscopic periods of time during performance of the memory task. The gradually-changing part of the ensemble state was causally affected by the visual stimulus being presented. Critically, repetition of a stimulus caused the ensemble to elicit a pattern of activity that resembled the pattern of activity present before the initial presentation of the stimulus. These findings confirm a direct prediction of this class of temporal context models and may be a signature of the mechanism that underlies the experience of episodic memory as mental time travel.
doi:10.1002/hipo.22018
PMCID: PMC3407826  PMID: 22488671
8.  Improved P300 speller performance using electrocorticography, spectral features, and natural language processing 
Objective
The P300 speller is a system designed to restore communication to patients with advanced neuromuscular disorders. This study was designed to explore the potential improvement from using electrocorticography (ECoG) compared to the more traditional usage of electroencephalography (EEG).
Methods
We tested the P300 speller on two epilepsy patients with temporary subdural electrode arrays over the occipital and temporal lobes respectively. We then performed offline analysis to determine the accuracy and bit rate of the system and integrated spectral features into the classifier and used a natural language processing (NLP) algorithm to further improve the results.
Results
The subject with the occipital grid achieved an accuracy of 82.77% and a bit rate of 41.02, which improved to 96.31% and 49.47 respectively using a language model and spectral features. The temporal grid patient achieved an accuracy of 59.03% and a bit rate of 18.26 with an improvement to 75.81% and 27.05 respectively using a language model and spectral features. Spatial analysis of the individual electrodes showed best performance using signals generated and recorded near the occipital pole.
Conclusions
Using ECoG and integrating language information and spectral features can improve the bit rate of a P300 speller system. This improvement is sensitive to the electrode placement and likely depends on visually evoked potentials.
Significance
This study shows that there can be an improvement in BCI performance when using ECoG, but that it is sensitive to the electrode location.
doi:10.1016/j.clinph.2013.02.002
PMCID: PMC3679217  PMID: 23465430
brain-computer interface; electrocorticography; event-related potential; P300; speller; natural language processing
9.  Contrasting Roles of Neural Firing Rate and Local Field Potentials in Human Memory 
Hippocampus  2007;17(8):606-617.
Recording the activity of neurons is a mainstay of animal memory research, while human recordings are generally limited to the activity of large ensembles of cells. The relationship between ensemble activity and neural firing rate during declarative memory processes, however, remains unclear. We recorded neurons and local field potentials (LFPs) simultaneously from the same sites in the human hippocampus and entorhinal cortex (ERC) in patients with implanted intracranial electrodes during a virtual taxi-driver task that also included a memory retrieval component. Neurons increased their firing rate in response to specific passengers or landmarks both during navigation and retrieval. Although we did not find item specificity in the broadband LFP, both θ- and γ-band LFPs increased power to specific items on a small but significant percent of channels. These responses, however, did not correlate with item-specific neural responses. To contrast item-specific responses with process-specific responses during memory, we compared neural and LFP responses during encoding (navigation) and retrieval (associative and item-specific recognition). A subset of neurons also altered firing rates nonspecifically while subjects viewed items during encoding. Interestingly, LFPs in the hippocampus and ERC increased in power nonspecifically while subjects viewed items during retrieval, more often during associative than item-recognition. Furthermore, we found no correlation between neural firing rate and broadband, θ-band, and γ-band LFPs during process-specific responses. Our findings suggest that neuronal firing and ensemble activity can be dissociated during encoding, item-maintenance, and retrieval in the human hippocampal area, likely relating to functional properties unique to this region.
doi:10.1002/hipo.20300
PMCID: PMC3568989  PMID: 17546683
hippocampus; depth electrode; local field potentials; single neuron; human memory; declarative memory
10.  Gray matter loss correlates with mesial temporal lobe neuronal hyperexcitability inside the human seizure onset zone 
Epilepsia  2011;53(1):25-34.
Summary
Purpose
Patient studies have not provided consistent evidence for interictal neuronal hyperexcitability inside the seizure onset zone (SOZ). We hypothesized that gray matter (GM) loss could have important effects on neuronal firing, and quantifying these effects would reveal significant differences in neuronal firing inside versus outside the SOZ.
Methods
MRI and computational unfolding of mesial temporal lobe (MTL) subregions was used to construct anatomical maps to compute GM loss in presurgical patients with medically intractable focal seizures in relation to control subjects. In patients, these same maps were used to locate the position of microelectrodes that recorded interictal neuronal activity. Single neuron firing and burst rates were evaluated in relation to GM loss and MTL subregions inside and outside the SOZ.
Key findings
MTL GM thickness was reduced inside and outside the SOZ in patients with respect to control subjects, yet GM loss was associated more strongly with firing and burst rates in several MTL subregions inside the SOZ. Adjusting single neuron firing and burst rates for the effects of GM loss revealed significantly higher firing rates in the subregion consisting of dentate gyrus and CA2 and CA3 (CA23DG), as well as CA1 and entorhinal cortex (EC) inside versus outside the SOZ where normalized MRI GM loss was ≥1.40 mm. Firing rates were higher in subicular cortex inside the SOZ at GM loss ≥1.97 mm, while burst rates were higher in CA23DG, CA1, and EC inside than outside the SOZ at similar levels of GM loss.
Significance
The correlation between GM loss and increased firing and burst rates suggests GM structural alterations in MTL subregions are associated with interictal neuronal hyperexcitability inside the SOZ. Significant differences in firing rates and bursting in areas with GM loss inside compared to outside the SOZ indicate that synaptic reorganization following cell loss could be associated with varying degrees of epileptogenicity in patients with intractable focal seizures.
doi:10.1111/j.1528-1167.2011.03333.x
PMCID: PMC3253228  PMID: 22126325
epilepsy; atrophy; interictal; hippocampus; MRI; microelectrode; single neuron
11.  A category-specific response to animals in the right human amygdala 
Nature neuroscience  2011;14(10):1247-1249.
The amygdala is important in emotion, but it remains unknown whether it is specialized for certain stimulus categories. We analyzed responses recorded from 489 single neurons in the amygdalae of 41 neurosurgical patients and found a categorical selectivity for pictures of animals in the right amygdala. This selectivity appeared to be independent of emotional valence or arousal and may reflect the importance that animals held throughout our evolutionary past.
doi:10.1038/nn.2899
PMCID: PMC3505687  PMID: 21874014
12.  Memory Enhancement and Deep-Brain Stimulation of the Entorhinal Area 
The New England journal of medicine  2012;366(6):502-510.
BACKGROUND
The medial temporal structures, including the hippocampus and the entorhinal cortex, are critical for the ability to transform daily experience into lasting memories. We tested the hypothesis that deep-brain stimulation of the hippocampus or entorhinal cortex alters memory performance.
METHODS
We implanted intracranial depth electrodes in seven subjects to identify seizure-onset zones for subsequent epilepsy surgery. The subjects completed a spatial learning task during which they learned destinations within virtual environments. During half the learning trials, focal electrical stimulation was given below the threshold that elicits an afterdischarge (i.e., a neuronal discharge that occurs after termination of the stimulus).
RESULTS
Entorhinal stimulation applied while the subjects learned locations of landmarks enhanced their subsequent memory of these locations: the subjects reached these landmarks more quickly and by shorter routes, as compared with locations learned without stimulation. Entorhinal stimulation also resulted in a resetting of the phase of the theta rhythm, as shown on the hippocampal electroencephalogram. Direct hippocampal stimulation was not effective. In this small series, no adverse events associated with the procedure were observed.
CONCLUSIONS
Stimulation of the entorhinal region enhanced memory of spatial information when applied during learning. (Funded by the National Institutes of Health and the Dana Foundation.)
doi:10.1056/NEJMoa1107212
PMCID: PMC3447081  PMID: 22316444
13.  Sleep spindles in humans: insights from intracranial EEG and unit recordings 
The Journal of Neuroscience  2011;31(49):17821-17834.
Sleep spindles are an electroencephalographic (EEG) hallmark of non-rapid eye movement (NREM) sleep and are believed to mediate many sleep-related functions, from memory consolidation to cortical development. Spindles differ in location, frequency, and association with slow waves, but whether this heterogeneity may reflect different physiological processes and potentially serve different functional roles remains unclear. Here we utilized a unique opportunity to record intracranial depth EEG and single-unit activity in multiple brain regions of neurosurgical patients to better characterize spindle activity in human sleep. We find that spindles occur across multiple neocortical regions, and less frequently also in the parahippocampal gyrus and hippocampus. Most spindles are spatially restricted to specific brain regions. In addition, spindle frequency is topographically organized with a sharp transition around the supplementary motor area between fast (13-15Hz) centroparietal spindles often occurring with slow wave up-states, and slow (9-12Hz) frontal spindles occurring 200ms later on average. Spindle variability across regions may reflect the underlying thalamocortical projections. We also find that during individual spindles, frequency decreases within and between regions. In addition, deeper sleep is associated with a reduction in spindle occurrence and spindle frequency. Frequency changes between regions, during individual spindles, and across sleep may reflect the same phenomenon, the underlying level of thalamocortical hyperpolarization. Finally, during spindles neuronal firing rates are not consistently modulated, although some neurons exhibit phase-locked discharges. Overall, anatomical considerations can account well for regional spindle characteristics, while variable hyperpolarization levels can explain differences in spindle frequency.
doi:10.1523/JNEUROSCI.2604-11.2011
PMCID: PMC3270580  PMID: 22159098
14.  Regional Slow Waves and Spindles in Human Sleep 
Neuron  2011;70(1):153-169.
SUMMARY
The most prominent EEG events in sleep are slow waves, reflecting a slow (<1 Hz) oscillation between up and down states in cortical neurons. It is unknown whether slow oscillations are synchronous across the majority or the minority of brain regions—are they a global or local phenomenon? To examine this, we recorded simultaneously scalp EEG, intracerebral EEG, and unit firing in multiple brain regions of neurosurgical patients. We find that most sleep slow waves and the underlying active and inactive neuronal states occur locally. Thus, especially in late sleep, some regions can be active while others are silent. We also find that slow waves can propagate, usually from medial prefrontal cortex to the medial temporal lobe and hippocampus. Sleep spindles, the other hallmark of NREM sleep EEG, are likewise predominantly local. Thus, intracerebral communication during sleep is constrained because slow and spindle oscillations often occur out-of-phase in different brain regions.
doi:10.1016/j.neuron.2011.02.043
PMCID: PMC3108825  PMID: 21482364
15.  3D surface maps link local atrophy & Fast Ripples in human epileptic hippocampus 
Annals of Neurology  2009;66(6):783-791.
Objective
There is compelling evidence that pathological high frequency oscillations (HFOs) called Fast Ripples (FR, 150–500 Hz) reflect abnormal synchronous neuronal discharges in areas responsible for seizure genesis in patients with mesial temporal lobe epilepsy (MTLE). It is hypothesized that morphological changes associated with hippocampal atrophy (HA) contribute to the generation of FR, yet there is limited evidence that hippocampal FR-generating sites correspond with local areas of atrophy.
Methods
Interictal HFOs were recorded from hippocampal microelectrodes in ten patients with MTLE. Rates of FR and Ripple discharge from each microelectrode were evaluated in relation to local measures of HA obtained using 3D MRI hippocampal modeling.
Results
Rates of FR discharge were three times higher in areas of significant local HA compared to rates in non-atrophic areas. Furthermore, FR occurrence correlated directly with the severity of damage in these local atrophic regions. In contrast, we found no difference in rates of Ripple discharge between local atrophic and non-atrophic areas.
Interpretation
The proximity between local HA and microelectrode-recorded FR suggest morphological changes such as neuron loss and synaptic reorganization may contribute to the generation of FR. Pathological HFOs, such as FR, may provide a reliable surrogate marker of abnormal neuronal excitability in hippocampal areas responsible for the generation of spontaneous seizures in patients with MTLE. Based on these data, it is possible that MRI-based measures of local HA could identify FR-generating regions, and thus provide a non-invasive means to localize epileptogenic regions in hippocampus.
doi:10.1002/ana.21703
PMCID: PMC3299311  PMID: 20035513
16.  Internally generated preactivation of single neurons in human medial frontal cortex predicts volition 
Neuron  2011;69(3):548-562.
Understanding how self-initiated behavior is encoded by neuronal circuits in the human brain remains elusive. We recorded the activity of 1019 neurons while twelve subjects performed self-initiated finger movement. We report progressive neuronal recruitment over ~1500 ms before subjects report making the decision to move. We observed progressive increase or decrease in neuronal firing rate, particularly in the supplementary motor area (SMA), as the reported time of decision was approached. A population of 256 SMA neurons is sufficient to predict in single trials the impending decision to move with accuracy greater than 80% already 700 ms prior to subjects’ awareness. Furthermore, we predict, with a precision of a few hundred ms, the actual time point of this voluntary decision to move. We implement a computational model whereby volition emerges once a change in internally generated firing rate of neuronal assemblies crosses a threshold.
doi:10.1016/j.neuron.2010.11.045
PMCID: PMC3052770  PMID: 21315264
17.  Enhanced functional synchronization of medial and lateral PFC underlies internally-guided action planning 
Actions are often internally guided, reflecting our covert will and intentions. The dorsomedial prefrontal cortex, including the pre-Supplementary Motor Area (pre-SMA), has been implicated in the internally generated aspects of action planning, such as choice and intention. Yet, the mechanism by which this area interacts with other cognitive brain regions such as the dorsolateral prefrontal cortex, a central node in decision-making, is still unclear. To shed light on this mechanism, brain activity was measured via fMRI and intracranial EEG in two studies during the performance of visually cued repeated finger tapping in which the choice of finger was guided by either a presented number (external) or self-choice (internal). A functional-MRI (fMRI) study in 15 healthy participants demonstrated that the pre-SMA, compared to the SMA proper, was more active and also more functionally correlated with the dorsolateral prefrontal cortex during internally compared to externally guided action planning (p < 0.05, random effect). In a similar manner, an intracranial-EEG study in five epilepsy patients showed greater inter-regional gamma-related connectivity between electrodes situated in medial and lateral aspects of the prefrontal cortex for internally compared to externally guided actions. Although this finding was observed for groups of electrodes situated both in the pre-SMA and SMA-proper, increased intra-cluster gamma-related connectivity was only observed for the pre-SMA (sign-test, p < 0.0001). Overall our findings provide multi-scale indications for the involvement of the dorsomedial prefrontal cortex, and especially the pre-SMA, in generating internally guided motor planning. Our intracranial-EEG results further point to enhanced functional connectivity between decision-making- and motor planning aspects of the PFC, as a possible neural mechanism for internally generated action planning.
doi:10.3389/fnhum.2012.00079
PMCID: PMC3324921  PMID: 22518101
fMRI; iEEG; gamma band; internally guided; prefrontal cortex; finger tapping
18.  Invariance of Firing Rate and Field Potential Dynamics to Stimulus Modulation Rate in Human Auditory Cortex 
Human brain mapping  2010;32(8):1181-1193.
The effect of stimulus modulation rate on the underlying neural activity in human auditory cortex is not clear. Human studies (using both invasive and noninvasive techniques) have demonstrated that at the population level, auditory cortex follows stimulus envelope. Here we examined the effect of stimulus modulation rate by using a rare opportunity to record both spiking activity and local field potentials (LFP) in auditory cortex of patients during repeated presentations of an audio-visual movie clip presented at normal, double, and quadruple speeds. Mean firing rate during evoked activity remained the same across speeds and the temporal response profile of firing rate modulations at increased stimulus speeds was a linearly scaled version of the response during slower speeds. Additionally, stimulus induced power modulation of local field potentials in the high gamma band (64–128 Hz) exhibited similar temporal scaling as the neuronal firing rate modulations. Our data confirm and extend previous studies in humans and anesthetized animals, supporting a model in which both firing rate, and high-gamma LFP power modulations in auditory cortex follow the temporal envelope of the stimulus across different modulation rates.
doi:10.1002/hbm.21100
PMCID: PMC3085610  PMID: 20665720
human; auditory cortex; spiking activity; local field potentials (LFP)
20.  Explicit Encoding of Multimodal Percepts by Single Neurons in the Human Brain 
Current biology : CB  2009;19(15):1308-1313.
Summary
Different pictures of Marilyn Monroe can evoke the same percept, even if greatly modified as in Andy Warhol’s famous portraits. But how does the brain recognize highly variable pictures as the same percept? Various studies have provided insights into how visual information is processed along the “ventral pathway,” via both single-cell recordings in monkeys [1, 2] and functional imaging in humans [3, 4]. Interestingly, in humans, the same “concept” of Marilyn Monroe can be evoked with other stimulus modalities, for instance by hearing or reading her name. Brain imaging studies have identified cortical areas selective to voices [5, 6] and visual word forms [7, 8]. However, how visual, text, and sound information can elicit a unique percept is still largely unknown. By using presentations of pictures and of spoken and written names, we show that (1) single neurons in the human medial temporal lobe (MTL) respond selectively to representations of the same individual across different sensory modalities; (2) the degree of multimodal invariance increases along the hierarchical structure within the MTL; and (3) such neuronal representations can be generated within less than a day or two. These results demonstrate that single neurons can encode percepts in an explicit, selective, and invariant manner, even if evoked by different sensory modalities.
doi:10.1016/j.cub.2009.06.060
PMCID: PMC3032396  PMID: 19631538
21.  On-line, voluntary control of human temporal lobe neurons 
Nature  2010;467(7319):1104-1108.
Daily life continually confronts us with an exuberance of external, sensory stimuli competing with a rich stream of internal deliberations, plans and ruminations. The brain must select one or more of these for further processing. How this competition is resolved across multiple sensory and cognitive regions is not known; nor is it clear how internal thoughts and attention regulate this competition1–4. Recording from single neurons in patients implanted with intracranial electrodes for clinical reasons5–9, here we demonstrate that humans can regulate the activity of their neurons in the medial temporal lobe (MTL) to alter the outcome of the contest between external images and their internal representation. Subjects looked at a hybrid superposition of two images representing familiar individuals, landmarks, objects or animals and had to enhance one image at the expense of the other, competing one. Simultaneously, the spiking activity of their MTL neurons in different subregions and hemispheres was decoded in real time to control the content of the hybrid. Subjects reliably regulated, often on the first trial, the firing rate of their neurons, increasing the rate of some while simultaneously decreasing the rate of others. They did so by focusing onto one image, which gradually became clearer on the computer screen in front of their eyes, and thereby overriding sensory input. On the basis of the firing of these MTL neurons, the dynamics of the competition between visual images in the subject's mind was visualized on an external display.
doi:10.1038/nature09510
PMCID: PMC3010923  PMID: 20981100
22.  Broadband shifts in LFP power spectra are correlated with single-neuron spiking in humans 
A fundamental question in neuroscience concerns the relation between the spiking of individual neurons and the aggregate electrical activity of neuronal ensembles as seen in local-field potentials (LFPs). Because LFPs reflect both spiking activity and subthreshold events, this question is not simply one of data aggregation. Recording from 20 neurosurgical patients, we directly examined the relation between LFPs and neuronal spiking. Examining 2,030 neurons in widespread brain regions, we found that firing rates were positively correlated with broadband (2 – 150 Hz) shifts in the LFP power spectrum. In contrast, narrowband oscillations correlated both positively and negatively with firing rates at different recording sites. Broadband power shifts were a more-reliable predictor of neuronal spiking than narrowband power shifts. These findings suggest that broadband LFP power provides valuable information concerning neuronal activity beyond that contained in narrowband oscillations.
doi:10.1523/JNEUROSCI.2041-09.2009
PMCID: PMC3001247  PMID: 19864573
Local field potentials; Broadband; Oscillations; Single-units; Humans; Epilepsy
23.  Large-Scale Microelectrode Recordings of High-Frequency Gamma Oscillations in Human Cortex during Sleep 
The Journal of Neuroscience  2010;30(23):7770-7782.
Gamma oscillations (40–120 Hz), usually associated with waking functions, can be recorded in the deepest stages of sleep in animals. The full details of their large-scale coordination across multiple cortical networks are still unknown. Furthermore, it is not known whether oscillations with similar characteristics are also present in the human brain. In this study, we examined the existence of gamma oscillations during polysomnographically defined sleep–wake states using large-scale microelectrode recordings (up to 56 channels), with single-cell and spike-time precision, in epilepsy patients. We report that low (40–80 Hz) and high (80–120 Hz) gamma oscillations recurrently emerged over time windows of several hundreds of milliseconds in all investigated cortical areas during slow-wave sleep. These patterns were correlated with positive peaks of EEG slow oscillations and marked increases in local cellular discharges, suggesting that they were associated with cortical UP states. These gamma oscillations frequently appeared at approximately the same time in many different cortical areas, including homotopic regions, forming large spatial patterns. Coincident firings with millisecond precision were strongly enhanced during gamma oscillations but only between cells within the same cortical area. Furthermore, in a significant number of cases, cortical gamma oscillations tended to occur within 100 ms after hippocampal ripple/sharp wave complexes. These data confirm and extend earlier animal studies reporting that gamma oscillations are transiently expressed during UP states during sleep. We speculate that these high-frequency patterns briefly restore “microwake” activity and are important for consolidation of memory traces acquired during previous awake periods.
doi:10.1523/JNEUROSCI.5049-09.2010
PMCID: PMC3842470  PMID: 20534826
24.  Right-lateralized Brain Oscillations in Human Spatial Navigation 
Journal of cognitive neuroscience  2010;22(5):824-836.
During spatial navigation, lesion and functional imaging studies suggest that the right hemisphere has a unique functional role. However, studies of direct human brain recordings have not reported interhemisphere differences in navigation-related oscillatory activity. We investigated this apparent discrepancy using intracranial electroencephalographic recordings from 24 neurosurgical patients playing a virtual taxi driver game. When patients were virtually moving in the game, brain oscillations at various frequencies increased in amplitude compared with periods of virtual stillness. Using log-linear analysis, we analyzed the region and frequency specificities of this pattern and found that neocortical movement-related gamma oscillations (34–54 Hz) were significantly lateralized to the right hemisphere, especially in posterior neocortex. We also observed a similar right lateralization of gamma oscillations related to searching for objects at unknown virtual locations. Thus, our results indicate that gamma oscillations in the right neocortex play a special role in human spatial navigation.
doi:10.1162/jocn.2009.21240
PMCID: PMC2839416  PMID: 19400683
25.  Neural “Ignition”: Enhanced Activation Linked to Perceptual Awareness in Human Ventral Stream Visual Cortex 
Neuron  2009;64(4):562-574.
SUMMARY
Human recognition performance is characterized by abrupt changes in perceptual states. Understanding the neuronal dynamics underlying such transitions could provide important insights into mechanisms of recognition and perceptual awareness. Here we examined patients monitored for clinical purposes with multiple subdural electrodes. The patients participated in a backward masking experiment in which pictures of various object categories were presented briefly followed by a mask. We recorded ECoG from 445 electrodes placed in 11 patients. We found a striking increase in gamma power (30–70 Hz) and evoked responses specifically associated with successful recognition. The enhanced activation occurred 150–200 ms after stimulus onset and consistently outlasted the stimulus presentation. We propose that the gamma and evoked potential activations reflect a rapid increase in recurrent neuronal activity that plays a critical role in the emergence of a recognizable visual percept in conscious awareness.
doi:10.1016/j.neuron.2009.11.001
PMCID: PMC2854160  PMID: 19945397

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