Single neuron responses underlying face recognition in the human midfusiform face-selective cortex.

Faces are critical for social interactions and their recognition constitutes one of the most important and challenging functions of the human brain. While neurons responding selectively to faces have been recorded for decades in the monkey brain, face-selective neural activations have been reported with neuroimaging primarily in the human midfusiform gyrus. Yet, the cellular mechanisms producing selective responses to faces in this hominoid neuroanatomical structure remain unknown. Here we report single neuron recordings performed in 5 human subjects (1 male, 4 females) implanted with intracerebral microelectrodes in the face-selective midfusiform gyrus, while they viewed pictures of familiar and unknown faces and places. We observed similar responses to faces and places at the single cell level, but a significantly higher number of neurons responding to faces, thus offering a mechanistic account for the face-selective activations observed in this region. Although individual neurons did not respond preferentially to familiar faces, a population level analysis could consistently determine whether or not the faces (but not the places) were familiar, only about 50 ms after the initial recognition of the stimuli as faces. These results provide insights into the neural mechanisms of face processing in the human brain.

Distinct population and single-neuron selectivity for executive and episodic processing in human dorsal posterior cingulate.

Posterior cingulate cortex (PCC) is an enigmatic region implicated in psychiatric and neurological disease, yet its role in cognition remains unclear. Human studies link PCC to episodic memory and default mode network (DMN), while findings from the non-human primate emphasize executive processes more associated with the cognitive control network (CCN) in humans. We hypothesized this difference reflects an important functional division between dorsal (executive) and ventral (episodic) PCC. To test this, we utilized human intracranial recordings of population and single unit activity targeting dorsal PCC during an alternated executive/episodic processing task. Dorsal PCC population responses were significantly enhanced for executive, compared to episodic, task conditions, consistent with the CCN. Single unit recordings, however, revealed four distinct functional types with unique executive (CCN) or episodic (DMN) response profiles. Our findings provide critical electrophysiological data from human PCC, bridging incongruent views within and across species, furthering our understanding of PCC function.

Single Neuron Coding of Identity in the Human Hippocampal Formation.

Experimental findings show the ubiquitous presence of graded responses and tuning curves in the neocortex, particularly in visual areas [1-15]. Among these, inferotemporal-cortex (IT) neurons respond to complex visual stimuli, but differences in the neurons' responses can be used to distinguish the stimuli eliciting the responses [8, 9, 16-18]. The IT projects directly to the medial temporal lobe (MTL) [19], where neurons respond selectively to different pictures of specific persons and even to their written and spoken names [20-22]. However, it is not clear whether this is done through a graded coding, as in the neocortex, or a truly invariant code, in which the response-eliciting stimuli cannot be distinguished from each other. To address this issue, we recorded single neurons during the repeated presentation of different stimuli (pictures and written and spoken names) corresponding to the same persons. Using statistical tests and a decoding approach, we found that only in a minority of cases can the different pictures of a given person be distinguished from the neurons' responses and that in a larger proportion of cases, the responses to the pictures were different to the ones to the written and spoken names. We argue that MTL neurons tend to lack a representation of sensory features (particularly within a sensory modality), which can be advantageous for the memory function attributed to this area [23-25], and that a full representation of memories is given by a combination of mostly invariant coding in the MTL with a representation of sensory features in the neocortex.

Encoding of long-term associations through neural unitization in the human medial temporal lobe.

Besides decades of research showing the role of the medial temporal lobe (MTL) in memory and the encoding of associations, the neural substrates underlying these functions remain unknown. We identified single neurons in the human MTL that responded to multiple and, in most cases, associated stimuli. We observed that most of these neurons exhibit no differences in their spike and local field potential (LFP) activity associated with the individual response-eliciting stimuli. In addition, LFP responses in the theta band preceded single neuron responses by ~70 ms, with the single trial phase providing fine tuning of the spike response onset. We postulate that the finding of similar neuronal responses to associated items provides a simple and flexible way of encoding memories in the human MTL, increasing the effective capacity for memory storage and successful retrieval.

A novel and fully automatic spike-sorting implementation with variable number of features.

The most widely used spike-sorting algorithms are semiautomatic in practice, requiring manual tuning of the automatic solution to achieve good performance. In this work, we propose a new fully automatic spike-sorting algorithm that can capture multiple clusters of different sizes and densities. In addition, we introduce an improved feature selection method, by using a variable number of wavelet coefficients, based on the degree of non-Gaussianity of their distributions. We evaluated the performance of the proposed algorithm with real and simulated data. With real data from single-channel recordings, in ~95% of the cases the new algorithm replicated, in an unsupervised way, the solutions obtained by expert sorters, who manually optimized the solution of a previous semiautomatic algorithm. This was done while maintaining a low number of false positives. With simulated data from single-channel and tetrode recordings, the new algorithm was able to correctly detect many more neurons compared with previous implementations and also compared with recently introduced algorithms, while significantly reducing the number of false positives. In addition, the proposed algorithm showed good performance when tested with real tetrode recordings. NEW & NOTEWORTHY We propose a new fully automatic spike-sorting algorithm, including several steps that allow the selection of multiple clusters of different sizes and densities. Moreover, it defines the dimensionality of the feature space in an unsupervised way. We evaluated the performance of the algorithm with real and simulated data, from both single-channel and tetrode recordings. The proposed algorithm was able to outperform manual sorting from experts and other recent unsupervised algorithms.

Extracting information from the shape and spatial distribution of evoked potentials.

BACKGROUND: Over 90 years after its first recording, scalp electroencephalography (EEG) remains one of the most widely used techniques in human neuroscience research, in particular for the study of event-related potentials (ERPs). However, because of its low signal-to-noise ratio, extracting useful information from these signals continues to be a hard-technical challenge. Many studies focus on simple properties of the ERPs such as peaks, latencies, and slopes of signal deflections. NEW METHOD: To overcome these limitations, we developed the Wavelet-Information method which uses wavelet decomposition, information theory, and a quantification based on single-trial decoding performance to extract information from evoked responses. RESULTS: Using simulations and real data from four experiments, we show that the proposed approach outperforms standard supervised analyses based on peak amplitude estimation. Moreover, the method can extract information using the raw data from all recorded channels using no a priori knowledge or pre-processing steps. COMPARISON WITH EXISTING METHOD(S): We show that traditional approaches often disregard important features of the signal such as the shape of EEG waveforms. Also, other approaches often require some form of a priori knowledge for feature selection and lead to problems of multiple comparisons. CONCLUSIONS: This approach offers a new and complementary framework to design experiments that go beyond the traditional analyses of ERPs. Potentially, it allows a wide usage beyond basic research; such as for clinical diagnosis, brain-machine interfaces, and neurofeedback applications requiring single-trial analyses.

Where is the ball? Behavioral and neural responses elicited by a magic trick.

We present results from two experiments, in which subjects watched continuous videos of a professional magician repeatedly performing a maneuver in which a ball could "magically" appear under a cup. In all cases, subjects were asked to predict whether the ball would appear under the cup or not, while scalp EEG recordings were performed. Both experiments elicited strong and consistent behavioral and neural responses. In the first experiment, we used two blocks of videos with different probabilities of the ball appearing in the cup and found that, first, based on the behavioral responses, the subjects could track this probability change; and second, the different probabilities modulated the neural responses. In the second experiment, we introduced a control condition in which the magician performed the maneuver under the table, out of subjects' view. Comparing the two conditions (i.e., performing the maneuver within or out of the subjects' view), we found that, first, the magic trick dramatically biased the subjects' behavioral responses; and second, the two conditions led to differential neural responses, in spite of the fact that the stimulus triggering the evoked responses (seeing the ball in the cup) was exactly the same. Altogether, our results show how new insights into sensory and cognitive processing can be obtained using adapted magic tricks. Moreover, the approach of analyzing responses to continuous video presentations offers a more ecological setting compared to classic evoked potential paradigms, which are typically based on presenting static images flashed at the center of the screen.

Single-cell recordings in the human medial temporal lobe.

Recordings from individual neurons in patients who are implanted with depth electrodes for clinical reasons have opened the possibility to narrow down the gap between neurophysiological studies in animals and non-invasive (e.g. functional magnetic resonance imaging, electroencephalogram, magnetoencephalography) investigations in humans. Here we provide a description of the main procedures for electrode implantation and recordings, the experimental paradigms used and the main steps for processing the data. We also present key characteristics of the so-called 'concept cells', neurons in the human medial temporal lobe with selective and invariant responses that represent the meaning of the stimulus, and discuss their proposed role in declarative memory. Finally, we present novel results dealing with the stability of the representation given by these neurons, by studying the effect of stimulus repetition in the strength of the responses. In particular, we show that, after an initial decay, the response strength reaches an asymptotic value after approximately 15 presentations that remains above baseline for the whole duration of the experiment.

Perceptual and contextual awareness: methodological considerations in the search for the neural correlates of consciousness.

In the last decades, the neural correlates of consciousness (NCCs) have been explored using both invasive and non-invasive recordings by comparing the brain activity elicited by seen versus unseen visual stimuli (i.e., the contrastive analysis). Here, we review a selection of these studies and discuss a set of considerations to improve the search for the NCCs using the contrastive analysis. In particular, we first argue in favor of implementing paradigms where different perceptual outputs are obtained using identical visual inputs. Second, we propose that the large disagreement in the field -in terms of the dissimilar neural patterns proposed as NCCs- is partially explained by the fact that different studies report the neural correlates of different conscious processes in the brain. More specifically, we distinguish between the perceptual awareness of a visual stimulus, associated to a boost in object-selective neural assemblies, and a more elaborate process (contextual awareness) that we argue is reflected in the firing of concept neurons in the medial temporal lobe, triggering a rich representation of the context, associations, and memories linked to the specific stimulus.

A biologically plausible model for same/different discrimination.

Abstract rules can be learned by several species (not only humans). We propose a biologically plausible model for same/different discrimination, that can point towards the neural basis of abstract concept learning. By including a neural adaptation mechanism to a discriminator model formerly introduced in the literature, selective clusters of neurons fire depending on whether or not the stimuli compared are the same or not. These selective neurons are consistent with experimental findings in the literature. Moreover, reward and attention can modulate the relative strength of each attribute/feature of the stimulus, so more complex abstract discriminations can be achieved using the proposed model as a building block. As a formal model, it can be easily incorporated into several applications in robotics and intelligent machines.