Dataset of human medial temporal lobe single neuron activity during declarative memory encoding and recognition.

We present a dataset of 1,576 single neurons recorded from the human amygdala and hippocampus in 65 sessions from 42 patients undergoing intracranial monitoring for localization of epileptic seizures. Subjects performed a recognition memory task with pictures as stimuli. Subjects were asked to identify whether they had seen a particular image the first time ('new') or second time ('old') on a 1-6 confidence scale. This comprehensive dataset includes the spike times of all neurons and their extracellular waveforms, behavior, electrode locations determined from post-operative MRI scans, demographics, and the stimuli shown. As technical validation, we provide spike sorting quality metrics and assessment of tuning of cells to verify the presence of visually-and memory selective cells. We also provide analysis code that reproduces key scientific findings published previously on a smaller version of this dataset. Together, this large dataset will facilitate the investigation of the neural mechanism of declarative memory by providing a substantial number of hard to obtain human single-neuron recordings during a well characterized behavioral task.

Neurons in the human amygdala encode face identity, but not gaze direction.

The amygdala is important for face processing, and direction of eye gaze is one of the most socially salient facial signals. Recording from over 200 neurons in the amygdala of neurosurgical patients, we found robust encoding of the identity of neutral-expression faces, but not of their direction of gaze. Processing of gaze direction may rely on a predominantly cortical network rather than the amygdala.

Representation of retrieval confidence by single neurons in the human medial temporal lobe.

Memory-based decisions are often accompanied by an assessment of choice certainty, but the mechanisms of such confidence judgments remain unknown. We studied the response of 1,065 individual neurons in the human hippocampus and amygdala while neurosurgical patients made memory retrieval decisions together with a confidence judgment. Combining behavioral, neuronal and computational analysis, we identified a population of memory-selective (MS) neurons whose activity signaled stimulus familiarity and confidence, as assessed by subjective report. In contrast, the activity of visually selective (VS) neurons was not sensitive to memory strength. The groups further differed in response latency, tuning and extracellular waveforms. The information provided by MS neurons was sufficient for a race model to decide stimulus familiarity and retrieval confidence. Together, our results indicate a trial-by-trial relationship between a specific group of neurons and declared memory strength in humans. We suggest that VS and MS neurons are a substrate for declarative memories.

Neurons in the human amygdala selective for perceived emotion.

The human amygdala plays a key role in recognizing facial emotions and neurons in the monkey and human amygdala respond to the emotional expression of faces. However, it remains unknown whether these responses are driven primarily by properties of the stimulus or by the perceptual judgments of the perceiver. We investigated these questions by recording from over 200 single neurons in the amygdalae of 7 neurosurgical patients with implanted depth electrodes. We presented degraded fear and happy faces and asked subjects to discriminate their emotion by button press. During trials where subjects responded correctly, we found neurons that distinguished fear vs. happy emotions as expressed by the displayed faces. During incorrect trials, these neurons indicated the patients' subjective judgment. Additional analysis revealed that, on average, all neuronal responses were modulated most by increases or decreases in response to happy faces, and driven predominantly by judgments about the eye region of the face stimuli. Following the same analyses, we showed that hippocampal neurons, unlike amygdala neurons, only encoded emotions but not subjective judgment. Our results suggest that the amygdala specifically encodes the subjective judgment of emotional faces, but that it plays less of a role in simply encoding aspects of the image array. The conscious percept of the emotion shown in a face may thus arise from interactions between the amygdala and its connections within a distributed cortical network, a scheme also consistent with the long response latencies observed in human amygdala recordings.

Single-neuron correlates of atypical face processing in autism.

People with autism spectrum disorder (ASD) show abnormal processing of faces. A range of morphometric, histological, and neuroimaging studies suggest the hypothesis that this abnormality may be linked to the amygdala. We recorded data from single neurons within the amygdalae of two rare neurosurgical patients with ASD. While basic electrophysiological response parameters were normal, there were specific and striking abnormalities in how individual facial features drove neuronal response. Compared to control patients, a population of neurons in the two ASD patients responded significantly more to the mouth, but less to the eyes. Moreover, we found a second class of face-responsive neurons for which responses to faces appeared normal. The findings confirm the amygdala's pivotal role in abnormal face processing by people with ASD at the cellular level and suggest that dysfunction may be traced to a specific subpopulation of neurons with altered selectivity for the features of faces.

Single-unit responses selective for whole faces in the human amygdala.

The human amygdala is critical for social cognition from faces, as borne out by impairments in recognizing facial emotion following amygdala lesions [1] and differential activation of the amygdala by faces [2-5]. Single-unit recordings in the primate amygdala have documented responses selective for faces, their identity, or emotional expression [6, 7], yet how the amygdala represents face information remains unknown. Does it encode specific features of faces that are particularly critical for recognizing emotions (such as the eyes), or does it encode the whole face, a level of representation that might be the proximal substrate for subsequent social cognition? We investigated this question by recording from over 200 single neurons in the amygdalae of seven neurosurgical patients with implanted depth electrodes [8]. We found that approximately half of all neurons responded to faces or parts of faces. Approximately 20% of all neurons responded selectively only to the whole face. Although responding most to whole faces, these neurons paradoxically responded more when only a small part of the face was shown compared to when almost the entire face was shown. We suggest that the human amygdala plays a predominant role in representing global information about faces, possibly achieved through inhibition between individual facial features.

Comparison of length judgments and the Müller-Lyer illusion in monkeys and humans.

Visuo-spatial magnitude judgements are abstract in that they are detached from the specific sensory parameters on which they are based. Nevertheless, the visual system is actively reconstructing and interpreting the outside world, which sometimes causes reproducible geometric illusions. Here, we investigated the visual length perception of rhesus macaques, an Old World monkey species, in a delayed match-to-sample task and compared the non-human primates' performance to the length judgment of human participants under identical conditions. The quantitative analysis of the length discrimination shows that humans and macaques both show a distance and size effect in judging length and have almost identical length judgment characteristics as determined by the widths of the discrimination functions and the Weber fractions. Moreover, both monkeys and humans were subject to the geometric Müller-Lyer illusion caused by inward or outward pointing 'arrows' at the ends of a line, resulting in over- or underestimation of length, respectively. The strength of the illusion effects (i.e., the magnitude of length misjudgement for stimuli with inward and outward pointing arrows at the end of the lines) was in the range between 1.17 and 1.57° of visual angle for both monkeys and the human participants, and thus very similar between the two primate species. Our results suggest that the visuo-spatial mechanisms underlying simple horizontal line-length perceptions in the human and macaque monkey are qualitatively and quantitatively similar, offering the possibility to investigate the neural correlates of geometric illusions in the monkey and to translate the findings to the human visual system.

Contributions of primate prefrontal and posterior parietal cortices to length and numerosity representation.

The ability to understand and manipulate quantities ensures the survival of animals and humans alike. The frontoparietal network in primates has been implicated in representing, along with other cognitive abilities, abstract quantity. The respective roles of the prefrontal and parietal areas and the way continuous quantities, as opposed to discrete ones, are represented in this network, however, are unknown. We investigated this issue by simultaneously analyzing recorded single-unit activity in the prefrontal cortex (PFC) and the fundus of the intraparietal sulcus (IPS) of two macaque monkeys while they were engaged in delayed match-to-sample tasks discriminating line length and numerosity. In both areas, we found anatomically intermingled neurons encoding either length, numerosity, or both types of quantities. Even though different sets of neurons coded these quantities, the representation of length and numerosity was similar within the IPS and PFC. Both length and numerosity were coded by tuning functions peaking at the preferred quantity, thus supporting a labeled-line code for continuous and discrete quantity. A comparison of the response characteristics between parietal and frontal areas revealed a larger proportion of IPS neurons representing each quantity type in the early sample phase, in addition to shorter response latencies to quantity for IPS neurons. Moreover, IPS neurons discriminated quantities during the sample phase better than PFC neurons, as quantified by the receiver operating characteristic area. In the memory period, the discharge properties of PFC and IPS neurons were comparable. These single-cell results are in good agreement with functional imaging data from humans and support the notion that representations of continuous and discrete quantities share a frontoparietal substrate, with IPS neurons constituting the putative entry stage of the processing hierarchy.

Neuronal population coding of continuous and discrete quantity in the primate posterior parietal cortex.

Quantitative knowledge guides vital decisions in the life of animals and humans alike. The posterior parietal cortex in primates has been implicated in representing abstract quantity, both continuous (extent) and discrete (number of items), supporting the idea of a putative generalized magnitude system in this brain area. Whether or not single neurons encode different types of quantity, or how quantitative information is represented in the neuronal responses, however, is unknown. We show that length and numerosity are encoded by functionally overlapping groups of parietal neurons. Using a statistical classifier, we found that the activity of populations of quantity-selective neurons contained accurate information about continuous and discrete quantity. Unexpectedly, even neurons that were nonselective according to classical spike-count measures conveyed robust categorical information that predicted the monkeys' quantity judgments. Thus, different information-carrying processes of partly intermingled neuronal networks in the parietal lobe seem to encode various forms of abstract quantity.

Temporal and spatial enumeration processes in the primate parietal cortex.

Humans and animals can nonverbally enumerate visual items across time in a sequence or rapidly estimate the set size of spatial dot patterns at a single glance. We found that temporal and spatial enumeration processes engaged different populations of neurons in the intraparietal sulcus of behaving monkeys. Once the enumeration process was completed, however, another neuronal population represented the cardinality of a set irrespective of whether it had been cued in a spatial layout or across time. These data suggest distinct neural processing stages for different numerical formats, but also a final convergence of the segregated information to form most abstract quantity representations.