Abstract representations emerge in human hippocampal neurons during inference.

Humans have the remarkable cognitive capacity to rapidly adapt to changing environments. Central to this capacity is the ability to form high-level, abstract representations that take advantage of regularities in the world to support generalization1. However, little is known about how these representations are encoded in populations of neurons, how they emerge through learning and how they relate to behaviour2,3. Here we characterized the representational geometry of populations of neurons (single units) recorded in the hippocampus, amygdala, medial frontal cortex and ventral temporal cortex of neurosurgical patients performing an inferential reasoning task. We found that only the neural representations formed in the hippocampus simultaneously encode several task variables in an abstract, or disentangled, format. This representational geometry is uniquely observed after patients learn to perform inference, and consists of disentangled directly observable and discovered latent task variables. Learning to perform inference by trial and error or through verbal instructions led to the formation of hippocampal representations with similar geometric properties. The observed relation between representational format and inference behaviour suggests that abstract and disentangled representational geometries are important for complex cognition.

Properties and hemispheric differences of theta oscillations in the human hippocampus.

The left and right primate hippocampi (LH and RH) are thought to support distinct functions, but little is known about differences between the hemispheres at the neuronal level. We recorded single-neuron and local field potentials from the human hippocampus in epilepsy patients implanted with depth electrodes. We detected theta-frequency bouts of oscillatory activity while patients performed a visual recognition memory task. Theta appeared in bouts of 3.16 cycles, with sawtooth-shaped oscillations that had a prolonged downswing period. Outside the seizure onset zone, the average frequency of theta bouts was higher in the RH compared to the LH (6.0 vs. 5.3 Hz). LH theta bouts had lower amplitudes and a higher prevalence compared to the RH (26% vs. 21% of total time). Additionally, the RH contained a population of thin spiking visually tuned neurons that were not present in the LH. These data show that human theta appears in short oscillatory bouts whose properties vary between hemispheres, thereby revealing neurophysiological properties of the hippocampus that differ between the hemispheres.

Value-Related Neuronal Responses in the Human Amygdala during Observational Learning.

The amygdala plays an important role in many aspects of social cognition and reward learning. Here, we aimed to determine whether human amygdala neurons are involved in the computations necessary to implement learning through observation. We performed single-neuron recordings from the amygdalae of human neurosurgical patients (male and female) while they learned about the value of stimuli through observing the outcomes experienced by another agent interacting with those stimuli. We used a detailed computational modeling approach to describe patients' behavior in the task. We found a significant proportion of amygdala neurons whose activity correlated with both expected rewards for oneself and others, and in tracking outcome values received by oneself or other agents. Additionally, a population decoding analysis suggests the presence of information for both observed and experiential outcomes in the amygdala. Encoding and decoding analyses suggested observational value coding in amygdala neurons occurred in a different subset of neurons than experiential value coding. Collectively, these findings support a key role for the human amygdala in the computations underlying the capacity for learning through observation.SIGNIFICANCE STATEMENT Single-neuron studies of the human brain provide a unique window into the computational mechanisms of cognition. In this study, epilepsy patients implanted intracranially with hybrid depth electrodes performed an observational learning (OL) task. We measured single-neuron activity in the amygdala and found a representation for observational rewards as well as observational expected reward values. Additionally, distinct subsets of amygdala neurons represented self-experienced and observational values. This study provides a rare glimpse into the role of human amygdala neurons in social cognition.

Musical Preferences Predict Personality: Evidence From Active Listening and Facebook Likes.

Research over the past decade has shown that various personality traits are communicated through musical preferences. One limitation of that research is external validity, as most studies have assessed individual differences in musical preferences using self-reports of music-genre preferences. Are personality traits communicated through behavioral manifestations of musical preferences? We addressed this question in two large-scale online studies with demographically diverse populations. Study 1 ( N = 22,252) shows that reactions to unfamiliar musical excerpts predicted individual differences in personality-most notably, openness and extraversion-above and beyond demographic characteristics. Moreover, these personality traits were differentially associated with particular music-preference dimensions. The results from Study 2 ( N = 21,929) replicated and extended these findings by showing that an active measure of naturally occurring behavior, Facebook Likes for musical artists, also predicted individual differences in personality. In general, our findings establish the robustness and external validity of the links between musical preferences and personality.

Saccade-related neural communication in the human medial temporal lobe is modulated by the social relevance of stimuli.

Humans predominantly explore their environment by moving their eyes. To optimally communicate and process visual information, neural activity needs to be coordinated with the execution of eye movements. We investigated the coordination between visual exploration and interareal neural communication by analyzing local field potentials and single neuron activity in patients with epilepsy. We demonstrated that during the free viewing of images, neural communication between the human amygdala and hippocampus is coordinated with the execution of eye movements. The strength and direction of neural communication and hippocampal saccade-related phase alignment were strongest for fixations that landed on human faces. Our results argue that the state of the human medial temporal lobe network is selectively coordinated with motor behavior. Interareal neural communication was facilitated for social stimuli as indexed by the category of the attended information.

Flexible recruitment of memory-based choice representations by the human medial frontal cortex.

Decision-making in complex environments relies on flexibly using prior experience. This process depends on the medial frontal cortex (MFC) and the medial temporal lobe, but it remains unknown how these structures implement selective memory retrieval. We recorded single neurons in the MFC, amygdala, and hippocampus while human subjects switched between making recognition memory-based and categorization-based decisions. The MFC rapidly implemented changing task demands by using different subspaces of neural activity and by representing the currently relevant task goal. Choices requiring memory retrieval selectively engaged phase-locking of MFC neurons to amygdala and hippocampus field potentials, thereby enabling the routing of memories. These findings reveal a mechanism for flexibly and selectively engaging memory retrieval and show that memory-based choices are preferentially represented in the frontal cortex when required.

Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala.

Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing.

Making decisions based on autobiographical memories.

A new human intracranial study by Foster et al. (2015) sheds light on the electrophysiological correlates of intrinsic and task-evoked functional connectivity in lateral and medial parietal cortex.

A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback.

OBJECTIVE: Present day cortical brain-machine interfaces (BMIs) have made impressive advances using decoded brain signals to control extracorporeal devices. Although BMIs are used in a closed-loop fashion, sensory feedback typically is visual only. However medical case studies have shown that the loss of somesthesis in a limb greatly reduces the agility of the limb even when visual feedback is available. APPROACH: To overcome this limitation, this study tested a closed-loop BMI that utilizes intracortical microstimulation to provide 'tactile' sensation to a non-human primate. MAIN RESULT: Using stimulation electrodes in Brodmann area 1 of somatosensory cortex (BA1) and recording electrodes in the anterior intraparietal area, the parietal reach region and dorsal area 5 (area 5d), it was found that this form of feedback can be used in BMI tasks. SIGNIFICANCE: Providing somatosensory feedback has the poyential to greatly improve the performance of cognitive neuroprostheses especially for fine control and object manipulation. Adding stimulation to a BMI system could therefore improve the quality of life for severely paralyzed patients.

WITHDRAWN: Corrigendum to "A novel method for analyzing images of live nerve cells" [J. Neurosci. Methods 201 (2011) 98-105].

This article has been withdrawn at the request of the author(s) and/or editor. The Publisher apologizes for any inconvenience this may cause. The full Elsevier Policy on Article Withdrawal can be found at http://www.elsevier.com/locate/withdrawalpolicy.

A novel method for analyzing images of live nerve cells.

Analysis of images from live-cell experiments is a central activity to studying the effects of stimulation on neuronal behavior. Image analysis techniques currently used to study these effects rely for the most part on the salience of the neuronal structures within the image. In both fluorescent and electron microscopy, neuronal structures are enhanced and therefore easy to distinguish in an image. Unlike images obtained via fluorescent or electron microscopy, however, images produced via transmission microscopy (e.g., bright field, phase contrast, DIC) are significantly more difficult to analyze because there is little contrast between the object-of-interest and the image background. This difficulty is amplified when a time-dependent sequence of images are to be analyzed, because of the corresponding large data sets. To address this problem, we introduce a novel approach to the analysis of images of live cells captured via transmission microscopy that takes advantage of commercially available software and the Fourier transform. Specifically, our approach utilizes several morphological functions in MATLAB to enhance the contrast of the cells with respect to the background, which is followed by 2-D Fourier analysis to generate a spectrum from which the orientation and alignment of cells and their processes can be measured. We show that this method can be used to simplify the interpretation of complex structure in images of live neurons obtained via transmission microscopy and consequently, discover trends in neurite development following different types of stimulation. This approach provides a consistent and reliable tool for analyzing changes in cell structure that occurs during live-cell experiments.

Developing implantable neuroprosthetics: a new model in pig.

A new model has been established in the domestic pig for neural prosthetic device development and testing. To this end, we report on a complete neural prosthetic developmental system using a wireless sensor as the implant, a pig as the animal model, and a novel data acquisition paradigm for actuator control. A new type of stereotactic frame with clinically-inspired fixations pins that place the pig brain in standard surgical plane was developed and tested with success during the implantation of the microsystem. The microsystem implanted was an ultra-low power (12.5 mW) 16-channel intracortical/epicranial device transmitting broadband (40 kS/s) data over a wireless infrared telemetric link. Pigs were implanted and neural data was collected over a period of 5 weeks, clearly showing single unit spiking activity.