The Geometry of Abstraction in the Hippocampus and Prefrontal Cortex.

The curse of dimensionality plagues models of reinforcement learning and decision making. The process of abstraction solves this by constructing variables describing features shared by different instances, reducing dimensionality and enabling generalization in novel situations. Here, we characterized neural representations in monkeys performing a task described by different hidden and explicit variables. Abstraction was defined operationally using the generalization performance of neural decoders across task conditions not used for training, which requires a particular geometry of neural representations. Neural ensembles in prefrontal cortex, hippocampus, and simulated neural networks simultaneously represented multiple variables in a geometry reflecting abstraction but that still allowed a linear classifier to decode a large number of other variables (high shattering dimensionality). Furthermore, this geometry changed in relation to task events and performance. These findings elucidate how the brain and artificial systems represent variables in an abstract format while preserving the advantages conferred by high shattering dimensionality.

Temporal multiplexing of perception and memory codes in IT cortex.

A central assumption of neuroscience is that long-term memories are represented by the same brain areas that encode sensory stimuli1. Neurons in inferotemporal (IT) cortex represent the sensory percept of visual objects using a distributed axis code2-4. Whether and how the same IT neural population represents the long-term memory of visual objects remains unclear. Here we examined how familiar faces are encoded in the IT anterior medial face patch (AM), perirhinal face patch (PR) and temporal pole face patch (TP). In AM and PR we observed that the encoding axis for familiar faces is rotated relative to that for unfamiliar faces at long latency; in TP this memory-related rotation was much weaker. Contrary to previous claims, the relative response magnitude to familiar versus unfamiliar faces was not a stable indicator of familiarity in any patch5-11. The mechanism underlying the memory-related axis change is likely intrinsic to IT cortex, because inactivation of PR did not affect axis change dynamics in AM. Overall, our results suggest that memories of familiar faces are represented in AM and perirhinal cortex by a distinct long-latency code, explaining how the same cell population can encode both the percept and memory of faces.

Place cells may simply be memory cells: Memory compression leads to spatial tuning and history dependence.

The observation of place cells has suggested that the hippocampus plays a special role in encoding spatial information. However, place cell responses are modulated by several nonspatial variables and reported to be rather unstable. Here, we propose a memory model of the hippocampus that provides an interpretation of place cells consistent with these observations. We hypothesize that the hippocampus is a memory device that takes advantage of the correlations between sensory experiences to generate compressed representations of the episodes that are stored in memory. A simple neural network model that can efficiently compress information naturally produces place cells that are similar to those observed in experiments. It predicts that the activity of these cells is variable and that the fluctuations of the place fields encode information about the recent history of sensory experiences. Place cells may simply be a consequence of a memory compression process implemented in the hippocampus.

Deep Learning without Weight Symmetry.

Backpropagation (BP), a foundational algorithm for training artificial neural networks, predominates in contemporary deep learning. Although highly successful, it is often considered biologically implausible. A significant limitation arises from the need for precise symmetry between connections in the backward and forward pathways to backpropagate gradient signals accurately, which is not observed in biological brains. Researchers have proposed several algorithms to alleviate this symmetry constraint, such as feedback alignment and direct feedback alignment. However, their divergence from backpropagation dynamics presents challenges, particularly in deeper networks and convolutional layers. Here we introduce the Product Feedback Alignment (PFA) algorithm. Our findings demonstrate that PFA closely approximates BP and achieves comparable performance in deep convolutional networks while avoiding explicit weight symmetry. Our results offer a novel solution to the longstanding weight symmetry problem, leading to more biologically plausible learning in deep convolutional networks compared to earlier methods.

Mixed selectivity: Cellular computations for complexity.

The property of mixed selectivity has been discussed at a computational level and offers a strategy to maximize computational power by adding versatility to the functional role of each neuron. Here, we offer a biologically grounded implementational-level mechanistic explanation for mixed selectivity in neural circuits. We define pure, linear, and nonlinear mixed selectivity and discuss how these response properties can be obtained in simple neural circuits. Neurons that respond to multiple, statistically independent variables display mixed selectivity. If their activity can be expressed as a weighted sum, then they exhibit linear mixed selectivity; otherwise, they exhibit nonlinear mixed selectivity. Neural representations based on diverse nonlinear mixed selectivity are high dimensional; hence, they confer enormous flexibility to a simple downstream readout neural circuit. However, a simple neural circuit cannot possibly encode all possible mixtures of variables simultaneously, as this would require a combinatorially large number of mixed selectivity neurons. Gating mechanisms like oscillations and neuromodulation can solve this problem by dynamically selecting which variables are mixed and transmitted to the readout.

Social isolation recruits amygdala-cortical circuitry to escalate alcohol drinking.

How do social factors impact the brain and contribute to increased alcohol drinking? We found that social rank predicts alcohol drinking, where subordinates drink more than dominants. Furthermore, social isolation escalates alcohol drinking, particularly impacting subordinates who display a greater increase in alcohol drinking compared to dominants. Using cellular resolution calcium imaging, we show that the basolateral amygdala-medial prefrontal cortex (BLA-mPFC) circuit predicts alcohol drinking in a rank-dependent manner, unlike non-specific BLA activity. The BLA-mPFC circuit becomes hyperexcitable during social isolation, detecting social isolation states. Mimicking the observed increases in BLA-mPFC activity using optogenetics was sufficient to increase alcohol drinking, suggesting the BLA-mPFC circuit may be a neural substrate for the negative impact of social isolation. To test the hypothesis that the BLA-mPFC circuit conveys a signal induced by social isolation to motivate alcohol consumption, we first determined if this circuit detects social information. Leveraging optogenetics in combination with calcium imaging and computer vision pose tracking, we found that BLA-mPFC circuitry governs social behavior and neural representation of social contact. We further show that BLA-mPFC stimulation mimics social isolation-induced mPFC encoding of sucrose and alcohol, and inhibition of the BLA-mPFC circuit decreases alcohol drinking following social isolation. Collectively, these data suggest the amygdala-cortical circuit mirrors a neural encoding state similar to social isolation and underlies social isolation-associated alcohol drinking.

Face familiarity detection with complex synapses.

Synaptic plasticity is a complex phenomenon involving multiple biochemical processes that operate on different timescales. Complexity can greatly increase memory capacity when the variables characterizing the synaptic dynamics have limited precision, as shown in simple memory retrieval problems involving random patterns. Here we turn to a real-world problem, face familiarity detection, and we show that synaptic complexity can be harnessed to store in memory a large number of faces that can be recognized at a later time. The number of recognizable faces grows almost linearly with the number of synapses and quadratically with the number of neurons. Complex synapses outperform simple ones characterized by a single variable, even when the total number of dynamical variables is matched. Complex and simple synapses have distinct signatures that are testable in experiments. Our results indicate that a system with complex synapses can be used in real-world tasks such as face familiarity detection.

The implications of categorical and category-free mixed selectivity on representational geometries.

The firing rates of individual neurons displaying mixed selectivity are modulated by multiple task variables. When mixed selectivity is nonlinear, it confers an advantage by generating a high-dimensional neural representation that can be flexibly decoded by linear classifiers. Although the advantages of this coding scheme are well accepted, the means of designing an experiment and analyzing the data to test for and characterize mixed selectivity remain unclear. With the growing number of large datasets collected during complex tasks, the mixed selectivity is increasingly observed and is challenging to interpret correctly. We review recent approaches for analyzing and interpreting neural datasets and clarify the theoretical implications of mixed selectivity in the variety of forms that have been reported in the literature. We also aim to provide a practical guide for determining whether a neural population has linear or nonlinear mixed selectivity and whether this mixing leads to a categorical or category-free representation.

Computational principles of synaptic memory consolidation.

Memories are stored and retained through complex, coupled processes operating on multiple timescales. To understand the computational principles behind these intricate networks of interactions, we construct a broad class of synaptic models that efficiently harness biological complexity to preserve numerous memories by protecting them against the adverse effects of overwriting. The memory capacity scales almost linearly with the number of synapses, which is a substantial improvement over the square root scaling of previous models. This was achieved by combining multiple dynamical processes that initially store memories in fast variables and then progressively transfer them to slower variables. Notably, the interactions between fast and slow variables are bidirectional. The proposed models are robust to parameter perturbations and can explain several properties of biological memory, including delayed expression of synaptic modifications, metaplasticity, and spacing effects.