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Yang, G. R.

Publications and source records attributed to Yang, G. R..

11 recordsLinked to original sources

Functional Dichotomy of Orbitofrontal Cortex and Anterior Cingulate Cortex Subregions in Decision-Making and Brain-Body Regulation

Mood disorders are associated with complex disruptions in brain networks, including those associated with the orbitofrontal cortex (OFC) and pregenual anterior cingulate cortex (pACC). The functional contribution of the caudal OFC (cOFC) has remained largely unexplored. We investigated the functions of the cOFC and pACC in macaques performing an approach-avoidance task by the combination of multimodal recordings and electrical microstimulation (EMS) of the cOFC. We assessed neural, autonomic and behavioral responses. We found the cOFC to be sensitive to both positive and negative stimuli, whereas the pACC was singificantly more active during aversive outcomes. EMS of the cOFC increased avoidance behavior, suggesting a causal role for the OFC subdivision in cost-benefit decision-making. Physiological measurements were positively correlated with behavioral patterns, emphasizing body-brain synchronization during emotionally significant decision-making. We suggest that the cOFC contributes to inducing pessimistic states, thereby making its dysfunction a potential contributor to the etiology of mood disorders.

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Natural constraints explain working memory capacity limitations in sensory-cognitive models

The limited capacity of the brain to retain information in working memory has been well-known and studied for decades, yet the root of this limitation remains unclear. Here we built sensory-cognitive neural network models of working memory that perform tasks using raw visual stimuli. Contrary to intuitions that working memory capacity limitation stems from memory or cognitive constraints, we found that pre-training the sensory region of our models with natural images imposes sufficient constraints on models to exhibit a wide range of human-like behaviors in visual working memory tasks designed to probe capacity. Examining the neural mechanisms in our model reveals that capacity limitation mainly arises in a bottom-up manner. Our models offer a principled and functionally grounded explanation for the working memory capacity limitation without parameter fitting to behavioral data or much hyperparameter tuning. This work highlights the importance of developing models with realistic sensory processing even when investigating memory and other high-level cognitive phenomena.

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Pre-training RNNs on ecologically relevant tasks explains sub-optimal behavioral reset

The strategies found by animals facing a new task are determined both by individual experience and by structural priors evolved to leverage the statistics of natural environments. Rats can quickly learn to capitalize on the trial sequence correlations of two-alternative forced choice (2AFC) tasks after correct trials, but consistently deviate from optimal behavior after error trials, when they waive the accumulated evidence. To understand this outcome-dependent gating, we first show that Recurrent Neural Networks (RNNs) trained in the same 2AFC task outperform rats as they can readily learn to use across-trial information both after correct and error trials. We hypothesize that, while RNNs can optimize their behavior in the 2AFC task without any a priori restrictions, rats strategy is constrained by a structural prior adapted to a natural environment in which rewarded and non-rewarded actions provide largely asymmetric information. When pre-training RNNs in a more ecological task with more than two possible choices, networks develop a strategy by which they gate off the across-trial evidence after errors, mimicking rats behavior. Population analyses show that the pre-trained networks form an accurate representation of the sequence statistics independently of the outcome in the previous trial. After error trials, gating is implemented by a change in the network dynamics which temporarily decouples the categorization of the stimulus from the across-trial accumulated evidence. Our results suggest that the suboptimal behavior observed in rats reflects the influence of a structural prior that reacts to errors by isolating the network decision dynamics from the context, ultimately constraining the performance in a 2AFC laboratory task.

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Evolving the Olfactory System with Machine Learning

The convergent evolution of the fly and mouse olfactory system led us to ask whether the anatomic connectivity and functional logic of olfactory circuits would evolve in artificial neural networks trained to perform olfactory tasks. Artificial networks trained to classify odor identity recapitulate the connectivity inherent in the olfactory system. Input units are driven by a single receptor type, and units driven by the same receptor converge to form a glomerulus. Glomeruli exhibit sparse, unstructured connectivity to a larger, expansion layer of Kenyon cells. When trained to both classify odor identity and to impart innate valence onto odors, the network develops independent pathways for identity and valence classification. Thus, the defining features of fly and mouse olfactory systems also evolved in artificial neural networks trained to perform olfactory tasks. This implies that convergent evolution reflects an underlying logic rather than shared developmental principles.

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Meta-learning local synaptic plasticity for continual familiarity detection

Over the course of a lifetime, a continual stream of information is encoded and retrieved from memory. To explore the synaptic mechanisms that enable this ongoing process, we consider a continual familiarity detection task in which a subject must report whether an image has been previously encountered. We design a class of feedforward neural network models endowed with biologically plausible synaptic plasticity dynamics, the parameters of which are meta-learned to optimize familiarity detection over long delay intervals. After training, we find that anti-Hebbian plasticity leads to better performance than Hebbian and replicates experimental results from the inferotemporal cortex, including repetition suppression. Unlike previous models, this network both operates continuously without requiring any synaptic resets and generalizes to intervals it has not been trained on. We demonstrate this not only for uncorrelated random stimuli but also for images of real-world objects. Our work suggests a biologically plausible mechanism for continual learning, and demonstrates an effective application of machine learning for neuroscience discovery.

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Constructing neural network models from brain data reveals representational transformations underlying adaptive behavior

The human ability to adaptively implement a wide variety of tasks is thought to emerge from the dynamic transformation of cognitive information. We hypothesized that these transformations are implemented via conjunctive activations in conjunction hubs - brain regions that selectively integrate sensory, cognitive, and motor activations. We used recent advances in using functional connectivity to map the flow of activity between brain regions to construct a task-performing neural network model from fMRI data during a cognitive control task. We verified the importance of conjunction hubs in cognitive computations by simulating neural activity flow over this empirically-estimated functional connectivity model. These empirically-specified simulations produced above-chance task performance (motor responses) by integrating sensory and task rule activations in conjunction hubs. These findings reveal the role of conjunction hubs in supporting flexible cognitive computations, while demonstrating the feasibility of using empirically-estimated neural network models to gain insight into cognitive computations in the human brain.

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Understanding the functional and structural differences across excitatory and inhibitory neurons

One of the most fundamental organizational principles of the brain is the separation of excitatory (E) and inhibitory (I) neurons. In addition to their opposing effects on post-synaptic neurons, E and I cells tend to differ in their selectivity and connectivity. Although many such differences have been characterized experimentally, it is not clear why they exist in the first place. We studied this question in an artificial neural network equipped with multiple E and I cell types. We found that a deep convolutional recurrent network trained to perform an object classification task was able to capture salient distinctions between E and I neurons. We explored the necessary conditions for the network to develop distinct selectivity and connectivity across cell types. We found that neurons that project to higher-order areas will have greater stimulus selectivity, regardless of whether they are excitatory or not. Sparser connectivity is required for higher selectivity, but only when the recurrent connections are excitatory. These findings demonstrate that the differences observed across E and I neurons are not independent, and can be explained using a smaller number of factors.

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Circuit mechanisms for the maintenance and manipulation of information in working memory

Recently it has been proposed that information in short-term memory may not always be stored in persistent neuronal activity, but can be maintained in \"activity-silent\" hidden states such as synaptic efficacies endowed with short-term plasticity (STP). However, working memory involves manipulation as well as maintenance of information in the absence of external stimuli. In this work, we investigated working memory representation using recurrent neural network (RNN) models trained to perform several working memory dependent tasks. We found that STP can support the short-term maintenance of information provided that the memory delay period is sufficiently short. However, in tasks that require actively manipulating information, persistent neuronal activity naturally emerges from learning, and the amount of persistent neuronal activity scales with the degree of manipulation required. These results shed insight into the current debate on working memory encoding, and suggest that persistent neural activity can vary markedly between tasks used in different experiments.

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Inter-areal balanced amplification enhances signal propagation in a large-scale circuit model of the primate cortex

Reliable signal transmission represents a fundamental challenge for cortical systems, which display a wide range of weights of feedforward and feedback connections among heterogeneous areas. We re-examine the question of signal transmission across the cortex in network models based on recently available mesoscopic, directed- and weighted-inter-areal connectivity data of the macaque cortex. Our findings reveal that, in contrast to feed-forward propagation models, the presence of long-range excitatory feedback projections could compromise stable signal propagation. Using population rate models as well as a spiking network model, we find that effective signal propagation can be accomplished by balanced amplification across cortical areas while ensuring dynamical stability. Moreover, the activation of prefrontal cortex in our model requires the input strength to exceed a threshold, in support of the ignition model of conscious processing, demonstrating our model as an anatomically-realistic platform for investigations of the global primate cortex dynamics.

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Clustering and compositionality of task representations in a neural network trained to perform many cognitive tasks

A neural system has the ability to flexibly perform many tasks, but the underlying mechanism cannot be elucidated in traditional experimental and modeling studies designed for one task at a time. Here, we trained a single network model to perform 20 cognitive tasks that may involve working memory, decision-making, categorization and inhibitory control. We found that after training, recurrent units developed into clusters that are functionally specialized for various cognitive processes. We introduce a measure to quantify relationships between single-unit neural representations of tasks, and report five distinct types of such relationships that can be tested experimentally. Surprisingly, our network developed compositionality of task representations, a critical feature for cognitive flexibility, whereby one task can be performed by recombining instructions for other tasks. Finally, we demonstrate how the network could learn multiple tasks sequentially. This work provides a computational platform to investigate neural representations of many cognitive tasks.

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Response Reversal During Top-Down Modulation In Cortical Circuits With Multiple Interneuron Types

Pyramidal cells and interneurons expressing parvalbumin, somatostatin, or vasoactive intestinal peptide show cell type-specific connectivity patterns leading to a canonical microcircuit across cortex. Dissecting the dynamics of this microcircuit is essential to our understanding of the mammalian cortex. However, experiments recording from this circuit often report counterintuitive and seemingly contradictory findings. For example, the response of a V1 neural population to top-down behavioral modulation can reverse from positive to negative when the bottom-up thalamic input changes. We developed a theoretical framework to explain such response reversal, and we showed how this complex dynamics can emerge in circuits that possess two key features: the presence of multiple interneuron populations and a non-linear dependence between the input and output of the populations. Furthermore, we built a cortical circuit model and the comparison of our simulations with real data shows that our model reproduces the complex dynamics observed experimentally in mouse V1. Our explicit calculations allowed us to pinpoint the connections critical to response reversal, and to predict the existence of more types of complex dynamics that could be experimentally tested and the conditions to observe them.

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