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Cortical-like dynamics in recurrent circuits optimized for sampling-based probabilistic inference.

ABSTRACT: Sensory cortices display a suite of ubiquitous dynamical features, such as ongoing noise variability, transient overshoots and oscillations, that have so far escaped a common, principled theoretical account. We developed a unifying model for these phenomena by training a recurrent excitatory-inhibitory neural circuit model of a visual cortical hypercolumn to perform sampling-based probabilistic inference. The optimized network displayed several key biological properties, including divisive normalization and stimulus-modulated noise variability, inhibition-dominated transients at stimulus onset and strong gamma oscillations. These dynamical features had distinct functional roles in speeding up inferences and made predictions that we confirmed in novel analyses of recordings from awake monkeys. Our results suggest that the basic motifs of cortical dynamics emerge as a consequence of the efficient implementation of the same computational function-fast sampling-based inference-and predict further properties of these motifs that can be tested in future experiments.

SUBMITTER: Echeveste R

PROVIDER: S-EPMC7610392 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Cortical-like dynamics in recurrent circuits optimized for sampling-based probabilistic inference.

Echeveste Rodrigo R Aitchison Laurence L Hennequin Guillaume G Lengyel Máté M

Nature neuroscience 20200810 9

Sensory cortices display a suite of ubiquitous dynamical features, such as ongoing noise variability, transient overshoots and oscillations, that have so far escaped a common, principled theoretical account. We developed a unifying model for these phenomena by training a recurrent excitatory-inhibitory neural circuit model of a visual cortical hypercolumn to perform sampling-based probabilistic inference. The optimized network displayed several key biological properties, including divisive norma ...[more]

PMID: 32778794

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Project description:Probabilistic inference offers a principled framework for understanding both behaviour and cortical computation. However, two basic and ubiquitous properties of cortical responses seem difficult to reconcile with probabilistic inference: neural activity displays prominent oscillations in response to constant input, and large transient changes in response to stimulus onset. Indeed, cortical models of probabilistic inference have typically either concentrated on tuning curve or receptive field properties and remained agnostic as to the underlying circuit dynamics, or had simplistic dynamics that gave neither oscillations nor transients. Here we show that these dynamical behaviours may in fact be understood as hallmarks of the specific representation and algorithm that the cortex employs to perform probabilistic inference. We demonstrate that a particular family of probabilistic inference algorithms, Hamiltonian Monte Carlo (HMC), naturally maps onto the dynamics of excitatory-inhibitory neural networks. Specifically, we constructed a model of an excitatory-inhibitory circuit in primary visual cortex that performed HMC inference, and thus inherently gave rise to oscillations and transients. These oscillations were not mere epiphenomena but served an important functional role: speeding up inference by rapidly spanning a large volume of state space. Inference thus became an order of magnitude more efficient than in a non-oscillatory variant of the model. In addition, the network matched two specific properties of observed neural dynamics that would otherwise be difficult to account for using probabilistic inference. First, the frequency of oscillations as well as the magnitude of transients increased with the contrast of the image stimulus. Second, excitation and inhibition were balanced, and inhibition lagged excitation. These results suggest a new functional role for the separation of cortical populations into excitatory and inhibitory neurons, and for the neural oscillations that emerge in such excitatory-inhibitory networks: enhancing the efficiency of cortical computations.

Dataset Information

Cortical-like dynamics in recurrent circuits optimized for sampling-based probabilistic inference.

Publications

Cortical-like dynamics in recurrent circuits optimized for sampling-based probabilistic inference.

Similar Datasets

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