Cited by 67Neural dynamics and brain functionVisual perception and processing mechanismsBayesian Modeling and Causal Inference

The Hamiltonian Brain: Efficient Probabilistic Inference with Excitatory-Inhibitory Neural Circuit Dynamics

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Aitchison, Laurence, Lengyel, Máté·2016·PLOS Computational Biology

Abstract

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.

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  • Approximate inference algorithms such as sampling may explain cortical feedback signals and activity correlations.

    “As theories of brain computation, approximate inference algorithms such as sampling may explain cortical feedback signals and activity correlations97,108–110.”

    From Cognitive computational neuroscience (2018) · cites this paper as [110]

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  1. [42]Karklin Y, Lewicki MS. Emergence of complex cell properties by learning to generalize in natural scenes. Nature. 2009; 457: 83– 86. 10.1038/nature07481 19020501 · DOI

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Authors
Aitchison, L., & Lengyel, M.
Affiliations
  • Gatsby Computational Neuroscience Unit (GB)
  • Central European University (AT)
Corresponding author
Aitchison, Laurence
Venue
PLOS Computational Biology
Published
2016-12-27
Volume
12
Issue
12
Pages
e1005186
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
OpenAlex
W2561212970
Cited by
67
References
90
Citations by year
2026: 2 · 2025: 7 · 2024: 8 · 2023: 6 · 2022: 8 · 2021: 7 · 2020: 10 · 2019: 9 · 2018: 4 · 2017: 5 · 2016: 1
FWCI
3.99
Type
journal article
Language
en
Open access
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • arXiv (Cornell University) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UCL Discovery (University College London) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • Cambridge University Engineering Department Publications Database (submittedVersion)
  • Open Research (Auckland University of Technology) (submittedVersion, cc-by)
  • Bristol Research (University of Bristol) (submittedVersion)
  • Explore Bristol Research (submittedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • arXiv (Cornell University)
  • Apollo (cc-by)
Funders
  • Gatsby Charitable Foundation
  • Seventh Framework Programme (FP7/2007–2013 269921)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Physical Sciences › Computer Science › Artificial Intelligence › Bayesian Modeling and Causal Inference
Keywords
probabilistic inference, Hamiltonian Monte Carlo, neural oscillations, primary visual cortex, cortical computation, excitation-inhibition balance, inference efficiency, state space exploration, stimulus contrast
MeSH terms
Animals, Computer Simulation, Humans, Models, Neurological, Nerve Net, Neural Inhibition, Synaptic Transmission, Visual Cortex, Visual Perception, Models, Statistical, Feedback, Physiological

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