Interrogating theoretical models of neural computation with emergent property inference

Author:

Bittner Sean R1ORCID,Palmigiano Agostina1,Piet Alex T234ORCID,Duan Chunyu A5ORCID,Brody Carlos D236ORCID,Miller Kenneth D1,Cunningham John7

Affiliation:

1. Department of Neuroscience, Columbia University, New York, United States

2. Princeton Neuroscience Institute, Princeton, United States

3. Princeton University, Princeton, United States

4. Allen Institute for Brain Science, Seattle, United States

5. Institute of Neuroscience, Chinese Academy of Sciences, Shanghai, China

6. Howard Hughes Medical Institute, Chevy Chase, United States

7. Department of Statistics, Columbia University, New York, United States

Abstract

A cornerstone of theoretical neuroscience is the circuit model: a system of equations that captures a hypothesized neural mechanism. Such models are valuable when they give rise to an experimentally observed phenomenon -- whether behavioral or a pattern of neural activity -- and thus can offer insights into neural computation. The operation of these circuits, like all models, critically depends on the choice of model parameters. A key step is then to identify the model parameters consistent with observed phenomena: to solve the inverse problem. In this work, we present a novel technique, emergent property inference (EPI), that brings the modern probabilistic modeling toolkit to theoretical neuroscience. When theorizing circuit models, theoreticians predominantly focus on reproducing computational properties rather than a particular dataset. Our method uses deep neural networks to learn parameter distributions with these computational properties. This methodology is introduced through a motivational example of parameter inference in the stomatogastric ganglion. EPI is then shown to allow precise control over the behavior of inferred parameters and to scale in parameter dimension better than alternative techniques. In the remainder of this work, we present novel theoretical findings in models of primary visual cortex and superior colliculus, which were gained through the examination of complex parametric structure captured by EPI. Beyond its scientific contribution, this work illustrates the variety of analyses possible once deep learning is harnessed towards solving theoretical inverse problems.

Funder

National Science Foundation

NINDS

McKnight Endowment Fund for Neuroscience

Gatsby Charitable Foundation

Simons Foundation

NIH

Grossman Charitable Foundation

Howard Hughes Medical Institute

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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