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How multisensory neurons solve causal inference

How multisensory neurons solve causal inference
How multisensory neurons solve causal inference

Sitting in a static railway carriage can produce illusory self-motion if the train on an adjoining track moves off. While our visual system registers motion, vestibular signals indicate that we are stationary. The brain is faced with a difficult challenge: is there a single cause of sensations (I am moving) or two causes (I am static, another train is moving)? If a single cause, integrating signals produces a more precise estimate of self-motion, but if not, one cue should be ignored. In many cases, this process of causal inference works without error, but how does the brain achieve it? Electrophysiological recordings show that the macaque medial superior temporal area contains many neurons that encode combinations of vestibular and visual motion cues. Some respond best to vestibular and visual motion in the same direction ("congruent" neurons), while others prefer opposing directions ("opposite" neurons). Congruent neurons could underlie cue integration, but the function of opposite neurons remains a puzzle. Here, we seek to explain this computational arrangement by training a neural network model to solve causal inference for motion estimation. Like biological systems, the model develops congruent and opposite units and recapitulates known behavioral and neurophysiological observations. We show that all units (both congruent and opposite) contribute to motion estimation. Importantly, however, it is the balance between their activity that distinguishes whether visual and vestibular cues should be integrated or separated. This explains the computational purpose of puzzling neural representations and shows how a relatively simple feedforward network can solve causal inference.

Causal inference, Deep neural network, MSTd, Multisensory integration, Visual and vestibular
0027-8424
Rideaux, Reuben
3ccb870a-2eca-4913-818d-4e20ce5babd0
Storrs, Katherine R.
d3376207-a72a-4931-a7fb-1cbef061c3f7
Maiello, Guido
c122b089-1bbc-4d3e-b178-b0a1b31a5295
Welchman, Andrew E.
c6db0722-5a74-4576-ad12-d3dec4814c59
Rideaux, Reuben
3ccb870a-2eca-4913-818d-4e20ce5babd0
Storrs, Katherine R.
d3376207-a72a-4931-a7fb-1cbef061c3f7
Maiello, Guido
c122b089-1bbc-4d3e-b178-b0a1b31a5295
Welchman, Andrew E.
c6db0722-5a74-4576-ad12-d3dec4814c59

Rideaux, Reuben, Storrs, Katherine R., Maiello, Guido and Welchman, Andrew E. (2021) How multisensory neurons solve causal inference. Proceedings of the National Academy of Sciences of the United States of America, 118 (32), [e2106235118]. (doi:10.1073/pnas.2106235118).

Record type: Article

Abstract

Sitting in a static railway carriage can produce illusory self-motion if the train on an adjoining track moves off. While our visual system registers motion, vestibular signals indicate that we are stationary. The brain is faced with a difficult challenge: is there a single cause of sensations (I am moving) or two causes (I am static, another train is moving)? If a single cause, integrating signals produces a more precise estimate of self-motion, but if not, one cue should be ignored. In many cases, this process of causal inference works without error, but how does the brain achieve it? Electrophysiological recordings show that the macaque medial superior temporal area contains many neurons that encode combinations of vestibular and visual motion cues. Some respond best to vestibular and visual motion in the same direction ("congruent" neurons), while others prefer opposing directions ("opposite" neurons). Congruent neurons could underlie cue integration, but the function of opposite neurons remains a puzzle. Here, we seek to explain this computational arrangement by training a neural network model to solve causal inference for motion estimation. Like biological systems, the model develops congruent and opposite units and recapitulates known behavioral and neurophysiological observations. We show that all units (both congruent and opposite) contribute to motion estimation. Importantly, however, it is the balance between their activity that distinguishes whether visual and vestibular cues should be integrated or separated. This explains the computational purpose of puzzling neural representations and shows how a relatively simple feedforward network can solve causal inference.

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Accepted/In Press date: 28 June 2021
Published date: 4 August 2021
Additional Information: Funding Information: ACKNOWLEDGMENTS. We thank Gregory DeAngelis for his insightful comments on a previous version of the manuscript. The work was supported by the Leverhulme Trust (ECF-2017-573), the Isaac Newton Trust (17.08(o)), Funding Information: and the Australian Research Council (DE210100790). G.M. was supported by the Deutsche Forschungsgemeinschaft (Grant SFB-TRR-135: “Cardinal Mechanisms of Perception”) and K.R.S. by an Alexander von Humboldt fellowship. Funding Information: We thank Gregory DeAngelis for his insightful comments on a previous version of the manuscript. The work was supported by the Leverhulme Trust (ECF-2017-573), the Isaac Newton Trust (17.08(o)), and the Australian Research Council (DE210100790). G.M. was supported by the Deutsche Forschungsgemeinschaft (Grant SFB-TRR-135: "Cardinal Mechanisms of Perception") and K.R.S. by an Alexander von Humboldt fellowship. Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.
Keywords: Causal inference, Deep neural network, MSTd, Multisensory integration, Visual and vestibular

Identifiers

Local EPrints ID: 484864
URI: http://eprints.soton.ac.uk/id/eprint/484864
ISSN: 0027-8424
PURE UUID: e7be1d28-6f03-496f-a4a4-ecb954c61df4
ORCID for Guido Maiello: ORCID iD orcid.org/0000-0001-6625-2583

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Date deposited: 23 Nov 2023 17:54
Last modified: 18 Mar 2024 04:11

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Contributors

Author: Reuben Rideaux
Author: Katherine R. Storrs
Author: Guido Maiello ORCID iD
Author: Andrew E. Welchman

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