Neural population dynamics underlying evidence accumulation in multiple rat brain regions

Abstract
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Abstract

Accumulating evidence to make decisions is a core cognitive function. Previous studies have tended to estimate accumulation using either neural or behavioral data alone. Here we develop a unified framework for modeling stimulus-driven behavior and multi-neuron activity simultaneously. We applied our method to choices and neural recordings from three rat brain regions - the posterior parietal cortex (PPC), the frontal orienting fields (FOF), and the anterior-dorsal striatum (ADS) - while subjects performed a pulse-based accumulation task. Each region was best described by a distinct accumulation model, which all differed from the model that best described the animal's choices. FOF activity was consistent with an accumulator where early evidence was favored while the ADS reflected near perfect accumulation. Neural responses within an accumulation framework unveiled a distinct association between each brain region and choice. Choices were better predicted from all regions using a comprehensive, accumulation-based framework and different brain regions were found to differentially reflect choice-related accumulation signals: FOF and ADS both reflected choice but ADS showed more instances of decision vacillation. Previous studies relating neural data to behaviorally-inferred accumulation dynamics have implicitly assumed that individual brain regions reflect the whole-animal level accumulator. Our results suggest that different brain regions represent accumulated evidence in dramatically different ways and that accumulation at the whole-animal level may be constructed from a variety of neural-level accumulators.

Data availability

All data analyzed during this study and original analysis computer code has been deposited at https://github.com/Brody-Lab/DePasquale-eLife-2022 and is publicly available. Additional original analysis code has been deposited at https://github.com/Brody-Lab/PulseInputDDM and is publicly available.

The following previously published data sets were used

1. Hanks TD
2. Kopec CD
3. Brunton BW
4. Duan CA
5. Erlich JC
6. Brody CD
(2015) Data from: Distinct relationships of parietal and prefrontal cortices to evidence accumulation
https://github.com/Brody-Lab/DePasquale-eLife-2022.

https://github.com/Brody-Lab/DePasquale-eLife-2022
1. Yartsev MM
2. Hanks TD
3. Yoon AM
4. Brody CD
(2018) Data from: Causal contribution and dynamical encoding in the striatum during evidence accumulation
https://github.com/Brody-Lab/DePasquale-eLife-2022.

https://github.com/Brody-Lab/DePasquale-eLife-2022

Article and author information

Author details

Brian DePasquale

Princeton Neuroscience Institute, Princeton University, Princeton, United States

For correspondence
depasquale@princeton.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-3830-3184
Carlos D Brody

Princeton University, Howard Hughes Medical Institute, Princeton, United States

For correspondence
brody@princeton.edu

Competing interests
Carlos D Brody, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-4201-561X
Jonathan W Pillow

Department of Psychology, Princeton University, Princeton, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-3638-8831

Funding

Simons Foundation (SCGB AWD543027 and AWD542593)

Carlos D Brody

National Institute of Neurological Disorders and Stroke (BRAIN Initiative Award 5U19NS104648-02)

Carlos D Brody

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.