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Research Articles, Behavioral/Cognitive

Accumulation System: Distributed Neural Substrates of Perceptual Decision Making Revealed by fMRI Deconvolution

Yusuke Morito and Tsutomu Murata
Journal of Neuroscience 12 May 2022, JN-RM-1062-21; DOI: https://doi.org/10.1523/JNEUROSCI.1062-21.2022
Yusuke Morito
1Center for Information and Neural Networks, Advanced ICT Research Institute, National Institute of Information and Communications Technology (NICT), Suita, Osaka 565-0871, Japan
2Center for Biosystems Dynamics Research, RIKEN, Kobe, Hyogo 650-0047, Japan
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Tsutomu Murata
1Center for Information and Neural Networks, Advanced ICT Research Institute, National Institute of Information and Communications Technology (NICT), Suita, Osaka 565-0871, Japan
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Abstract

Neural substrates of evidence accumulation have been a central issue in decision-making studies because of the prominent success of the accumulation model in explaining a wide range of perceptual decision making. Since accumulation-shaped activities have been found in multiple brain regions, which are called accumulators, questions regarding functional relations among these accumulators are emerging. This study employed the deconvolution method of functional magnetic resonance imaging (fMRI) signals from human male and female participants during object-category decision tasks, taking advantage of the whole-brain coverage of fMRI with improved availability of temporal information of the deconvolved activity. We detected the accumulation activity in many non-category-selective regions over the frontal, parietal, and temporal lobes as well as category-selective regions of the categorization task. Importantly, the frontal regions mostly showed activity peaks matching the decision timing (classified as “type-A accumulator”), while activity peaks of the parietal and temporal regions were behind the decision (classified as “type-B accumulator”). The category-selective regions showed activity peaks whose timing depended on both region and stimulus preference, plausibly reflecting the competition among the alternative choices (classified as “type-C accumulator”). The results suggest that these functionally heterogeneous accumulators form a system for evidence accumulation in which the type-A accumulator regions make decisions in a general manner while the type-B and type-C accumulator regions are employed depending on the modality and content of decision tasks. The concept of the accumulation system may provide a key to understanding the universality of the accumulation model over various kinds of decision tasks.

Significance Statement

Perceptual decision making, such as deciding to walk or stop on seeing the signal colors, has been explained theoretically by the accumulation model, in which sensory information is accumulated to reach a certain threshold for making decisions. Neural substrates of this model, however, are still under elucidation among candidate regions found over the brain. We show here that, taking advantage of the whole-brain coverage of fMRI with improving availability of temporal information by deconvolution method, the accumulation is carried out by a system comprising many regions in different abstraction levels and only a part of these regions in the frontal cortex make decisions. The system concept may provide a key to explain the universality of the accumulation model.

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by JSPS KAKENHI Grant Number JP24700421 and MIC Grant Number JPMI00316 of Japan. The authors thank Dr. Daniel Handwerker of National Institute of Mental Health for sharing his data set of BOLD response from Handwerker et al. (2004). We thank the following members of NICT: Prof. Toshio Yanagida and Dr. Takahisa Taguchi for generous support to this study; Dr. Takafumi Suzuki for considerable encouragement; Dr. Hiroshi Toyoda for productive technical advice on data processing; Drs. Makoto Kato and Yasushi Naruse for useful discussion in early phase of this study; Mr. Seishi Itoi for excellent technical support. We are grateful to two anonymous reviewers for their constructive feedback.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Accumulation System: Distributed Neural Substrates of Perceptual Decision Making Revealed by fMRI Deconvolution
Yusuke Morito, Tsutomu Murata
Journal of Neuroscience 12 May 2022, JN-RM-1062-21; DOI: 10.1523/JNEUROSCI.1062-21.2022

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Accumulation System: Distributed Neural Substrates of Perceptual Decision Making Revealed by fMRI Deconvolution
Yusuke Morito, Tsutomu Murata
Journal of Neuroscience 12 May 2022, JN-RM-1062-21; DOI: 10.1523/JNEUROSCI.1062-21.2022
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