Literature DB >> 32839338

Multiple timescales of neural dynamics and integration of task-relevant signals across cortex.

Mehran Spitmaan1, Hyojung Seo2, Daeyeol Lee3,4,5,6, Alireza Soltani7.   

Abstract

A long-lasting challenge in neuroscience has been to find a set of principles that could be used to organize the brain into distinct areas with specific functions. Recent studies have proposed the orderly progression in the time constants of neural dynamics as an organizational principle of cortical computations. However, relationships between these timescales and their dependence on response properties of individual neurons are unknown, making it impossible to determine how mechanisms underlying such a computational principle are related to other aspects of neural processing. Here, we developed a comprehensive method to simultaneously estimate multiple timescales in neuronal dynamics and integration of task-relevant signals along with selectivity to those signals. By applying our method to neural and behavioral data during a dynamic decision-making task, we found that most neurons exhibited multiple timescales in their response, which consistently increased from parietal to prefrontal and cingulate cortex. While predicting rates of behavioral adjustments, these timescales were not correlated across individual neurons in any cortical area, resulting in independent parallel hierarchies of timescales. Additionally, none of these timescales depended on selectivity to task-relevant signals. Our results not only suggest the existence of multiple canonical mechanisms for increasing timescales of neural dynamics across cortex but also point to additional mechanisms that allow decorrelation of these timescales to enable more flexibility.

Keywords:  neural heterogeneity; prefrontal cortex; reward integration

Mesh:

Year:  2020        PMID: 32839338      PMCID: PMC7486728          DOI: 10.1073/pnas.2005993117

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  40 in total

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Journal:  Perception       Date:  1998       Impact factor: 1.490

Review 2.  Architectonic Mapping of the Human Brain beyond Brodmann.

Authors:  Katrin Amunts; Karl Zilles
Journal:  Neuron       Date:  2015-12-16       Impact factor: 17.173

3.  Cortical signals for rewarded actions and strategic exploration.

Authors:  Christopher H Donahue; Hyojung Seo; Daeyeol Lee
Journal:  Neuron       Date:  2013-09-05       Impact factor: 17.173

Review 4.  Macroscopic gradients of synaptic excitation and inhibition in the neocortex.

Authors:  Xiao-Jing Wang
Journal:  Nat Rev Neurosci       Date:  2020-02-06       Impact factor: 34.870

5.  A Large-Scale Circuit Mechanism for Hierarchical Dynamical Processing in the Primate Cortex.

Authors:  Rishidev Chaudhuri; Kenneth Knoblauch; Marie-Alice Gariel; Henry Kennedy; Xiao-Jing Wang
Journal:  Neuron       Date:  2015-10-01       Impact factor: 17.173

6.  Lateral intraparietal cortex and reinforcement learning during a mixed-strategy game.

Authors:  Hyojung Seo; Dominic J Barraclough; Daeyeol Lee
Journal:  J Neurosci       Date:  2009-06-03       Impact factor: 6.167

7.  Demixed principal component analysis of neural population data.

Authors:  Dmitry Kobak; Wieland Brendel; Christos Constantinidis; Claudia E Feierstein; Adam Kepecs; Zachary F Mainen; Xue-Lian Qi; Ranulfo Romo; Naoshige Uchida; Christian K Machens
Journal:  Elife       Date:  2016-04-12       Impact factor: 8.140

8.  Autocorrelation structure at rest predicts value correlates of single neurons during reward-guided choice.

Authors:  Sean E Cavanagh; Joni D Wallis; Steven W Kennerley; Laurence T Hunt
Journal:  Elife       Date:  2016-10-05       Impact factor: 8.140

9.  Intrinsic neuronal dynamics predict distinct functional roles during working memory.

Authors:  D F Wasmuht; E Spaak; T J Buschman; E K Miller; M G Stokes
Journal:  Nat Commun       Date:  2018-08-29       Impact factor: 14.919

10.  Partitioning neuronal variability.

Authors:  Robbe L T Goris; J Anthony Movshon; Eero P Simoncelli
Journal:  Nat Neurosci       Date:  2014-04-28       Impact factor: 24.884

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  15 in total

1.  Multiple timescales of neural dynamics and integration of task-relevant signals across cortex.

Authors:  Mehran Spitmaan; Hyojung Seo; Daeyeol Lee; Alireza Soltani
Journal:  Proc Natl Acad Sci U S A       Date:  2020-08-24       Impact factor: 11.205

2.  Inhibitory control of frontal metastability sets the temporal signature of cognition.

Authors:  Vincent Fontanier; Matthieu Sarazin; Bruno Delord; Emmanuel Procyk; Frederic M Stoll
Journal:  Elife       Date:  2022-05-30       Impact factor: 8.713

Review 3.  The brain and its time: intrinsic neural timescales are key for input processing.

Authors:  Mehrshad Golesorkhi; Javier Gomez-Pilar; Federico Zilio; Nareg Berberian; Annemarie Wolff; Mustapha C E Yagoub; Georg Northoff
Journal:  Commun Biol       Date:  2021-08-16

4.  Value signals guide abstraction during learning.

Authors:  Aurelio Cortese; Asuka Yamamoto; Maryam Hashemzadeh; Pradyumna Sepulveda; Mitsuo Kawato; Benedetto De Martino
Journal:  Elife       Date:  2021-07-13       Impact factor: 8.140

Review 5.  Interactions between ventrolateral prefrontal and anterior cingulate cortex during learning and behavioural change.

Authors:  Ilya E Monosov; Matthew F S Rushworth
Journal:  Neuropsychopharmacology       Date:  2021-07-07       Impact factor: 7.853

6.  Moving a Shape behind a Slit: Partial Shape Representations in Inferior Temporal Cortex.

Authors:  Anna Bognár; Rufin Vogels
Journal:  J Neurosci       Date:  2021-06-15       Impact factor: 6.167

7.  Timescales of Cognition in the Brain.

Authors:  Alireza Soltani; John D Murray; Hyojung Seo; Daeyeol Lee
Journal:  Curr Opin Behav Sci       Date:  2021-03-31

8.  Invariant timescale hierarchy across the cortical somatosensory network.

Authors:  Román Rossi-Pool; Antonio Zainos; Manuel Alvarez; Sergio Parra; Jerónimo Zizumbo; Ranulfo Romo
Journal:  Proc Natl Acad Sci U S A       Date:  2021-01-19       Impact factor: 12.779

Review 9.  A Diversity of Intrinsic Timescales Underlie Neural Computations.

Authors:  Sean E Cavanagh; Laurence T Hunt; Steven W Kennerley
Journal:  Front Neural Circuits       Date:  2020-12-21       Impact factor: 3.492

10.  Slower prefrontal metastable dynamics during deliberation predicts error trials in a distance discrimination task.

Authors:  Danilo Benozzo; Giancarlo La Camera; Aldo Genovesio
Journal:  Cell Rep       Date:  2021-04-06       Impact factor: 9.423

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