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Research Article

Invariant timescale hierarchy across the cortical somatosensory network

View ORCID ProfileRomán Rossi-Pool, View ORCID ProfileAntonio Zainos, Manuel Alvarez, View ORCID ProfileSergio Parra, View ORCID ProfileJerónimo Zizumbo, and Ranulfo Romo
  1. aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
  2. bEl Colegio Nacional, 06020 Mexico City, Mexico

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PNAS January 19, 2021 118 (3) e2021843118; https://doi.org/10.1073/pnas.2021843118
Román Rossi-Pool
aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
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  • ORCID record for Román Rossi-Pool
  • For correspondence: romanr@ifc.unam.mx ranulfo.romo@gmail.com
Antonio Zainos
aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
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  • ORCID record for Antonio Zainos
Manuel Alvarez
aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
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Sergio Parra
aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
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Jerónimo Zizumbo
aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
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  • ORCID record for Jerónimo Zizumbo
Ranulfo Romo
aInstituto de Fisiología Celular–Neurociencias, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico;
bEl Colegio Nacional, 06020 Mexico City, Mexico
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  • For correspondence: romanr@ifc.unam.mx ranulfo.romo@gmail.com
  1. Contributed by Ranulfo Romo, November 27, 2020 (sent for review October 19, 2020; reviewed by Bruno Averbeck and Miguel Maravall)

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Significance

Cortical networks integrate information from different sources during cognitive processes. In doing so, they implement a broad diversity of time constants, constituting an organizational hierarchy. In the somatosensory network, while monkeys perform a highly demanding vibrotactile discrimination task, area 3b depicts a much faster time constant than area 1, both of which are historically included in the primary somatosensory cortex (S1). Timescales are longer in areas downstream to S1. This timescale hierarchy exhibits invariance across task context, neural coding, hemispheres, and response latency. Surprisingly, the vast heterogeneity of neural responses observed in each area is accompanied by homogeneity in timescales. Such homogeneity may be an inherent feature of each processing stage within the cortical somatosensory network.

Abstract

The ability of cortical networks to integrate information from different sources is essential for cognitive processes. On one hand, sensory areas exhibit fast dynamics often phase-locked to stimulation; on the other hand, frontal lobe areas with slow response latencies to stimuli must integrate and maintain information for longer periods. Thus, cortical areas may require different timescales depending on their functional role. Studying the cortical somatosensory network while monkeys discriminated between two vibrotactile stimulus patterns, we found that a hierarchical order could be established across cortical areas based on their intrinsic timescales. Further, even though subareas (areas 3b, 1, and 2) of the primary somatosensory (S1) cortex exhibit analogous firing rate responses, a clear differentiation was observed in their timescales. Importantly, we observed that this inherent timescale hierarchy was invariant between task contexts (demanding vs. nondemanding). Even if task context severely affected neural coding in cortical areas downstream to S1, their timescales remained unaffected. Moreover, we found that these time constants were invariant across neurons with different latencies or coding. Although neurons had completely different dynamics, they all exhibited comparable timescales within each cortical area. Our results suggest that this measure is demonstrative of an inherent characteristic of each cortical area, is not a dynamical feature of individual neurons, and does not depend on task demands.

  • timescale hierarchy
  • behaving monkeys
  • somatosensory network
  • inherent time constants
  • primary somatosensory cortex

Footnotes

  • ↵1To whom correspondence may be addressed. Email: romanr{at}ifc.unam.mx or ranulfo.romo{at}gmail.com.
  • Author contributions: R.R.-P. and R.R. designed research; A.Z., M.A., and R.R. performed research; R.R.-P., S.P., and J.Z. analyzed data; R.R.-P., S.P., J.Z., and R.R. wrote the paper; and R.R.-P. and R.R. supervised all stages of the study.

  • Reviewers: B.A., National Institute of Mental Health; and M.M., University of Sussex.

  • The authors declare no competing interest.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2021843118/-/DCSupplemental.

Data Availability.

Data files are publicly available at Zenodo (DOI: 10.5281/zenodo.4421855); see reference (52).

Published under the PNAS license.

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Invariant timescale hierarchy across the cortical somatosensory network
Román Rossi-Pool, Antonio Zainos, Manuel Alvarez, Sergio Parra, Jerónimo Zizumbo, Ranulfo Romo
Proceedings of the National Academy of Sciences Jan 2021, 118 (3) e2021843118; DOI: 10.1073/pnas.2021843118

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Invariant timescale hierarchy across the cortical somatosensory network
Román Rossi-Pool, Antonio Zainos, Manuel Alvarez, Sergio Parra, Jerónimo Zizumbo, Ranulfo Romo
Proceedings of the National Academy of Sciences Jan 2021, 118 (3) e2021843118; DOI: 10.1073/pnas.2021843118
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