Literature DB >> 35606141

Mapping the Integration of Sensory Information across Fingers in Human Sensorimotor Cortex.

Spencer A Arbuckle1, J Andrew Pruszynski2,3,4, Jörn Diedrichsen1,5.   

Abstract

The integration of somatosensory signals across fingers is essential for dexterous object manipulation. Previous experiments suggest that this integration occurs in neural populations in the primary somatosensory cortex (S1). However, the integration process has not been fully characterized, as previous studies have mainly used 2-finger stimulation paradigms. Here, we addressed this gap by stimulating all 31 single- and multifinger combinations. We measured population-wide activity patterns evoked during finger stimulation in human S1 and primary motor cortex (M1) using 7T fMRI in female and male participants. Using multivariate fMRI analyses, we found clear evidence of unique nonlinear interactions between fingers. In Brodmann area (BA) 3b, interactions predominantly occurred between pairs of neighboring fingers. In BA 2, however, we found equally strong interactions between spatially distant fingers, as well as interactions between finger triplets and quadruplets. We additionally observed strong interactions in the hand area of M1. In both M1 and S1, these nonlinear interactions did not reflect a general suppression of overall activity, suggesting instead that the interactions we observed reflect rich, nonlinear integration of sensory inputs from the fingers. We suggest that this nonlinear finger integration allows for a highly flexible mapping from finger sensory inputs to motor responses that facilitates dexterous object manipulation.SIGNIFICANCE STATEMENT Processing of somatosensory information in primary somatosensory cortex (S1) is essential for dexterous object manipulation. To successfully handle an object, the sensorimotor system needs to detect complex patterns of haptic information, which requires the nonlinear integration of sensory inputs across multiple fingers. Using multivariate fMRI analyses, we characterized brain activity patterns evoked by stimulating all single- and multifinger combinations. We report that progressively stronger multifinger interactions emerge in posterior S1 and in the primary motor cortex (M1), with interactions arising between inputs from neighboring and spatially distant fingers. Our results suggest that S1 and M1 provide the neural substrate necessary to support a flexible mapping from sensory inputs to motor responses of the hand.
Copyright © 2022 the authors.

Entities:  

Keywords:  fMRI; fingers; hand; primary motor cortex; primary somatosensory cortex; sensory integration

Mesh:

Year:  2022        PMID: 35606141      PMCID: PMC9236287          DOI: 10.1523/JNEUROSCI.2152-21.2022

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.709


  63 in total

1.  Interaction of tactile input in the human primary and secondary somatosensory cortex--a magnetoencephalographic study.

Authors:  K Hoechstetter; A Rupp; A Stancák; H M Meinck; C Stippich; P Berg; M Scherg
Journal:  Neuroimage       Date:  2001-09       Impact factor: 6.556

2.  Image distortion correction in fMRI: A quantitative evaluation.

Authors:  Chloe Hutton; Andreas Bork; Oliver Josephs; Ralf Deichmann; John Ashburner; Robert Turner
Journal:  Neuroimage       Date:  2002-05       Impact factor: 6.556

3.  Receptive field integration and submodality convergence in the hand area of the post-central gyrus of the alert monkey.

Authors:  J Hyvärinen; A Poranen
Journal:  J Physiol       Date:  1978-10       Impact factor: 5.182

4.  Sub-area-specific Suppressive Interaction in the BOLD responses to simultaneous finger stimulation in human primary somatosensory cortex: evidence for increasing rostral-to-caudal convergence.

Authors:  Jan Ruben; Thomas Krause; Birol Taskin; Felix Blankenburg; Matthias Moosmann; Arno Villringer
Journal:  Cereb Cortex       Date:  2005-09-14       Impact factor: 5.357

5.  Sensory information from a slipping object elicits a rapid and automatic shoulder response.

Authors:  Carlos R Hernandez-Castillo; Rodrigo S Maeda; J Andrew Pruszynski; Jörn Diedrichsen
Journal:  J Neurophysiol       Date:  2020-02-19       Impact factor: 2.714

6.  Representation of tactile curvature in macaque somatosensory area 2.

Authors:  Jeffrey M Yau; Charles E Connor; Steven S Hsiao
Journal:  J Neurophysiol       Date:  2013-03-27       Impact factor: 2.714

7.  The somatotopic pattern of afferent projections from the digits to the spinal cord and cuneate nucleus in macaque monkeys.

Authors:  S L Florence; J T Wall; J H Kaas
Journal:  Brain Res       Date:  1988-06-14       Impact factor: 3.252

8.  Thalamic projections to areas 3a, 3b, and 4 in the sensorimotor cortex of the mature and infant macaque monkey.

Authors:  C Darian-Smith; I Darian-Smith
Journal:  J Comp Neurol       Date:  1993-09-08       Impact factor: 3.215

Review 9.  Normalization as a canonical neural computation.

Authors:  Matteo Carandini; David J Heeger
Journal:  Nat Rev Neurosci       Date:  2011-11-23       Impact factor: 34.870

10.  Elementary motion sequence detectors in whisker somatosensory cortex.

Authors:  Keven J Laboy-Juárez; Tomer Langberg; Seoiyoung Ahn; Daniel E Feldman
Journal:  Nat Neurosci       Date:  2019-07-22       Impact factor: 24.884

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  2 in total

Review 1.  Somatotopic Mapping of the Fingers in the Somatosensory Cortex Using Functional Magnetic Resonance Imaging: A Review of Literature.

Authors:  Daniel Janko; Kristina Thoenes; Dahye Park; W R Willoughby; Meredith Horton; Mark Bolding
Journal:  Front Neuroanat       Date:  2022-06-29       Impact factor: 3.543

2.  Fast Event-Related Mapping of Population Fingertip Tuning Properties in Human Sensorimotor Cortex at 7T.

Authors:  Sarah Khalife; Susan T Francis; Denis Schluppeck; Rosa-Maria Sánchez-Panchuelo; Julien Besle
Journal:  eNeuro       Date:  2022-09-14
  2 in total

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