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Focal neocortical lesions impair distant neuronal information processing

Wahlbom, Anders LU ; Enander, Jonas M.D. LU ; Bengtsson, Fredrik LU and Jörntell, Henrik LU (2019) In Journal of Physiology 597(16). p.4357-4371
Abstract

Key points: Parts of the fields of neuroscience and neurology consider the neocortex to be a functionally parcelled structure. Viewed through such a conceptual filter, there are multiple clinical observations after localized stroke lesions that seem paradoxical. We tested the effect that localized stroke-like lesions have on neuronal information processing in a part of the neocortex that is distant to the lesion using animal experiments. We find that the distant lesion degrades the quality of neuronal information processing of tactile input patterns in primary somatosensory cortex. The findings suggest that even the processing of primary sensory information depends on an intact neocortical network, with the implication that all... (More)

Key points: Parts of the fields of neuroscience and neurology consider the neocortex to be a functionally parcelled structure. Viewed through such a conceptual filter, there are multiple clinical observations after localized stroke lesions that seem paradoxical. We tested the effect that localized stroke-like lesions have on neuronal information processing in a part of the neocortex that is distant to the lesion using animal experiments. We find that the distant lesion degrades the quality of neuronal information processing of tactile input patterns in primary somatosensory cortex. The findings suggest that even the processing of primary sensory information depends on an intact neocortical network, with the implication that all neocortical processing may rely on widespread interactions across large parts of the cortex. 

Abstract: Recent clinical studies report a surprisingly weak relationship between the location of cortical brain lesions and the resulting functional deficits. From a neuroscience point of view, such findings raise questions as to what extent functional localization applies in the neocortex and to what extent the functions of different regions depend on the integrity of others. Here we provide an in-depth analysis of the changes in the function of the neocortical neuronal networks after distant focal stroke-like lesions in the anaesthetized rat. Using a recently introduced high resolution analysis of neuronal information processing, consisting of pre-set spatiotemporal patterns of tactile afferent activation against which the neuronal decoding performance can be quantified, we found that stroke-like lesions in distant parts of the cortex significantly degraded the decoding performance of individual neocortical neurons in the primary somatosensory cortex (decoding performance decreased from 30.9% to 24.2% for n = 22 neurons, Wilcoxon signed rank test, P = 0.028). This degrading effect was not due to changes in the firing frequency of the neuron (Wilcoxon signed rank test, P = 0.499) and was stronger the higher the decoding performance of the neuron, indicating a specific impact on the information processing capacity in the cortex. These findings suggest that even primary sensory processing depends on widely distributed cortical networks and could explain observations of focal stroke lesions affecting a large range of functions.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
information processing, Neocortex, neuron, parietal cortex, photothrombosis, somatosensory cortex, spreading depression, stroke, tactile, touch
in
Journal of Physiology
volume
597
issue
16
pages
4357 - 4371
publisher
The Physiological Society
external identifiers
  • scopus:85069718893
  • pmid:31342538
ISSN
0022-3751
DOI
10.1113/JP277717
language
English
LU publication?
yes
id
c71d121c-cb00-4c27-8a2e-a0e233089545
date added to LUP
2019-08-09 15:15:23
date last changed
2020-02-19 05:37:42
@article{c71d121c-cb00-4c27-8a2e-a0e233089545,
  abstract     = {<p>Key points: Parts of the fields of neuroscience and neurology consider the neocortex to be a functionally parcelled structure. Viewed through such a conceptual filter, there are multiple clinical observations after localized stroke lesions that seem paradoxical. We tested the effect that localized stroke-like lesions have on neuronal information processing in a part of the neocortex that is distant to the lesion using animal experiments. We find that the distant lesion degrades the quality of neuronal information processing of tactile input patterns in primary somatosensory cortex. The findings suggest that even the processing of primary sensory information depends on an intact neocortical network, with the implication that all neocortical processing may rely on widespread interactions across large parts of the cortex. </p><p>Abstract: Recent clinical studies report a surprisingly weak relationship between the location of cortical brain lesions and the resulting functional deficits. From a neuroscience point of view, such findings raise questions as to what extent functional localization applies in the neocortex and to what extent the functions of different regions depend on the integrity of others. Here we provide an in-depth analysis of the changes in the function of the neocortical neuronal networks after distant focal stroke-like lesions in the anaesthetized rat. Using a recently introduced high resolution analysis of neuronal information processing, consisting of pre-set spatiotemporal patterns of tactile afferent activation against which the neuronal decoding performance can be quantified, we found that stroke-like lesions in distant parts of the cortex significantly degraded the decoding performance of individual neocortical neurons in the primary somatosensory cortex (decoding performance decreased from 30.9% to 24.2% for n = 22 neurons, Wilcoxon signed rank test, P = 0.028). This degrading effect was not due to changes in the firing frequency of the neuron (Wilcoxon signed rank test, P = 0.499) and was stronger the higher the decoding performance of the neuron, indicating a specific impact on the information processing capacity in the cortex. These findings suggest that even primary sensory processing depends on widely distributed cortical networks and could explain observations of focal stroke lesions affecting a large range of functions.</p>},
  author       = {Wahlbom, Anders and Enander, Jonas M.D. and Bengtsson, Fredrik and Jörntell, Henrik},
  issn         = {0022-3751},
  language     = {eng},
  month        = {07},
  number       = {16},
  pages        = {4357--4371},
  publisher    = {The Physiological Society},
  series       = {Journal of Physiology},
  title        = {Focal neocortical lesions impair distant neuronal information processing},
  url          = {http://dx.doi.org/10.1113/JP277717},
  doi          = {10.1113/JP277717},
  volume       = {597},
  year         = {2019},
}