Short-term brain ‘plasticity’ in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia

doi:10.1016/0006-8993(94)90919-9

Brain Research

Volume 642, Issues 1–2, 11 April 1994, Pages 169-177

https://doi.org/10.1016/0006-8993(94)90919-9 Get rights and content

Abstract

Transient rearrangements of finger representation in primary somatosensory cortex induced by an anesthetic block of the sensory information from adjacent fingers have been shown invasively in animals. Such a phenomenon has been now replicated in seven healthy human volunteers. Somatosensory Evoked Fields (SEFs) have been recorded during separate electrical stimulation of the 1st, 3rd, or 5th finger. Recordings were obtained in control conditions (stage A), following complete ischemic anesthesia of the 4 non-stimulated fingers (stage B), and after regaining sensation (stage C). SEFs were recorded using a 28-channel DC-SQUID magnetometer; a single position of the sensor was enough to identify the source of N20m, P30m and following components using the Equivalent Current Dipole (ECD) model. The amount of afferent input during stages A through C was monitored with surface electrodes placed on the nerve at wrist and elbow. No variation of the nerve compound potential was observed during stages A through C. In stage A, the localizing algorithm was able to discriminate the individual finger representation in accordance with the somatotopic organisation of the sensory homunculus. It was observed that the ECDs responsible for the cortical responses from the unanesthetized finger were significantly changing following a relatively brief period of sensory deprivation from the adjacent fingers. Such changes of the ECDs with respect to the control conditions were characterized by an increase in strength and deepening for the middle finger, and by a shift on the coronal plane for the thumb and the little finger (medial for the former, lateral for the latter). Such changes became progressively evident in stage B, but were persisting in stage C.

Reference (31)

AsanumaC.
Mapping movements within a moving motor map
Trends Neurol. Sci.
(1991)
DesmedtJ.E. et al.
Non-cephalic reference recording early somatosensory potentials to finger stimulation in adult or aging man: differentiation of widespread N18 and contralateral N20 from the prerolandic P22 and N30 components
Electroenceph. Clin. Neurophysiol.
(1981)
HariR. et al.
Spatial resolution of neuromagnetic records: theoretical calculations in a spherical model
Electroenceph. Clin. Neurophysiol.
(1988)
HariR. et al.
Multichannel detection of magnetic compound action fields of median and ulnar nerves
Electroenceph. Clin. Neurophysiol.
(1989)
KelahanA.M. et al.
Functional reorganization of adult racoon somatosensory cerebral cortex following neonatal digit amputation
Brain Res.
(1981)
MerzenichM.M. et al.
Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation
Neuroscience
(1983)
MetzlerJ. et al.
Functional changes in cat somatosensory-motor cortex during short-term reversible epidural blocks
Brain Res.
(1979)
NariciL. et al.
Neuromagnetic somatosensory homunculus: a non-invasive approach in humans
Neurosci. Lett.
(1991)
RasmussonD.D. et al.
Unexpected reorganization of somatosensory cortex in a racoon with extensive forelimb loss
Neurosci. Lett.
(1985)
AllardT. et al.
Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly
J. Neurophysiol.
(1991)

BrownP.B. et al.

Cat hindlimb tactile dermatoms determined with single-unit recordings

J. Neurophysiol.

(1978)

CarsonL.V. et al.

Effects of early peripheral lesions on the somatotopic organization of the cerebral cortex

DevorM. et al.

Plasticity in the spinal cord sensory map following peripheral nerve injury in rats

J. Neurosci.

(1981)

Erne`S.N. et al.

The positioning problem in biomagnetic measurement: a solution for arrays of superconducting sensors

IEEE Trans. Magn.

(1987)

HariR. et al.

Recording and interpretation of cerebral magnetic fields

Science

(1989)

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Short-term brain ‘plasticity’ in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia

Abstract

Trends Neurol. Sci.

Electroenceph. Clin. Neurophysiol.

Electroenceph. Clin. Neurophysiol.

Electroenceph. Clin. Neurophysiol.

Brain Res.

Neuroscience

Brain Res.

Neurosci. Lett.

Neurosci. Lett.

Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly

J. Neurophysiol.

Cat hindlimb tactile dermatoms determined with single-unit recordings

J. Neurophysiol.

Effects of early peripheral lesions on the somatotopic organization of the cerebral cortex

Plasticity in the spinal cord sensory map following peripheral nerve injury in rats

J. Neurosci.

The positioning problem in biomagnetic measurement: a solution for arrays of superconducting sensors

IEEE Trans. Magn.

Recording and interpretation of cerebral magnetic fields

Science