Research reportShort-term plasticity of the human auditory cortex
Introduction
Several previous experiments have demonstrated that the functional organization of sensory maps is not statically fixed in adult cortex 9, 12, 13, 15, 18, 27, 28, 29. Early studies in animals utilized large and permanent changes of afferent sensory input, such as amputation of a forelimb 14, 19, 24or mechanical destruction of part of the cochlea 12, 25, 26, 32. The findings showed that cortical regions that have lost their normal input take over and serve functions found in adjacent cortical areas 25, 33. Using magnetoencephalography (MEG) which allows non-invasive measurement in human subjects, changes in cortical maps similar to those observed in primate cortex have been demonstrated in patients with limb amputations and finger syndactyly 4, 5, 20, 36.
Most studies of deafferentation-induced cortical reorganization including those just mentioned have investigated cortical reorganization on a time scale of days to weeks or more. However, other more recent studies have documented rapid changes in cortical dynamics following deafferentation. These studies have shown that neurons broaden and shift their receptive fields to sensory surfaces near or beyond the edge of the lesioned zone within a few minutes of deafferentation in the somatosensory [3]and visual [7]systems, and within hours in the auditory system [30]. Rapid retuning of sensory neurons has also been observed following reversible “functional” deafferentations in which sensory input from the environment is altered by procedures such as artificial scotomas [8]or digit ligation [31]rather than by permanent lesions of the receptor organs. Rapid expansion of receptive fields induced by lesioning or functional deafferentation appears to reflect an unmasking of existing excitatory connections when lateral inhibition is withdrawn following deafferentation [37]. However, because rapid changes in cortical dynamics continue to develop for an hour or more after deafferentation and are sensitive NMDA receptor blockade, plastic changes in synaptic efficacy have also been implicated. These observations suggest that cortical remodelling induced by deafferentation may be mediated by mechanisms similar to those activated by behavioral training which has been shown to alter the tuning of somatosensory [2]and auditory 34, 35cortical neurons within minutes to hours.
The objective of the present study was to determine whether plastic changes of frequency representation occur on a short time scale of a few hours when the adult human auditory cortex is deprived of sensory input. Subjects listened for 3 h to music notched at a narrow frequency band centered at 1 kHz. Immediately before and after listening to the notched music, auditory cortical representations were measured neuromagnetically for a “test” stimulus of 1 kHz centered on the notched region and a “control” stimulus of 0.5 kHz.
Section snippets
Subjects
Three female and seven male subjects aged between 25 and 50 years (median 31 years) with no history of otological or neurological disorders participated in the study. A normal audiological status was assured with air and bone conduction thresholds of no more than 10 dB hearing level in the range from 250 to 8000 Hz. All subjects were right-handed according to the Edinburgh handedness questionnaire [21]. Informed consent was obtained from each subject after explaining to her/him the nature of
Results
The comparison of the field amplitudes of selected MEG channels or of the RMS value for the sensor array before and after 3 h of listening to notched music is acceptable only if the position of the head with respect to the sensor array is more or less constant between the two measurement periods. Therefore, special efforts (retention of the evacuated vacuum cushion between measurements and photographs of head position) were made to achieve this relative constancy. The grand average of the
Discussion
Animal studies have shown that removing spectral input by cochlear lesions is followed by a shift in the tuning of deafferented neurons in the auditory projection pathway to frequencies adjacent to the lesioned area 11, 25, 32. The present MEG study examined the effect of “functionally” deafferenting the human auditory system. The effect of functional deafferentation was most evident in field patterns that were adequately modeled by a single ECD. Overall, the strength of the cortical source (Q)
Acknowledgements
Supported by grants from the Deutsche Forschungsgemeinschaft (Pa 392/6-2) and the Medical Research Council of Canada (MT14033, L.R.).
References (37)
- et al.
Long-term potentiation trains induce mossy fiber sprouting
Brain Res.
(1997) - et al.
Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity
Brain Res. Brain Res. Rev.
(1997) - et al.
Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation
Neuroscience
(1983) The assessment and analysis of handedness: the Edinburgh inventory
Neurophysiologia
(1971)Compensatory plasticity and sensory substitution in the cerebral cortex
Trends Neurosci.
(1995)- et al.
Short-term brain plasticity in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia
Brain Res.
(1994) - et al.
Laminar comparison of somatosensory cortical plasticity
Science
(1994) - et al.
Short-term plasticity in primary somatosensory cortex of the rat: rapid changes in magnitudes and latencies of neuronal responses following digit denervation
Exp. Brain Res.
(1996) - et al.
Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury
NeuroReport
(1994) - et al.
Phantom limb pain as a perceptual correlate of massive cortical reorganization in upper limp amputees
Nature
(1995)