Experience–dependent modulation of tonotopic neural responses in human auditory cortex

Experience–dependent plasticity of receptive fields in the auditory cortex has been demonstrated by electrophysiological experiments in animals. In the present study we used PET neuroimaging to measure regional brain activity in volunteer human subjects during discriminatory classical conditioning of high (8000 Hz) or low (200 Hz) frequency tones by an aversive 100 dB white noise burst. Conditioning–related, frequency–specific modulation of tonotopic neural responses in the auditory cortex was observed. The modulated regions of the auditory cortex positively covaried with activity in the amygdala, basal forebrain and orbitofrontal cortex, and showed context–specific functional interactions with the medial geniculate nucleus. These results accord with animal single–unit data and support neurobiological models of auditory conditioning and value–dependent neural selection.

[1]  J. Edeline,et al.  Thalamic short-term plasticity in the auditory system: associative returning of receptive fields in the ventral medial geniculate body. , 1991, Behavioral neuroscience.

[2]  A Sakaguchi,et al.  Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  R. Racine,et al.  Kindling mechanisms: Current progress on an experimental epilepsy model , 1986, Progress in Neurobiology.

[4]  J. Price,et al.  The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat , 1977, The Journal of comparative neurology.

[5]  Karl J. Friston,et al.  Neural responses to salient visual stimuli , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Joseph E LeDoux,et al.  Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat , 1985, The Journal of comparative neurology.

[7]  J. Edeline,et al.  Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. , 1993, Behavioral neuroscience.

[8]  D. Diamond,et al.  Physiological plasticity in auditory cortex: Rapid induction by learning , 1987, Progress in Neurobiology.

[9]  Norman M. Weinberger,et al.  Retuning the brain by fear conditioning. , 1995 .

[10]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[11]  Joseph E LeDoux,et al.  Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  N. Weinberger,et al.  Cholinergic modulation of frequency receptive fields in auditory cortex: II. Frequency‐specific effects of anticholinesterases provide evidence for a modulatory action of endogenous Ach , 1989, Synapse.

[13]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[14]  D. Pandya,et al.  Frontal lobe connections of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[15]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[16]  J. Edeline,et al.  Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. , 1992, Behavioral neuroscience.

[17]  R. Metherate,et al.  Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors , 1991, Brain Research.

[18]  Edmund T. Rolls,et al.  A theory of emotion and consciousness, and its application to understanding the neural basis of emotion. , 1995 .

[19]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Kaas.  The reorganization of sensory and motor maps after injury in adult mammals , 2000 .

[21]  N. Weinberger,et al.  Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency‐specific effects of muscarinic agonists , 1989, Synapse.

[22]  Larry L. Butcher,et al.  Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: A combined fluorescent tracer and acetylcholinesterase analysis , 1982, Brain Research Bulletin.

[23]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[24]  A R McIntosh,et al.  Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. , 1997, Journal of neurophysiology.

[25]  F. Ohl,et al.  Functional organization and learning-related plasticity in auditory cortex of the Mongolian gerbil. , 1993, Progress in brain research.

[26]  A. McIntosh,et al.  Functional network interactions between parallel auditory pathways during Pavlovian conditioned inhibition , 1995, Brain Research.

[27]  Karl J. Friston,et al.  Value-dependent selection in the brain: Simulation in a synthetic neural model , 1994, Neuroscience.

[28]  K. Fox,et al.  A critical period for experience-dependent synaptic plasticity in rat barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[30]  J. Edeline,et al.  Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat , 1993, Neuroscience.

[31]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[32]  D. Amaral,et al.  The amygdalostriatal projections in the monkey. An anterograde tracing study , 1985, Brain Research.

[33]  J. D. Nichols,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. , 1997, Science.

[34]  E. Rolls.  A Theory of Emotion, and its Application to Understanding the Neural Basis of Emotion , 1990 .

[35]  B. Rockstroh,et al.  Increased Cortical Representation of the Fingers of the Left Hand in String Players , 1995, Science.

[36]  N. Weinberger,et al.  Cholinergic modulation of responses to single tones produces tone‐specific receptive field alterations in cat auditory cortex , 1990, Synapse.

[37]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  A. Levey,et al.  Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey , 1983, The Journal of comparative neurology.

[39]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[40]  C. Pantev,et al.  Tonotopic organization of the sources of human auditory steady-state responses , 1996, Hearing Research.

[41]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[42]  D. Cohen.  The Neural Pathways and Informational Flow Mediating a Conditioned Autonomic Response , 1974 .

[43]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[44]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[45]  J. Price,et al.  A direct input from the amygdala to the thalamus and the cerebral cortex. , 1974, Brain research.

[46]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[47]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[48]  M. Davis,et al.  Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  T. Robbins,et al.  A specific form of cognitive rigidity following excitotoxic lesions of the basal forebrain in marmosets , 1992, Neuroscience.