Pharmacological modulation of learning-induced plasticity in human auditory cortex.

PURPOSE Converging evidence from animals and humans indicate that the primary auditory cortex is continuously reshaped in an experience-dependent way. Reorganisation in primary auditory cortex can be observed at the level of receptive fields, topographic maps and brain activations measured with neuroimaging methods. Several neuromodulatory systems were shown to contribute to such an experience-dependent reorganization. METHODS This paper reviews evidence addressing the cholinergic, noradrenergic, dopaminergic and serotonergic modulation of learning-, experience-, and injury-induced plasticity in the auditory cortex. RESULTS Regarding learning-induced plasticity in the auditory cortex most studies have investigated the role of the cholinergic system and shown that ACh is essential for this form of rapid plasticity. Nevertheless there is also evidence that the catecholamines dopamine and noradrenaline might contribute to learning- and experience-induced changes in the auditory cortex. CONCLUSIONS I suggest, that the available experimental data on cholinergic and noradrenergic modulation of plasticity offers a promising basis for potential pharmacological interventions to aid recovery of aural functions.

[1]  Ramesh Rajan,et al.  Injury- and Use-Related Plasticity in Adult Auditory Cortex , 2001, Audiology and Neurotology.

[2]  A Poremba,et al.  Classical conditioning modifies cytochrome oxidase activity in the auditory system , 1998, The European journal of neuroscience.

[3]  Pienie Zwitserlood,et al.  D-Amphetamine Boosts Language Learning Independent of its Cardiovascular and Motor Arousing Effects , 2004, Neuropsychopharmacology.

[4]  T Wüstenberg,et al.  Short-term functional plasticity in the human auditory cortex: an fMRI study. , 2001, Brain research. Cognitive brain research.

[5]  M. Tuszynski,et al.  The Basal Forebrain Cholinergic System Is Essential for Cortical Plasticity and Functional Recovery following Brain Injury , 2005, Neuron.

[6]  L. Cohen,et al.  Improved motor skill acquisition after selective stimulation of central norepinephrine , 2004, Neurology.

[7]  D. M. Feeney,et al.  Intraventricular norepinephrine facilitates motor recovery following sensorimotor cortex injury , 1990, Pharmacology Biochemistry and Behavior.

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

[9]  F. Chollet,et al.  Fluoxetine modulates motor performance and cerebral activation of patients recovering from stroke , 2001, Annals of neurology.

[10]  S. Knecht,et al.  A shift of paradigm: From noradrenergic to dopaminergic modulation of learning? , 2006, Journal of the Neurological Sciences.

[11]  S. Kähkönen Magnetoencephalography (MEG): a non-invasive tool for studying cortical effects in psychopharmacology. , 2006, The international journal of neuropsychopharmacology.

[12]  Joseph Classen,et al.  Modulation of use-dependent plasticity by d-amphetamine. , 2002, Annals of neurology.

[13]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[14]  J. Edeline,et al.  Effects of Noradrenaline on Frequency Tuning of Rat Auditory Cortex Neurons , 1997, The European journal of neuroscience.

[15]  F E Bloom,et al.  Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. , 1978, Annual review of neuroscience.

[16]  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.

[17]  Norman M Weinberger,et al.  Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  N. Weinberger Specific long-term memory traces in primary auditory cortex , 2004, Nature Reviews Neuroscience.

[19]  Satrajit S. Ghosh,et al.  Representation of sound categories in auditory cortical maps. , 2004, Journal of speech, language, and hearing research : JSLHR.

[20]  N. Weinberger,et al.  Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. , 1991, Behavioral neuroscience.

[21]  G L Gerstein,et al.  Daily variation and appetitive conditioning‐induced plasticity of auditory cortex receptive fields , 2001, The European journal of neuroscience.

[22]  R. Dykes,et al.  Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. , 1990, Journal of neurophysiology.

[23]  J. Bakin,et al.  Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Edeline,et al.  Effects of noradrenaline on rate-level function of auditory cortex neurons: Is there a “gating” effect of noradrenaline? , 1998, Experimental Brain Research.

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

[26]  B. Schreurs,et al.  A functional anatomical study of associative learning in humans. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[27]  D. Hovda,et al.  Reinstatement of binocular depth perception by amphetamine and visual experience after visual cortex ablation , 1985, Brain Research.

[28]  Norman M. Weinberger,et al.  Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning. , 1996 .

[29]  D. Irvine,et al.  Perceptual learning on an auditory frequency discrimination task by cats: association with changes in primary auditory cortex. , 2004, Cerebral cortex.

[30]  K. Krnjević,et al.  Iontophoretic studies of neurones in the mammalian cerebral cortex , 1963, The Journal of physiology.

[31]  S. Eksborg,et al.  Drugs for Stroke Recovery , 2004, Drugs & Aging.

[32]  R. Dolan,et al.  Effects of cholinergic enhancement on conditioning‐related responses in human auditory cortex , 2002, The European journal of neuroscience.

[33]  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.

[34]  Henning Scheich,et al.  Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity , 1986, Behavioural Brain Research.

[35]  N. Weinberger,et al.  Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[36]  E. Bullmore,et al.  Human pharmacological MRI. , 2004, Trends in pharmacological sciences.

[37]  Hugh J. McDermott,et al.  Injury-induced reorganization in adult auditory cortex and its perceptual consequences , 2000, Hearing Research.

[38]  N. Weinberger,et al.  Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity , 2001, Neuroreport.

[39]  Selene Cansino,et al.  Neuromagnetic fields reveal cortical plasticity when learning an auditory discrimination task , 1997, Brain Research.

[40]  Norman M. Weinberger,et al.  Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig , 1990, Brain Research.

[41]  N. Weinberger,et al.  Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex , 1989, Brain Research.

[42]  T. Tsumoto,et al.  A functional role of cholinergic innervation to neurons in the cat visual cortex. , 1987, Journal of neurophysiology.

[43]  D. M. Feeney,et al.  Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. , 1982, Science.

[44]  C. Pantev,et al.  Cortical reorganization in patients with high frequency cochlear hearing loss , 2001, Hearing Research.

[45]  T. M. Barth,et al.  Amphetamine and task-specific practice augment recovery of vibrissae-evoked forelimb placing after unilateral sensorimotor cortical injury in the rat. , 1997, Journal of neurotrauma.

[46]  M. Merzenich,et al.  Cortical remodelling induced by activity of ventral tegmental dopamine neurons , 2001, Nature.

[47]  B. Pleger,et al.  Amphetamine enhances training‐induced motor cortex plasticity , 2004, Acta neurologica Scandinavica.

[48]  M. Kilgard Cortical Map Reorganization without Cholinergic Modulation , 2005, Neuron.

[49]  F. Müller,et al.  Effect of levodopa in combination with physiotherapy on functional motor recovery after stroke: a prospective, randomised, double-blind study , 2001, The Lancet.

[50]  S. Juliano,et al.  Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Karl J. Friston,et al.  Cholinergic Modulation of Experience-Dependent Plasticity in Human Auditory Cortex , 2002, Neuron.

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

[53]  K. Krnjević,et al.  Acetylcholine‐sensitive cells in the cerebral cortex , 1963, The Journal of physiology.

[54]  J. Edeline,et al.  Rapid development of learning-induced receptive field plasticity in the auditory cortex. , 1993, Behavioral neuroscience.

[55]  Karl J. Friston,et al.  Experience–dependent modulation of tonotopic neural responses in human auditory cortex , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  M. Devous,et al.  Pharmacological Enhancement of Aural Habilitation in Adult Cochlear Implant Users , 2005, Ear and hearing.

[57]  L. Cohen,et al.  Cholinergic influences on use-dependent plasticity. , 2002, Journal of neurophysiology.

[58]  E. Azmitia,et al.  An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat , 1978, The Journal of comparative neurology.

[59]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  M. Husain,et al.  Neuropharmacological modulation of cognitive deficits after brain damage , 2005, Current opinion in neurology.

[61]  N. Weinberger,et al.  Induction of behavioral associative memory by stimulation of the nucleus basalis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  C. Thiel,et al.  Auditory noise can prevent increased extracellular acetylcholine levels in the hippocampus in response to aversive stimulation , 2000, Brain Research.

[63]  H. Scheich,et al.  Dopaminergic and Serotonergic Neurotransmission Systems Are Differentially Involved in Auditory Cortex Learning: A Long‐Term Microdialysis Study of Metabolites , 1997, Journal of neurochemistry.

[64]  H. Fibiger,et al.  Conditioned and Unconditioned Stimuli Increase Frontal Cortical and Hippocampal Acetylcholine Release: Effects of Novelty, Habituation, and Fear , 1996, The Journal of Neuroscience.

[65]  D. Prince,et al.  Cholinergic switching within neocortical inhibitory networks. , 1998, Science.

[66]  Christo Pantev,et al.  Music and Learning‐Induced Cortical Plasticity , 2003, Annals of the New York Academy of Sciences.

[67]  D. Irvine,et al.  Basal Forebrain Cholinergic Input Is Not Essential for Lesion-Induced Plasticity in Mature Auditory Cortex , 2005, Neuron.

[68]  J. Edeline Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms , 1999, Progress in Neurobiology.

[69]  Henning Scheich,et al.  Learning-induced plasticity in animal and human auditory cortex , 2005, Current Opinion in Neurobiology.

[70]  B. Pleger,et al.  Fluoxetine facilitates use-dependent excitability of human primary motor cortex , 2004, Clinical Neurophysiology.

[71]  Shinobu Masaki,et al.  Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast , 2003, NeuroImage.

[72]  Christian Gaser,et al.  Improvement-related functional plasticity following pitch memory training , 2006, NeuroImage.

[73]  Larry E. Roberts,et al.  Plastic changes in the auditory cortex induced by intensive frequency discrimination training , 2000, Neuroreport.

[74]  T. Tsumoto,et al.  Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input , 1999, The European journal of neuroscience.

[75]  J. Edeline,et al.  Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. , 2004, Journal of neurophysiology.