Does Hebbian synaptic plasticity explain learning-induced sensory plasticity in adult mammals?

Over the last decade, a large number of studies have demonstrated that sensory systems undergo functional reorganizations in adult mammals. In the auditory system, highly specific reorganizations were observed during learning situations in which a particular tone frequency predicts the occurrence of an aversive event. After a brief overview of the specific receptive field changes observed after associative learning in cortical and thalamic neurons, I will raise the question concerning whether or not Hebbian synaptic plasticity adequately accounts for these data. The required conditions for Hebbian synaptic plasticity to act do not seem to be met in situations in which learning-induced receptive field plasticity occurs. This analysis points out the weakness of the traditional Hebbian scheme to provide realistic bases for learning-induced neuronal plasticity and stresses the need to look for other potential mechanisms involving neuromodulators.

[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]  James L. McGaugh,et al.  Brain and memory : modulation and mediation of neuroplasticity , 1995 .

[3]  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.

[4]  R. Rescorla.  Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

[5]  N. Weinberger,et al.  Receptive-field plasticity in the adult auditory cortex induced by Hebbian covariance , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Y. Frégnac,et al.  Temporal constraints in associative synaptic plasticity in hippocampus and neocortex. , 1995, Canadian journal of physiology and pharmacology.

[7]  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.

[8]  J. Weinman,et al.  Memory : neurochemical and abnormal perspectives , 1990 .

[9]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[10]  Norman M. Weinberger,et al.  Rapid development of learning-induced receptive field plasticity in the auditory cortex. , 1993 .

[11]  M. Ahissar,et al.  Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. , 1992, Science.

[12]  Y. Dan,et al.  Hebbian depression of isolated neuromuscular synapses in vitro. , 1992, Science.

[13]  W. Levy,et al.  Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus , 1983, Neuroscience.

[14]  H. Hatfield,et al.  The Psychology of Animals , 1933 .

[15]  William D. Hopkins,et al.  Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: I. Primary field (AI). , 1984 .

[16]  C. Woody,et al.  Properties of associative long-lasting potentiation induced by cellular conditioning in the motor cortex of conscious cats , 1991, Neuroscience.

[17]  C. Gallistel.  The organization of learning , 1990 .

[18]  N. Weinberger,et al.  Acetylcholine Modulation of Cellular Excitability Via Muscarinic Receptors: Functional Plasticity in Auditory Cortex , 1991 .

[19]  J. Edeline,et al.  Conditioned changes in the basal forebrain: Relations with learning-induced cortical plasticity , 1995, Psychobiology.

[20]  J. Kaas.  The Plasticity of Sensory Representations in Adult Primates , 1995 .

[21]  J. Kaas.  Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[22]  Norman M. Weinberger,et al.  Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. , 1989 .

[23]  J. Edeline,et al.  Subcortical adaptive filtering in the auditory system: associative receptive field plasticity in the dorsal medial geniculate body. , 1991, Behavioral neuroscience.

[24]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[25]  L. Benardo,et al.  Characterization of cholinergic and noradrenergic slow excitatory postsynaptic potentials from rat cerebral cortical neurons , 1993, Neuroscience.

[26]  R. Richardson.  Current Status of the Basal Forebrain Cholinergic System: A Preview and Commentary , 1991 .

[27]  B. C. Motter.  Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[28]  N. Mackintosh.  The psychology of animal learning , 1974 .

[29]  D. Hubel,et al.  Binocular interaction in striate cortex of kittens reared with artificial squint. , 1965, Journal of neurophysiology.

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

[31]  T. Robbins,et al.  Cortical noradrenaline, attention and arousal , 1984, Psychological Medicine.

[32]  H. Fibiger,et al.  The nucleus basalis magnocellularis: The origin of a cholinergic projection to the neocortex of the rat , 1980, Neuroscience.

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

[34]  J. Delacour,et al.  “Learned” changes in the responses of the rat barrel field neurons , 1987, Neuroscience.

[35]  Tadaharu Tsumoto,et al.  Long-term potentiation and long-term depression in the neocortex , 1992, Progress in Neurobiology.

[36]  M. Segal,et al.  Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. , 1991, Progress in brain research.

[37]  Y. Frégnac,et al.  Cellular analogs of visual cortical epigenesis. II. Plasticity of binocular integration , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  N. Weinberger.  Dynamic regulation of receptive fields and maps in the adult sensory cortex. , 1995, Annual Review of Neuroscience.

[39]  Norman M. Weinberger,et al.  Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields , 1986, Brain Research.

[40]  Norman M. Weinberger,et al.  Sensitization induced receptive field plasticity in the auditory cortex is independent of CS-modality , 1992, Brain Research.

[41]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[42]  T. Tsumoto,et al.  Cross-depression: an electrophysiological manifestation of binocular competition in the developing visual cortex , 1979, Brain Research.

[43]  Mark F. Bear,et al.  Bidirectional modification of CA1 synapses in the adult hippocampus in vivo , 1996, Nature.

[44]  Charles D. Gilbert,et al.  Rapid dynamic changes in adult cerebral cortex , 1993, Current Opinion in Neurobiology.

[45]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[46]  M. Merzenich,et al.  Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. , 1990, Journal of neurophysiology.

[47]  D. McCormick.  Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity , 1992, Progress in Neurobiology.

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