Plasticity of temporal information processing in the primary auditory cortex

Neurons in the rat primary auditory cortex (A1) generally cannot respond to tone sequences faster than 12 pulses per second (pps). To test whether experience can modify this maximum following rate in adult rats, trains of brief tones with random carrier frequency but fixed repetition rate were paired with electrical stimulation of the nucleus basalis (NB) 300 to 400 times per day for 20–25 days. Pairing NB stimulation with 5-pps stimuli markedly decreased the cortical response to rapidly presented stimuli, whereas pairing with 15-pps stimuli significantly increased the maximum cortical following rate. In contrast, pairing with fixed carrier frequency 15-pps trains did not significantly increase the mean maximum following rate. Thus this protocol elicits extensive cortical remodeling of temporal response properties and demonstrates that simple differences in spectral and temporal features of the sensory input can drive very different cortical reorganizations.

[1]  H. Woodrow.  The effect of practice upon time-order errors in the comparison of temporal intervals. , 1935 .

[2]  M. Goldstein,et al.  Intracellular study of the cat's primary auditory cortex. , 1972, Brain research.

[3]  M. Goldstein,et al.  Cortical coding of repetitive acoustic pulses. , 1972, Brain research.

[4]  U. Neisser,et al.  Effect of practice on the identification of auditory sequences , 1974 .

[5]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of striate cortical neurones , 1975, Nature.

[6]  J. Kelly,et al.  Auditory sensitivity of the albino rat. , 1976, Journal of comparative and physiological psychology.

[7]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[8]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[9]  M. Lings,et al.  Articles , 1967, Soil Science Society of America Journal.

[10]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF) , 1986, Hearing Research.

[11]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields , 1988, Hearing Research.

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

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

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

[15]  M. Cynader,et al.  Effect of the richness of the environment on neurons in cat visual cortex. II. Spatial and temporal frequency characteristics. , 1990, Brain research. Developmental brain research.

[16]  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.

[17]  G. Recanzone,et al.  Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task. , 1992, Journal of neurophysiology.

[18]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[19]  D. Rasmusson,et al.  Frequency-dependent increase in cortical acetylcholine release evoked by stimulation of the nucleus basalis magnocellularis in the rat , 1992, Brain Research.

[20]  W M Jenkins,et al.  Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. , 1992, Journal of neurophysiology.

[21]  N. Weinberger.  Learning-induced changes of auditory receptive fields , 1993, Current Opinion in Neurobiology.

[22]  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.

[23]  S. Hochstein,et al.  Attentional control of early perceptual learning. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Faber,et al.  "Latent" inhibitory connections become functional during activity-dependent plasticity. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Ostwald,et al.  Temporal Coding of Amplitude and Frequency Modulation in the Rat Auditory Cortex , 1995, The European journal of neuroscience.

[26]  J J Eggermont,et al.  Synchrony between single-unit activity and local field potentials in relation to periodicity coding in primary auditory cortex. , 1995, Journal of neurophysiology.

[27]  M M Merzenich,et al.  Temporal information transformed into a spatial code by a neural network with realistic properties , 1995, Science.

[28]  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.

[29]  Steven L. Miller,et al.  Temporal Processing Deficits of Language-Learning Impaired Children Ameliorated by Training , 1996, Science.

[30]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[31]  J. Bakin,et al.  Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning. , 1996, Behavioral neuroscience.

[32]  M. Merzenich,et al.  Experience-induced plasticity of cutaneous maps in the primary somatosensory cortex of adult monkeys and rats , 1996, Journal of Physiology-Paris.

[33]  R. Shapley,et al.  Temporal-frequency selectivity in monkey visual cortex , 1996, Visual Neuroscience.

[34]  L. Maffei,et al.  Temporal Aspects of Contrast Visual Evoked Potentials in the Pigmented Rat: Effect of Dark Rearing , 1997, Vision Research.

[35]  D. Buonomano,et al.  Learning and Generalization of Auditory Temporal–Interval Discrimination in Humans , 1997, The Journal of Neuroscience.

[36]  Bo Cartling,et al.  Control of computational dynamics of coupled integrate-and-fire neurons , 1997, Biological Cybernetics.

[37]  C. Schreiner,et al.  Temporal processing in cat primary auditory cortex. , 1997, Acta oto-laryngologica. Supplementum.

[38]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[39]  R. Dykes,et al.  Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences , 1997, The Journal of comparative neurology.

[40]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. Schreiner,et al.  Low-frequency oscillations of visual, auditory and somatosensory cortical neurons evoked by sensory stimulation. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  J. Eggermont,et al.  Autonomous cortical rhythms affect temporal modulation transfer functions , 1997, Neuroreport.

[43]  Thomas J. Carew,et al.  Metaplasticity at identified inhibitory synapses in Aplysia , 1997, Nature.

[44]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[45]  M M Merzenich,et al.  Context-sensitive synaptic plasticity and temporal-to-spatial transformations in hippocampal slices. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[47]  I. Soltesz,et al.  Enhanced bursts of IPSCs in dentate granule cells in mice with regionally inhibited long–term potentiation , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  M. Dimyan,et al.  Induction of long-term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. , 1998, Behavioral neuroscience.

[49]  R. Bradley,et al.  Tetanic stimulation induces short-term potentiation of inhibitory synaptic activity in the rostral nucleus of the solitary tract. , 1998, Journal of neurophysiology.

[50]  Nancy Byl,et al.  Practice-Related Improvements in Somatosensory Interval Discrimination Are Temporally Specific But Generalize across Skin Location, Hemisphere, and Modality , 1998, The Journal of Neuroscience.

[51]  Frances S. Chance,et al.  Synaptic Depression and the Temporal Response Characteristics of V1 Cells , 1998, The Journal of Neuroscience.