Reward-dependent plasticity in the primary auditory cortex of adult monkeys trained to discriminate temporally modulated signals

Adult owl monkeys were trained to detect an increase in the envelope frequency of a sinusoidally modulated 1-kHz tone. Detection was positively correlated with the magnitude of the change in the envelope frequency. Surprisingly, neuronal responses recorded in the primary auditory cortex of trained monkeys were globally suppressed by the modulated tone. However, the contrast in neuronal responsiveness to small increases versus large increases in envelope frequencies was actually enhanced in the trained animals. The results suggest behaviorally contingent inhibitory and excitatory processes that are modulated by the probability that a particular signal predicts a reward.

[1]  J. Konorski Conditioned reflexes and neuron organization. , 1948 .

[2]  Mitchell Steinschneider,et al.  Speech evoked activity in the auditory radiations and cortex of the awake monkey , 1982, Brain Research.

[3]  C. Schreiner,et al.  Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. , 2002, Journal of neurophysiology.

[4]  H. Heffner,et al.  Effect of unilateral and bilateral auditory cortex lesions on the discrimination of vocalizations by Japanese macaques. , 1986, Journal of neurophysiology.

[5]  G. Recanzone,et al.  Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey , 1999, The Journal of comparative neurology.

[6]  D P Phillips,et al.  Effect of tone-pulse rise time on rate-level functions of cat auditory cortex neurons: excitatory and inhibitory processes shaping responses to tone onset. , 1988, Journal of neurophysiology.

[7]  S. Rosen Temporal information in speech: acoustic, auditory and linguistic aspects. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[9]  J. Lee Amplitude modulation rate discrimination with sinusoidal carriers. , 1994, The Journal of the Acoustical Society of America.

[10]  Xiaoqin Wang,et al.  Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. , 2002, Journal of neurophysiology.

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

[12]  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.

[13]  Jos J. Eggermont,et al.  Rate and synchronization measures of periodicity coding in cat primary auditory cortex , 1991, Hearing Research.

[14]  H. Scheich,et al.  Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil , 1997, Journal of Comparative Physiology A.

[15]  T. G. Forrest,et al.  The role of frequency selectivity in measures of auditory and vibrotactile temporal resolution. , 1992, The Journal of the Acoustical Society of America.

[16]  R. Rescorla,et al.  Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. , 1967, Psychological review.

[17]  R. Rescorla Pavlovian conditioning and its proper control procedures. , 1967, Psychological review.

[18]  Anne K. Churchland,et al.  Neural correlates of instrumental learning in primary auditory cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[22]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[23]  C. Schreiner,et al.  Organization of inhibitory frequency receptive fields in cat primary auditory cortex. , 1999, Journal of neurophysiology.

[24]  T. Imig,et al.  Organization of auditory cortex in the owl monkey (Aotus trivirgatus) , 1977, The Journal of comparative neurology.

[25]  M. Kilgard,et al.  Distributed representation of spectral and temporal information in rat primary auditory cortex , 1999, Hearing Research.

[26]  F. de Ribaupierre,et al.  Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions , 1994, Neuroscience Research.

[27]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[28]  F. Ohl,et al.  Differential Frequency Conditioning Enhances Spectral Contrast Sensitivity of Units in Auditory Cortex (Field Al) of the Alert Mongolian Gerbil , 1996, The European journal of neuroscience.

[29]  Shihab A. Shamma,et al.  Patterns of inhibition in auditory cortical cells in awake squirrel monkeys , 1985, Hearing Research.

[30]  J. L. Hollett,et al.  Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex. , 1989, The Journal of the Acoustical Society of America.

[31]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[32]  G. Langner,et al.  Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Merionesunguiculatus ): two different coding strategies for pitch and rhythm? , 1997, Journal of Comparative Physiology A.

[33]  W. R. Lieb,et al.  Molecular and cellular mechanisms of general anaesthesia , 1994, Nature.

[34]  Z. Wollberg,et al.  DISCRIMINATION OF COMMUNICATION CALLS IN THE SQUIRREL MONKEY: "CALL DETECTORS" OR "CELL ENSEMBLES"? , 1991, Journal of basic and clinical physiology and pharmacology.

[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]  J. Eggermont Temporal modulation transfer functions for AM and FM stimuli in cat auditory cortex. Effects of carrier type, modulating waveform and intensity , 1994, Hearing Research.

[37]  C E Schreiner,et al.  Functional topography of cat primary auditory cortex: distribution of integrated excitation. , 1990, Journal of neurophysiology.

[38]  R. Drullman Temporal envelope and fine structure cues for speech intelligibility , 1994 .

[39]  A. Dickinson,et al.  Classical conditioning in animals. , 1978, Annual review of psychology.

[40]  J. Pearce,et al.  A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli. , 1980 .

[41]  Thomas J. Boll,et al.  Handbook of clinical neuropsychology , 1981 .

[42]  S C McLoon,et al.  Nitric oxide and the developmental remodeling of retinal connections in the brain. , 1996, Progress in brain research.

[43]  P. Müller-Preuss,et al.  Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds , 1996, Experimental Brain Research.

[44]  David B. Moody Detection and discrimination of amplitude-modulated signals by macaque monkeys. , 1994, The Journal of the Acoustical Society of America.

[45]  Henning Scheich,et al.  Auditory cortex: comparative aspects of maps and plasticity , 1991, Current Opinion in Neurobiology.