Abstract
The possibility that learning induces frequency-specific changes at different levels of the auditory system was investigated by recording multiunit activity at the level of the auditory cortex, the magnocellular medial geniculate, and the dorsal cochlear nucleus. Chronically implanted rats were submitted to frequency discrimination (CS+/CS-) and reversal training while they were engaged in a leverpressing for food task. The conditioned suppression response indicated the acquisition of the discrimination and its reversal at the behavioral level. Off-line test sessions, during which different frequencies were tested, were conducted before conditioning, after acquisition of the initial discrimination, and after its reversal. They showed that frequency-specific changes occurred during the initial discrimination at the level of the auditory cortex, the medial geniculate, and, to a lesser extent, the dorsal cochlear nucleus. After acquisition of the reversal, frequency-specific changes, in relation to the new reinforcement rule, were also detected at the cortical and thalamic level but not at the cochlear nucleus level. These results indicate that frequency-specific changes can occur during conditioning at different levels of the CS auditory pathway and suggest that interactions between these different levels must be studied to understand modifications of information processing during learning.
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References
Aitkin, L. M. (1973). Medial geniculate body of the cat: Responses to tonal stimuli of neurons in medial division. Journal of Neurophysiology, 36, 275–283.
Bakin, J., Condon, C.D., Weinberger, N. M. (1988). Learning specifically alters frequency receptive fields in the auditory cortex of guinea pigs. Society for Neuroscience Abstracts, 14, 862 (Abstract No. 344.13).
Birt, D., & Olds, M. (1981). Associative response changes in lateral midbrain tegmentum and medial geniculate during differential appetitive conditioning. Journal of Neurophysiology, 46, 1039–1055.
Birt, D., Nienhuis, R., & Olds, M. (1979). Separation of associative from non-associative short latency changes in medial geniculate and inferior colliculus during differential conditioning and reversal in rats. Brain Research, 167, 129–138.
Buchwald, J. S., Halas, E. S., & Schramm, S. (1966). Changes in cortical and subcortical unit activity during behavioral conditioning. Physiology & Behavior, 1, 11–22.
Calford, M. B. (1983). The panellation of the medial geniculate body of the cat defined by the auditory responses properties of single units. Journal of Neuroscience, 3, 2350–2365.
Carmel, P. W., & Starr, A. (1963). Acoustic and non-acoustic factors modifying middle-ear muscles activity in awake cats. Journal of Neurophysiology, 26, 598–616.
Courtice, C. J. (1975). Action potential selection by amplitude and width. Journal of Physiology (London), 246, 18–P.
Davis, M. (1984). The mammalian startle response. In R. C. Eaton (Ed.), Neural mechanisms of startle behavior (pp. 287–351). New York: Plenum.
Diamond, D. M., & Weinberger, N. M. (1984). Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: Secondary field (AH). Behavioral Neuroscience, 98, 198–210.
Diamond, D. M., & Weinberger, N. M. (1986). Classical conditioning rapidly induced changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Research, 372, 357–360.
Diamond, D. M., & Weinberger, N. M. (1989). Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex. Behavioral Neuroscience, 103, 471–494.
Disterhoft, J. F., & Stuart, D. K. (1976). Trial sequence of changed unit activity in the auditory system of alert rat during conditioned response acquisition and extinction. Journal of Neurophysiology, 39, 266–281.
Disterhoft, J. F., & Stuart, D. K. (1977). Different short latency response increases after conditioning in inferior colliculus of alert rat. Brain Research, 130, 315–334.
Edeune, J.-M., Dutrieux, G., & Neuenschwander-El Massioui, N. (1988). Multiunit changes in hippocampus and medial geniculate body in free-behaving rats during acquisition and retention of a conditioned response to a tone. Behavioral & Neural Biology, 50, 61-79
Edeune, J.-M., NEUENSCHWANDER-EL MASSIOUI, N., & DUTRIEUX, G. (1990). Discriminative long-term retention of multiunit changes in the hippocampus, the medial geniculate and the auditory cortex. Behavioral Brain Research, 39, 145–155.
Evans, E. F., & Nelson, P. G. (1973). The responses of single neurones in the cochlear nucleus of the cat as a function of their location and anaesthetic state. Experimental Brain Research, 17, 402–427.
Gabriel, M. (1976). Short-latency discriminative unit responses: En-gram or bias? Physiological Psychology, 4, 275–280.
Gabriel, M., Miller, J. D., & Saltwick, S. E. (1976). Multiple-unit activity of the rabbit medial geniculate nucleus in conditioning, extinction, and reversal. Physiological Psychology, 4, 124–134.
Gabriel, M., Saltwick, S. E., & Miller, J. D. (1975). Conditioning and reversal of short-latency multiunit responses in the rabbit medial geniculate nucleus. Science, 189, 1108–1109.
Graybiel, A.M. (1972). Some fiber pathways related to the posterior thalamic region in the cat. Brain Behavior & Evolution, 6, 363–393.
Halas, E. S., Bearlsey, J. V., & Sandlie, M. E. (1970). Conditioned neuronal responses at various levels in conditioning paradigms. Electroencephalography & Clinical Neurophysiology, 28, 468–477.
Ledoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985). Projection to subcortical forebrain from anatomically defined regions of the medial geniculate body. Journal of Comparative Neurology, 242, 182–213.
Morel, A., Rouiller, E., DeRibeaupierre, Y., & DeRibeaupierre, F. (1987). Tonotopic organization in the Medial Geniculate Body (MGB) of lightly anesthetized cats. Experimental Brain Research, 69, 24–42.
Mugnaini, E., Warr, W. B., & Osen, K. K. (1980). Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. Journal of Comparative Neurology, 191, 581–606.
Olds, J., Disterhoft, J. T., Segal, M., Kornblith, C. L., & Hirsh, R. (1972). Learning centers of rat brain mapped by measuring the latencies of conditioned unit responses. Journal of Neurophysiology, 35, 202–219.
Oleson, T., Ashe, J., & Weinberger, N. M. (1975). Modification of auditory and somatosensory activity during pupillary conditioning in the paralysed cat. Journal of Neurophysiology, 38, 1114–1139.
Paxinos, G., & Watson, C. (1982). The rat brain in stereotaxic atlas. New York: Academic Press.
Perruchet, P. (1982). Programme de description et d’analyses inférentielles de données expérimentales par microordinateur. Informatique & Sciences Humaines, 85, 87–101.
Rhode, W. S., & Kettner, R. E. (1987). Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthe-tized cat. Journal of Neurophysiology, 57, 414–442.
Roger, M., & Arnault, P. (1989). Anatomical study of the connections of the primary auditory area in the rat. Journal of Comparative Neurology, 287, 339–356.
Ryugo, D. K., & Weinberger, N. M. (1978). Differential plasticity of morphologically distinct neuron populations in the medial geniculate body of the cat during classical conditioning. Behavioral Biology, 22, 275–301.
Starr, A., & Livingston, R. (1963). Long-lasting nervous system responses to prolonged sound stimulation in awake cats. Journal of Neurophysiology, 26, 416–431.
Vaughan, D. W. (1980). Thalamic and callosal connection of the rat auditory cortex. Brain Research, 260, 181–189.
Weinberger, N. M. (1982). Sensory plasticity and learning: The magno-cellular medial geniculate nucleus of the auditory system. In C.D. Woody (Ed.), Conditioning: Representation of involved neural function (pp. 697–710). New York: Plenum.
Weinberger, N. M., Ashe, J., Metherate, R., McKenna, T. M., Diamond, D. M., & Bakin, J. (1990). Retuning auditory cortex by learning: A preliminary model. Concepts in Neuroscience, 1, 91–132.
Weinberger, N. M., Hopkins, W., & Diamond, D. M. (1984). Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: Primary field (AI). Behavioral Neuroscience, 98, 171–188.
Young, E. D., & Brownell, W. E. (1976). Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. Journal of Neurophysiology, 39, 282–300.
Zilles, K. (1985). The cortex of the rat: A stereotaxic atlas. Berlin-Heidelberg: Springer-Verlag.
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This work was supported by Fellowship 84158 from the Ministere de la Recherche et de la Technologic.
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Edeline, JM., Neuenschwander-El Massioui, N. & Dutrieux, G. Frequency-specific cellular changes in the auditory system during acquisition and reversal of discriminative conditioning. Psychobiology 18, 382–393 (1990). https://doi.org/10.3758/BF03333084
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DOI: https://doi.org/10.3758/BF03333084