Corticofugal Gating of Auditory Information in the Thalamus: An In Vivo Intracellular Recording Study

In the present study, we investigated the auditory responses of the medial geniculate (MGB) neurons, through in vivo intracellular recordings of anesthetized guinea pigs, while the auditory cortex was electrically activated. Of the 63 neurons that received corticofugal modulation of the membrane potential, 30 received potentiation and 33 received hyperpolarization. The corticofugal potentiation of the membrane potential (amplitude, mean ± SD, 8.6 ± 5.5 mV; duration, 125.5 ± 75.4 msec) facilitated the auditory responses and spontaneous firing of the MGB neurons. The hyperpolarization of –11.3 ± 4.9 mV in amplitude and 210.0 ± 210.1 msec in duration suppressed the auditory responses and spontaneous firing of the MGB neurons. Four of the five neurons that were histologically confirmed to be located in the lemniscal MGB received corticofugal facilitatory modulation, and all of the four neurons that were confirmed to be located in the non-lemniscal MGB received corticofugal inhibitory modulation. The present intracellular recording provides novel results on how the corticofugal projection gates the sensory information in the thalamus: via the spatially selective depolarization of lemniscal MGB neurons and hyperpolarization of non-lemniscal MGB neurons. It is speculated that the systematic selectivity of facilitation and inhibition over the lemniscal and non-lemniscal MGB is related to the attention shift within the auditory modality and across the sensory modalities.

[1]  N Suga,et al.  Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. , 1997, Journal of neurophysiology.

[2]  Martin Deschênes,et al.  Electrophysiology and Pharmacology of the Corticothalamic Input to Lateral Thalamic Nuclei: an Intracellular Study in the Cat , 1990, The European journal of neuroscience.

[3]  T. Hashikawa,et al.  Modulatory effect of cortical activation on the lemniscal auditory thalamus of the Guinea pig. , 2002, Journal of neurophysiology.

[4]  N Suga,et al.  Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. , 1997, Journal of neurophysiology.

[5]  C. Koch,et al.  The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus , 2004, Experimental Brain Research.

[6]  E. G. Jones,et al.  Synaptic distribution of afferents from reticular nucleus in ventroposterior nucleus of cat thalamus , 1995, The Journal of comparative neurology.

[7]  N. Suga,et al.  Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Barth,et al.  Cellular mechanisms of thalamically evoked gamma oscillations in auditory cortex. , 2001, Journal of neurophysiology.

[9]  T. Sejnowski,et al.  Control of Spatiotemporal Coherence of a Thalamic Oscillation by Corticothalamic Feedback , 1996, Science.

[10]  J. He,et al.  Modulatory effects of regional cortical activation on the onset responses of the cat medial geniculate neurons. , 1997, Journal of neurophysiology.

[11]  D. McCormick,et al.  Corticothalamic Inputs Control the Pattern of Activity Generated in Thalamocortical Networks , 2000, The Journal of Neuroscience.

[12]  P. Golshani,et al.  Synchronized Paroxysmal Activity in the Developing Thalamocortical Network Mediated by Corticothalamic Projections and “Silent” Synapses , 1999, The Journal of Neuroscience.

[13]  R. Guillery,et al.  Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body , 2000, Neuroscience.

[14]  M. Steriade.  Impact of network activities on neuronal properties in corticothalamic systems. , 2001, Journal of neurophysiology.

[15]  James E. Vaughn,et al.  GABA neurons are the major cell type of the nucleus reticularis thalami , 1980, Brain Research.

[16]  M. Deschenes,et al.  Dendrodendritic and Axoaxonic Synapses in the Thalamic Reticular Nucleus of the Adult Rat , 1997, The Journal of Neuroscience.

[17]  N. Suga,et al.  Corticofugal modulation of frequency processing in bat auditory system , 1997, Nature.

[18]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[19]  N Suga,et al.  Corticofugal Modulation of Time-Domain Processing of Biosonar Information in Bats , 1996, Science.

[20]  M. Steriade.  Corticothalamic resonance, states of vigilance and mentation , 2000, Neuroscience.

[21]  E. Young,et al.  The electrotonic structure of regular-spiking neurons in the ventral cochlear nucleus may determine their response properties. , 1994, Journal of neurophysiology.

[22]  Maria V. Sanchez-Vives,et al.  Functional dynamics of GABAergic inhibition in the thalamus. , 1997, Science.

[23]  A. Scheibel,et al.  The organization of the nucleus reticularis thalami: a Golgi study. , 1966, Brain research.

[24]  Ying-Shing Chan,et al.  An in vivo intracellular study of auditory thalamic neurons , 2003 .

[25]  J. Edeline,et al.  Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex , 2004, Experimental Brain Research.

[26]  P. C. Murphy,et al.  Corticofugal feedback influences the generation of length tuning in the visual pathway , 1987, Nature.

[27]  T. Powell,et al.  An electron microscopic study of the mode of termination of cortico-thalamic fibres within the sensory relay nuclei of the thalamus , 1969, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[28]  Y. Katsuki,et al.  Cortical efferent flow influencing unit responses of medial geniculate body to sound stimulation , 2004, Experimental Brain Research.

[29]  E. Puil,et al.  Effects of metabotropic glutamate receptor activation in auditory thalamus. , 1999, Journal of neurophysiology.

[30]  J. Huguenard,et al.  Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. , 1999, Science.

[31]  J R Huguenard,et al.  Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: a dynamic clamp study. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  E. Puil,et al.  Mechanisms for signal transformation in lemniscal auditory thalamus. , 1996, Journal of neurophysiology.

[33]  D. McCormick,et al.  Cellular mechanisms of a synchronized oscillation in the thalamus. , 1993, Science.

[34]  F. de Ribaupierre,et al.  Corticofugal modulation of the information processing in the auditory thalamus of the cat , 2004, Experimental Brain Research.

[35]  Edward L. Bartlett,et al.  Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. , 1999, Journal of neurophysiology.

[36]  T. Powell,et al.  Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat , 1969, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[37]  R. W. Guillery,et al.  The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[38]  E. G. Jones,et al.  Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat , 1995, The Journal of comparative neurology.

[39]  D. Contreras,et al.  The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  A. Graybiel,et al.  Coexistence of glutamic acid decarboxylase- and somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  D. Prince,et al.  Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[42]  GABAB receptor activation changes membrane and filter properties of auditory thalamic neurons , 1998, Hearing Research.

[43]  E. G. Jones,et al.  The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  P. Jen,et al.  Corticofugal influences on the responses of bat inferior collicular neurons to sound stimulation , 1989, Brain Research.

[45]  P. Jen,et al.  An electrophysiological study of neural pathways for corticofugally inhibited neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus , 2001, Experimental Brain Research.

[46]  B. Hu,et al.  Cellular basis of temporal synaptic signalling: an in vitro electrophysiological study in rat auditory thalamus. , 1995, The Journal of physiology.

[47]  R. Andersen,et al.  The thalamocortical and corticothalamic conections of AI, AII, and the anteriior auditory field (AFF) in the cat: Evidence ofr two largely sergregarted systems of connections , 1980, The Journal of comparative neurology.

[48]  A. Destexhe,et al.  Cortical Feedback Controls the Frequency and Synchrony of Oscillations in the Visual Thalamus , 2000, The Journal of Neuroscience.

[49]  M. Semple,et al.  Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences. , 1993, Journal of neurophysiology.

[50]  T J Sejnowski,et al.  Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. , 1993, Biophysical journal.

[51]  C. Frassoni,et al.  GABAergic Neurons in Mammalian Thalamus: A Marker of Thalamic Complexity? , 1997, Brain Research Bulletin.

[52]  E. G. Jones,et al.  Predominance of corticothalamic synaptic inputs to thalamic reticular nucleus neurons in the rat , 1999, The Journal of comparative neurology.

[53]  P. Torterolo,et al.  Intracellular in vivo recording of inferior colliculus auditory neurons from awake guinea-pigs. , 1995, Archives italiennes de biologie.

[54]  A. Shosaku,et al.  Auditory neurons in the rat thalamic reticular nucleus , 2004, Experimental Brain Research.

[55]  E. G. Jones,et al.  Differences in quantal amplitude reflect GluR4- subunit number at corticothalamic synapses on two populations of thalamic neurons , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  E. G. Jones,et al.  Some aspects of the organization of the thalamic reticular complex , 2004, The Journal of comparative neurology.

[57]  N. Weinberger,et al.  Corticofugal modulation of the medial geniculate body , 1976, Experimental Neurology.

[58]  J. Bourassa,et al.  Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer , 1995, Neuroscience.

[59]  M. Steriade,et al.  The GABAergic reticular nucleus: A preferential target of corticothalamic projections , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[60]  T. Sejnowski,et al.  Spatiotemporal Patterns of Spindle Oscillations in Cortex and Thalamus , 1997, The Journal of Neuroscience.

[61]  D. McCormick,et al.  Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Jufang He,et al.  Slow Oscillation in Non-Lemniscal Auditory Thalamus , 2003, The Journal of Neuroscience.

[63]  Jufang He.  Corticofugal modulation on both ON and OFF responses in the nonlemniscal auditory thalamus of the guinea pig. , 2003, Journal of neurophysiology.

[64]  Philip H Smith,et al.  Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices , 2001, The Journal of comparative neurology.

[65]  V. Montero,et al.  A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus , 2004, Experimental Brain Research.

[66]  S. Sherman,et al.  N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[67]  P. Jen,et al.  Brief and short-term corticofugal modulation of subcortical auditory responses in the big brown bat, Eptesicus fuscus. , 2000, Journal of neurophysiology.