Corticofugal modulation of the information processing in the auditory thalamus of the cat

SummarySingle unit activity of 355 cells was recorded in the auditory thalamus of anesthetized cats before, during, and after the inactivation by cooling of the ipsilateral primary auditory cortex (AI). Most of the units (n = 288) showed similar functional characteristics of firing before and after the cryogenic blockade of AI. The spontaneous firing rate remained unchanged by cooling in 20% of the units and decreased in the majority of them (60%). In some regions, i.e. dorsal division of the medial geniculate body (MGB), lateral part of the posterior group of the thalamus, and auditory sector of the reticular nucleus of the thalamus, the maximum firing rate evoked by white noise bursts was generally affected by cooling in the same direction and to the same extent as the spontaneous activity. Units in the ventral division of MGB showed a characteristic increase of signal-to-noise ratio during cortical cooling. The corticofugal modulation led to the appearance or disappearance of the best frequency of tuning in 51 units and changed it by more than 0.5 octave in 34 units. The bandwidths of different response patterns to pure tones stimulation were used to define a set of functional properties. During cryogenic blockade of AI, two cortically modulated sub-populations of units were usually distinguished that exhibited changes for a given functional property. The complexity and diversity of the effects of cortical inactivation suggest that the corticothalamic projection may be the support for selective operations such as an adaptive filtering of the incoming acoustic signal at the thalamic level adjusted as a function of cortical activity.

[1]  J. Winer,et al.  Subdivisions of the auditory cortex of the cat: The retrograde transport of horseradish peroxidase to the medial geniculate body and posterior thalamic nuclei , 1977, The Journal of comparative neurology.

[2]  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.

[3]  P. D. Spear,et al.  Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons , 1981, Brain Research.

[4]  M. Deschenes,et al.  Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. , 1985, Journal of neurophysiology.

[5]  G. Amato,et al.  The control exerted by the auditory cortex on the activity of the medial geniculate body and inferior colliculus. , 1969, Archivio di scienze biologiche.

[6]  W. Pond,et al.  Modern Pork Production , 1983 .

[7]  H. Laborit,et al.  [Experimental study]. , 1958, Bulletin mensuel - Societe de medecine militaire francaise.

[8]  L. Aitkin,et al.  Inhibition in the medial geniculate body of the cat , 2004, Experimental Brain Research.

[9]  G Oakson,et al.  Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones. , 1986, The Journal of physiology.

[10]  J. Desmedt,et al.  Suppression of Acoustic Input by Thalamic Stimulation.∗ , 1958, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[11]  Y. Katoh,et al.  The GABAergic neurons and axon terminals in the lateralis medialis‐suprageniculate nuclear complex of the cat: GABA‐immunocytochemical and WGA‐HRP studies by light and electron microscopy , 1987, The Journal of comparative neurology.

[12]  J. Wepsic,et al.  Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. , 1966, Experimental neurology.

[13]  M Steriade,et al.  Electrophysiology of neurons of lateral thalamic nuclei in cat: mechanisms of long-lasting hyperpolarizations. , 1984, Journal of neurophysiology.

[14]  M. Steriade,et al.  Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  N. Mizuno,et al.  Distrubution and size of thalamic neurons projecting to layer I of the auditory cortical fields of the cat compared to those projecting to layer IV , 1987, The Journal of comparative neurology.

[16]  D. Georgescauld Local Cortical Circuits, An Electrophysiological Study , 1983 .

[17]  G. L. Humphrey,et al.  Effects of changes in cortical arousal and of auditory cortex cooling on neuronal activity in the medial geniculate body , 2004, Experimental Brain Research.

[18]  J. Winer,et al.  The medial geniculate body of the cat. , 1985, Advances in anatomy, embryology, and cell biology.

[19]  S. Thomas Alexander,et al.  Adaptive Signal Processing , 1986, Texts and Monographs in Computer Science.

[20]  P. H. Schiller Parallel Pathways in the Visual System , 1993 .

[21]  T. Imig,et al.  Thalamic projections to fields A, AI, P, and VP in the cat auditory cortex , 1987, The Journal of comparative neurology.

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

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

[24]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[25]  Alessandro E. P. Villa,et al.  Evidence for spatiotemporal firing patterns within the auditory thalamus of the cat , 1990, Brain Research.

[26]  P. Stanfield Electrical properties of white and red muscle fibres of the elasmobranch fish Scyliorhinus canicula , 1972, The Journal of physiology.

[27]  E. Rouiller,et al.  Origin of afferents to physiologically defined regions of the medial geniculate body of the cat: ventral and dorsal divisions , 1985, Hearing Research.

[28]  M. Abeles Quantification, smoothing, and confidence limits for single-units' histograms , 1982, Journal of Neuroscience Methods.

[29]  Léopold Simar,et al.  Computer Intensive Methods in Statistics , 1994 .

[30]  R W Guillery,et al.  A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat , 1966, The Journal of comparative neurology.

[31]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[32]  W. R. Webster,et al.  Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. , 1972, Journal of neurophysiology.

[33]  E. Rouiller,et al.  Projections of the reticular complex of the thalamus onto physiologically characterized regions of the medial geniculate body , 1985, Neuroscience Letters.

[34]  Y. de Ribaupierre,et al.  Influence of auditory localization cues on neuronal activity in the auditory thalamus of the cat. , 1988, Journal of neurophysiology.

[35]  R. Kalil,et al.  Corticofugal influence on activity of lateral geniculate neurons in the cat. , 1970, Journal of neurophysiology.

[36]  A. Morel,et al.  Tonotopic organization in the medial geniculate body (MGB) of lightly anesthetized cats , 2004, Experimental Brain Research.

[37]  W Singer,et al.  Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. , 1977, Physiological reviews.

[38]  Michael B. Calford,et al.  Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  L. Aitkin,et al.  External nucleus of inferior colliculus: auditory and spinal somatosensory afferents and their interactions. , 1978, Journal of neurophysiology.

[40]  O. D. Creutzfeldt,et al.  Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat , 1978, Experimental Brain Research.

[41]  I. Whitfield,et al.  Thalamo-cortical connexions and tonotopicity in the cat medial geniculate body. , 1972, The Journal of physiology.

[42]  T. Morrow,et al.  Corticofugal influences of S1 cortex on ventrobasal thalamic neurons in the awake rat , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  W. Singer,et al.  Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat , 2004, Experimental Brain Research.

[44]  I. Divac,et al.  Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain , 1981, Neuroscience.

[45]  Gary A. Winans,et al.  I. BIOCHEMICAL EVIDENCE , 1980 .

[46]  Morest Dk The neuronal architecture of the medial geniculate body of the cat , 1964 .

[47]  E. Rouiller,et al.  Functional organization of the ventral division of the medial geniculate body of the cat: Evidence for a rostro-caudal gradient of response properties and cortical projections , 1989, Hearing Research.

[48]  R. Galamboš,et al.  Microelectrode studies on medial geniculate body of cat. I. Thalamic region activated by click stimuli. , 1952, Journal of neurophysiology.

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

[50]  B. Sychowa Medial geniculate body of the dog , 1962 .

[51]  Y. De Ribaupierre,et al.  Functional organization of the medial division of the medial geniculate body of the cat: Tonotopic organization, spatial distribution of response properties and cortical connections , 1989, Hearing Research.

[52]  P. Diaconis,et al.  Computer-Intensive Methods in Statistics , 1983 .

[53]  C. J. Heath,et al.  An experimental study of ascending connections from the posterior group of thalamic nuclei in the cat , 1971, The Journal of comparative neurology.

[54]  Vernon B. Brooks,et al.  Study of brain function by local, reversible cooling , 1983 .

[55]  J. Edeline Frequency-specific plasticity of single unit discharges in the rat medial geniculate body , 1990, Brain Research.

[56]  M. Abeles Local Cortical Circuits: An Electrophysiological Study , 1982 .

[57]  Alessandro E. P. Villa,et al.  Physiological differentiation within the auditory part of the thalamic reticular nucleus of the cat , 1990, Brain Research Reviews.