Abstract
The influence of the corticothalamic projections from somatosensory areas I and II (SI and SII) on the transmission of tactile information through the ventroposterolateral (VPL) thalamus was investigated by examining the effects of cooling-induced, reversible inactivation of SI and/or SII on the responsiveness of 32 VPL neurons to controlled tactile stimulation of the distal forelimb in anaesthetized cats. Both the response levels and spontaneous activity were unaffected in 21 (66%) of the VPL neurons as a result of inactivation of SI or SII singly, or both SI and SII simultaneously. In the remaining 11 neurons, 10 displayed a reduction in response level, an effect observed over the whole of the stimulus-response relations for the neurons studied at different stimulus amplitudes, and one neuron displayed an increase in response level in association with cortical inactivation. When responses in VPL neurons were affected by inactivation of one cortical somatosensory area, they were not necessarily affected by inactivation of the other. Of 14 neurons studied for the effects of the separate inactivation of SI alone and of SII alone, 7 were affected, one from both areas, but the remaining 6 were affected by inactivation of only one of these areas. Phaselocking, and therefore the precision of impulse patterning in the responses of VPL neurons to skin vibration, was unchanged by the cortical inactivation irrespective of whether the response level was affected. The results suggest that SI and SII may exert a facilitatory influence on at least a third of VPL neurons and in this way may modulate the gain of transmission of tactile signalling through the thalamus.
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Ahlsen G, Grant K, Lindström S (1982) Monosynaptic excitation of principal cells in the lateral geniculate nucleus by corticofugal fibers. Brain Res 234:454–458
Andersen P, Jung K, Sveen O (1967) Corticothalamic facilitation of somatosensory impulses. Nature 214:1011–1012
Bennett RE, Ferrington DG, Rowe MJ (1980) Tactile neuron classes within second somatosensory area (SII) of cat cerebral cortex. J Neurophysiol 43:292–309
Burchfiel JL, Duffy FH (1974) Corticofugal influences upon cat thalamic ventrobasal complex. Brain Res 70:395–411
Brooks VB (1983) Study of brain function by local, reversible cooling. Rev Physiol Biochem Pharmacol 95:1–109
Burton H (1986) Second somatosensory cortex and related areas. In: Jones EG, Peters A (eds) Cerebral cortex. Sensory motor areas and aspects of cortical connectivity, Vol 5. Plenum Press, New York, pp 31–98
Douglas PR, Ferrington DG, Rowe MJ (1978) Coding of information about tactile stimuli by neurons of the cuneate nucleus. J Physiol (Lond) 285:493–513
Dykes RW, Sur M, Merzenich MM, Kaas JH, Nelson RJ (1981) Regional segregation of neurons responding to quickly adapting, slowly adapting, deep, and Pacinian receptors within thalamic ventroposterior lateral and ventroposterior inferior nuclei in the squirrel monkey (Saimiri sciureus). J Neurosci 6:1687–1692
Geisert EE, Langsetmo A, Spear PD (1981) Influence of the corticogeniculate pathway on response properties of cat lateral geniculate neurons. Brain Res 208:409–415
Ghosh S, Turman AB, Murray GM, Rowe MJ (1990a) Corticothalamic influences on transmission of tactile information in the ventrobasal thalamus: effect of inactivation of somatosensory cortical areas I and II in the cat. Proc Aust Physiol Pharmacol Soc 21:110P
Ghosh S, Turman AB, Murray GM, Rowe MJ (1990b) The effects of cooling cortical somatosensory areas I (SI) or II (SII) on the responsiveness of ventrobasal (VB) thalamic neurons to forepaw mechanical stimulation in the cat. Soc Neurosci Abstr 16:224
Ghosh S, Turman AB, Vickery RM, Rowe MJ (1992) Responses of cat ventroposterolateral thalamic neurons to vibrotactile stimulation of forelimb footpads. Exp Brain Res 92:286–298
Gordon G, Jukes MGM (1964) Dual organisation of the exteroceptive components of the cat's gracile nucleus. J Physiol (Lond) 173:263–290
Grieve KL, Sillito AM (1991) A re-appraisal of the role of layer VI of the visual cortex in the generation of cortical end inhibition. Exp Brain Res 87:521–529
Hyvärinen J, Poranen A, Jokinen Y (1980) Influence of attentive behaviour on neuronal responses to vibration in primary somatosensory cortex of the monkey. J Neurophysiol 43:870–882
Jones EG (1975) Some aspects of the organisation of the thalamic reticular complex. J Comp Neurol 162:285–308
Jones EG (1985) The thalamus. Plenum Press, New York
Jones EG (1986) Connectivity of the primate sensory-motor cortex. In: Jones EG, Peters A (eds) Cerebral cortex. Sensory-motor areas and aspects of cortical connectivity, Vol 5. Plenum Press, New York, pp 113–183
Jones EG, Powell TPS (1969) An electron microscope study of the mode of termination of corticothalamic fibers within the sensory relay nuclei of the thalamus. Proc R Soc Lond [Biol] 172:173–185
Kayama Y, Shosaku A, Doty RW (1984) Cryogenic blockade of the visual corticothalamic projection in the rat. Exp Brain Res 54:157–165
Koch C (1987) The action of the corticofugal pathway on sensory thalamic nuclei: a hypothesis. Neuroscience 23:399–406
Marrocco RT, McClurkin JW, Young RA (1982) Modulation of lateral geniculate nucleus cell responsiveness by visual activation of the corticogeniculate pathway. J Neurosci 2:256–263
Montero VM, Singer W (1985) Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res 59:151–165
Morrow TJ, Casey KL (1990) Effects of attention on VP thalamic neuronal responses in awake monkey. Soc Neurosci 16:225
Morrow TJ, Casey KL (1992) State-related modulation of thalamic somatosensory responses in the awake monkey. J Neurophysiol 67:305–317
Murphy PC, Sillito AM (1987) Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329:727–729
Murray GM, Zhang HQ, Kaye AN, Sinnadurai T, Campbell DH, Rowe MJ (1992) Parallel processing in the first (SI) and second (SII) somatosensory areas in the rabbit: effects of reversible inactivation by cooling of SI on responses in SII. J Neurophysiol 68:703–710
Rall W (1962) Theory of physiological properties of dendrites. Ann NY Acad Sci 96:1071–1092
Ralston HJ (1983) The synaptic organization of the ventrobasal thalamus in the rat, cat and monkey in somatosensory integration in the thalamus. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory integration in the thalamus. Elsevier/ North Holland, Amsterdam, pp 241–250
Rapisarda C, Palmeri A, Sapienza S (1992) Cortical modulation of thalamo-cortical neurons relaying exteroceptive information: a microstimulation study in the guinea pig. Exp Brain Res 88:140–150
Schmielau F, Singer W (1977) The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res 120:354–361
Sherk H (1978) Area 18 responses in cat during reversible inactivation of area 17. J Neurophysiol 41:204–215
Sherman SM, Koch C (1986) The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res 63:1–20
Shin HC, Chapin JK (1990) Mapping the effects of SI cortex stimulation on somatosensory relay neurons in the rat thalamus: direct responses and afferent modulation. Somatosens Mot Res 7:421–434
Singer W (1977) Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiol Rev 57:386–420
Tsumoto T, Nakamura S, Iwama K (1975) Pyramidal tract control over cutaneous and kinesthetic sensory transmission in the cat thalamus. Exp Rain Res 22:281–294
Turman AB, Morley JW, Rowe MJ (1991) Corticofugal influences on transmission through the dorsal column nuclei: effect of inactivation of somatosensory cortical areas I and II in the cat. Proc Aust Physiol Pharmacol Soc 22:95P
Turman AB, Ferrington DG, Ghosh S, Morley JW, Rowe MJ (1992a) Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons. J Neurophysiol 67:411–429
Turman AB, Morley JW, Rowe MJ (1992b) Parallel distributed processing in somatosensory cortex: effects of SII inactivation on SI responses in cat. Soc Neurosci 18:1543
Villa AEP, Rouiller EM, Simm GM, Zurita P, Ribaupierre Y de, Ribaupierre F de (1991) Corticofugal modulation of the information processing in the auditory thalamus of the cat. Exp Brain Res 86:506–517
Watanabe T, Yanagisawa K, Kanaki J, Katsuki Y (1966) Cortical efferent flow influencing unit responses of medial geniculate body to sound stimulation. Exp Brain Res 2:302–317
Weisberg JA, Rustioni A (1979) Differential projections of cortical sensorimotor areas upon the dorsal column nuclei of cats. J Comp Neurol 184:401–422
Yuan B, Morrow TJ, Casey KL (1985) Responsiveness of ventrobasal thalamic neurons after suppression of the SI cortex in the anaesthetized rat. J Neurosci 5:2971–2978
Yuan B, Morrow TJ, Casey KL (1986) Corticofugal influences of SI cortex on ventrobasal thalamic neurons in the awake rat. J Neurosci 8:3611–3617
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Ghosh, S., Murray, G.M., Turman, A.B. et al. Corticothalamic influences on transmission of tactile information in the ventroposterolateral thalamus of the cat: effect of reversible inactivation of somatosensory cortical areas I and II. Exp Brain Res 100, 276–286 (1994). https://doi.org/10.1007/BF00227197
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DOI: https://doi.org/10.1007/BF00227197