Abstract
Neuronal responses to hairy skin stimulation were simultaneously recorded in the ventral posterolateral nucleus (VPL) of the thalamus and primary somatosensory cortex (SI) of halothane-anesthetized cats. Among 233 thalamocortical neuron pairs, cross-correlation analysis revealed significant interactions in 120 pairs. Excitatory interactions were most prevalent and included influences occurring exclusively in the thalamocortical (41 pairs) or corticothalamic (23 pairs) directions as well as multiphasic interactions (40 pairs) in both directions. Only 16 pairs exhibited inhibitory interactions and 7 of these involved multiphasic combinations of excitation and inhibition. In 14 of these neuron pairs, inhibition was exerted in the corticothalamic direction. Receptive field (RF) overlap between thalamic and cortical neurons varied considerably, and neuronal interactions were more likely for neuron pairs sharing large portions of their combined RFs. Computer-controlled stimulation was delivered to multiple RF sites but only 46% of the neuron pairs displayed interactions at more than one stimulation site and only four neuron pairs showed interactions at all stimulus positions. When interactions occurred at multiple stimulus sites, 40% of these interactions were characterized by timing shifts where the time interval between VPL and SI discharges varied as much as 20 ms because of stimulus relocation. In nine neuron pairs, systematic shifts in stimulus position produced reversals in the temporal sequence of thalamic and cortical neuronal discharges. Functional interactions between thalamic and cortical neurons were detected during both spontaneous and stimulus-induced activity. Matched-sample comparisons of connection strength and half-widths of thalamocortical peaks during spontaneous and stimulus-induced activity indicated that functional interactions produced by cutaneous stimulation were significantly stronger and had less temporal variability than those occurring spontaneously.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aertsen AMHJ, Gerstein GL, Habib MK, Palm G (1989) Dynamics of neuronal firing correlation: modulation of “effective connectivity”. J Neurophysiol 61:900–917
Alloway KD, Burton H (1985) Submodality and columnar organization of the second somatic sensory area in cats. Exp Brain Res 61:128–140
Alloway KD, Rosenthal P, Burton H (1989) Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats. Exp Brain Res 78:514–532
Alloway KD, Johnson MJ, Wallace MB (1993) Thalamocortical interactions in the somatosensory system: interpretations of latency and cross-correlation analyses. J Neurophysiol 70:892–908
Alloway KD, Wallace MB, Johnson MJ (1994) Cross-correlation analysis of cuneothalamic interactions in the rat somatosensory system: influence of receptive field topography and comparisons with thalamocortical interactions. J Neurophysiol 72:1949–1972
Angel A, Gratton DA (1982) The effect of anaesthetic agents on cerebral cortical responses in the rat. Br J Pharmacol 76:541–549
Chapin JK, Lin CS (1984) Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229:199–213
Curro Dossi R, Nunez A, Steriade M (1992) Electrophysiology of a slow (0.5–4 Hz) intrinsic oscillation of cat thalamocortical neurones in vivo. J Physiol (Lond) 447:215–234
DeFelipe J, Conley M, Jones EG (1986) Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J Neurosci 6:3749–3766
Dykes RW, Landry P, Metherate R, Hicks TP (1984) Functional role of GABA in the cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J Neurophysiol 52:1066–1093
Felleman DJ, Wall JT, Cusick CG, Kaas JH (1983) The representation of the body surface in SI of cats. J Neurosci 3:1648–1669
Gerstein GL, Perkel DH (1972) Mutual temporal relationships among neuronal spike trains: statistical techniques for display and analysis. Biophys J 12:453–473
Gochin PM, Kaltenbach JA, Gerstein GL (1989) Coordinated activity of neuron pairs in anesthetized rat dorsal cochlear nucleus. Brain Res 497:1–11
Hicks TP, Metherate R, Landry P, Dykes RW (1986) Bicuculline-induced alterations of response properties in functionally identified ventroposterior thalamic neurones. Exp Brain Res 63:248–264
Jones EG (1985) The Thalamus. Plenum, New York, pp 128–137
Keifer JC, Baghdoyan HA, Becker L, Lydie R (1994) Halothane decreases pontine acetylcholine release and increases EEG spindles. Neuroreport 5:577–580
Landry P, Deschenes M (1981) Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical affernts to the primary somatic sensory cortex in the cat. J Comp Neurol 199:345–371
Landry P, Dykes RW (1985) Identification of two populations of corticothalamic neurons in cat primary somatosensory cortex. Exp Brain Res 60:289–298
Levick WR, Cleland BG, Dubin MW (1972) Lateral geniculate neurons of cat: retinal inputs and physiology. Invest Ophthalmol 11:302–311
McKenna TM, Light AR, Whitsel BL (1984) Neurons with unusual response and receptive-field properties in upper laminae of cat SI cortex. J Neurophysiol 51:1055–1076
Perkel DH, Gerstein GL, Moore GP (1967a) Neuronal spikes trains and stochastic point processes. I. The single spike train. Biophys J 7:391–418
Perkel DH, Gerstein GL, Moore GP (1967b) Neuronal spikes trains and stochastic point processes. II. Simultaneous spike trains. Biophys J 7:419–440
Poggio GF, Mountcastle VB (1963) The functional properties of ventrobasal thalamic neurons studied in unanesthetized moneys. J Neurophysiol 26:775–806
Steriade M, Jones EG, Llinas RR (1990) Thalamic oscillations and signalling. Wiley, New York
Steriade M, Curro Dossi RC, Nunez A (1991) Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. J Neuosci 11(10):3200–3217
Steriade M, Contreras D, Curro Dossi R, Nunez A (1993a) The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci 13(8):3284–3299
Steriade M, McCormick DA, Sejnowski TJ (1993b) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679–685
Swadlow HA (1990) Efferent neurons and suspected interneurons in S-1 forelimb repesentation of the awake rabbit: receptive fields and axonal properties. J Neurophysiol 63(6): 1477–1498
Tsumoto T, Creutzfeldt OD, Legendy CR (1978) Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat. (With an appendix on geniculocortical mono-synaptic connections). Exp Brain Res 32:345–364
Vahle-Hinz C, Hicks TP, Gottschaldt K-M (1994) Amino acids modify thalamoc-cortical response transformation expressed by neurons of the ventrobasal complex. Brain Res 637:139–155
White EL (1986) Termination of thalamic afferents in the cerebral cortex. Cereb Cortex 5:271–289
Yen C-T, Conley M, Jones EG (1985) Morphological and functional types of neurons in cat ventral posterior thalamic nucleus. J Neurosci 5(5):1316–1338
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Johnson, M.J., Alloway, K.D. Sensory modulation of synchronous thalamocortical interactions in the somatosensory system of the cat. Exp Brain Res 102, 181–197 (1994). https://doi.org/10.1007/BF00227508
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00227508