Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-23T11:18:36.172Z Has data issue: false hasContentIssue false
  • English
  • Français

Brain-stem modulation of the response properties of cells in the cat's perigeniculate nucleus

Published online by Cambridge University Press:  02 June 2009

P. C. Murphy ,
D. J. Uhlrich ,
N. Tamamaki  and
S. Murray Sherman
P. C. Murphy
Affiliation:
Department of Neurobiology, State University of New York, Stony Brook
D. J. Uhlrich
Affiliation:
Department of Neurobiology, State University of New York, Stony Brook
N. Tamamaki
Affiliation:
Department of Neurobiology, State University of New York, Stony Brook
S. Murray Sherman
Affiliation:
Department of Neurobiology, State University of New York, Stony Brook
Get access Rights & Permissions [Opens in a new window]

Abstract

Transmission through the lateral geniculate nucleus is facilitated following activation of the cholinergic input from the brain stem, which is thought to reflect activity patterns seen during arousal. One of the underlying mechanisms is the suppression of inhibitory circuits local to the lateral geniculate nucleus. However, evidence exists that some visually driven inhibitory inputs to geniculate relay cells may be preserved or even enhanced under conditions of arousal, and during electrical activation of the parabrachial region of the brain stem. We have therefore reexamined the effect of brain-stem activation on the visual responses of one group of local inhibitory inputs to geniculate relay cells, those emanating from the adjacent perigeniculate nucleus. We recorded single perigeniculate cells in anesthetized, paralyzed cats. Axons innervating the lateral geniculate and perigeniculate nuclei from the parabrachial region of the brain stem were electrically activated, and the effect of this activation was assessed on both spontaneous and visually evoked responses. Visual stimulation consisted of sinusoidally modulated sine–wave gratings of varying spatial and temporal frequency. For the great majority of perigeniculate cells (32 of 40), brain-stem activation inhibited spontaneous activity, while one cell was excited, three showed a mixed effect and four were unaffected. Nevertheless, the responses of most cells (30 of 40) were facilitated when brain-stem activation was paired with certain spatio-temporal patterns of visual stimulation. Spatial tuning curves were constructed for 17 cells and temporal tuning curves for 14, before and during parabrachial activation. The responses of any one cell could be facilitated, unchanged, or suppressed, depending on the visual stimulus used. In some cases, this substantially modified the cell’s spatial and temporal tuning properties. We conclude that activation of the brain stem disinhibits geniculate relay cells in the absence of visual stimulation, but it has the potential to enhance either the magnitude or specificity of visually driven inhibition arising from the perigeniculate nucleus.

Keywords

Perigeniculate nucleusThalamic reticular nucleusParabrachial regionAcetylcholineRetinogeniculate transmission
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 781 - 791
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahlsén, G. & Lindström, S. (1982). Excitation of perigeniculate neurons via axon collaterals of principal cells. Brain Research 236, 477–481.CrossRefGoogle ScholarPubMed
Ahlsén, G., Lindström, S. & Lo, F.-S. (1982). Functional distinction of perigeniculate and thalamic reticular neurons in the cat. Experimental Brain Research 46, 118–126.CrossRefGoogle ScholarPubMed
Ahlsén, G., Lindström, S. & Lo, F.-S. (1984). Inhibition from the brainstem of inhibitory interneurones of the cat’s dorsal lateral geniculate nucleus. Journal of Physiology 347, 593–609.CrossRefGoogle ScholarPubMed
Ahlsen, G., Lindström, S. & Sybirska, E. (1978). Subcortical axon collaterals of principal cells in the lateral geniculate body of the cat. Brain Research 156, 106–109.CrossRefGoogle ScholarPubMed
Ahlsen, G. & Lo, F.-S. (1982). Projection of brain stem neurons to the perigeniculate nucleus and the lateral geniculate nucleus in the cat. Brain Research 238, 433–438.CrossRefGoogle Scholar
Aston-Jones, G. & Bloom, F.E. (1981). Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. Journal of Neuroscience 1, 876–886.CrossRefGoogle ScholarPubMed
Bickford, M.E., Günlük, A.E., Guido, W. & Sherman, S.M. (1993 a). Evidence that cholinergic axons from the parabrachial region of the brainstem are the exclusive source of nitric oxide in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 334, 410–430.CrossRefGoogle ScholarPubMed
Bickford, M.E., Günlük, A.E., Guido, W. & Sherman, S.M. (1993 b). Basal forebrain projection to the visual thalamic reticular nucleus in the cat. Society for Neuroscience Abstracts 19, 14.Google Scholar
Bloomfield, S.A. & Sherman, S.M. (1987). Passive cable properties and morphological correlates of neurones in the lateral geniculate nucleus of the cat. Journal of Physiology 383, 653–692.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Lee, B.B. (1985). A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. Journal of Physiology 369, 249–268.CrossRefGoogle Scholar
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1988). Parabrachial innervation of the cat's lateral geniculate nucleus, an electron microscopic study using the tracer phaseolus vulgaris leucoagglutinin (PHA-L). Journal of Neuroscience 8, 4576–4588.CrossRefGoogle ScholarPubMed
De Lima, A.D., Montero, V.M. & Singer, W. (1985). The cholinergic innervation of the visual thalamus, an EM immunocytochemical study. Experimental Brain Research 59, 206–212.CrossRefGoogle ScholarPubMed
De Lima, A.D. & Singer, W. (1987). The brainstem projection to the lateral geniculate nucleus in the cat, identification of cholinergic and monoaminergic elements. Journal of Comparative Neurology 259, 92–121.CrossRefGoogle Scholar
Dingledine, R. & Kelly, J.S. (1977). Brain stem stimulation and acetylcholine-evoked inhibition of neurons in the feline nucleus reticularis thalami. Journal of Physiology 271, 135–154.CrossRefGoogle ScholarPubMed
Dubin, M.W. & Cleland, B.G. (1977). The organization of visual inputs to interneurons of the lateral geniculate nucleus of the cat. Journal of Neurophysiology 40, 410–427.CrossRefGoogle ScholarPubMed
Frrzpatrick, D., Penny, G.R. & Schmechel, D.E. (1984). Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. Journal of Neuroscience 4, 1809–1829.CrossRefGoogle Scholar
Francesconi, W., Müller, C. M. & Singer, W. (1988). Cholinergic mechanisms in the reticular control of transmission in the cat lateral geniculate nucleus. Journal of Neurophysiology 59, 1690–1718.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Lin, C.-S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in the lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80–129.CrossRefGoogle ScholarPubMed
Fukuda, Y. & Stone, J. (1976). Evidence of differential inhibitory influences on X- and Y-type relay cells in the cat’s lateral geniculate nucleus. Brain Research 113, 188–196.CrossRefGoogle ScholarPubMed
Godfraind, J.M. (1978). Acetylcholine and somatically evoked inhibition on perigeniculate neurones in the cat. British Journal of Pharmacology 63, 295–302.CrossRefGoogle ScholarPubMed
Hartveit, E., Ramberg, S.I. & Heggelund, P. (1993). Brainstem modulation of spatial receptive field properties of single cells in the dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 70, 1644–1655.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1961). Integrative action in the cat’s lateral geniculate body. Journal of Physiology 155, 385–398.CrossRefGoogle ScholarPubMed
Ide, L.S. (1982). The fine structure of the perigeniculate nucleus in the cat. Journal of Comparative Neurology 210, 317–334.CrossRefGoogle ScholarPubMed
Kimura, H., McGeer, P.L., Peng, J.H. & McGeer, E.G. (1981). The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. Journal of Comparative Neurology 200, 151–201.CrossRefGoogle ScholarPubMed
Lindström, S. (1982). Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus. Brain Research 23, 447–453.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1981). Effects of sleep and arousal on the processing of visual information in the cat. Nature 291, 554–561.CrossRefGoogle ScholarPubMed
Lu, S.-M., Guido, W. & Sherman, S.M. (1993). The brainstem parabrachial region controls mode of response to visual stimulation of neurons in the cat’s lateral geniculate nucleus. Visual Neuroscience 10, 631–642.CrossRefGoogle ScholarPubMed
McCormick, D.A. (1989). Cholinergic and noradrenergic modulation of thalamocortical processing. TINS 12, 215–221.Google ScholarPubMed
McCormick, D.A. & Pape, H.-C. (1988). Acetylcholine inhibits identified interneurons in the cat lateral geniculate nucleus. Nature 334, 246–248.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Prince, D.A. (1986). Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature 319, 402–405.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Prince, D.A. (1987). Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei. Journal of Physiology 392, 147–165.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Wang, Z. (1991). Serotonin and noradrenalin excite GABAergic neurones of the guinea-pig and cat nucleus reticularis thalami. Journal of Physiology 442, 235–255.CrossRefGoogle ScholarPubMed
Montero, V.M. (1989). Ultrastructural identification of synaptic terminals from cortical axons and from collateral axons of geniculo-cortical relay cells in the perigeniculate nucleus of the cat. Experimental Brain Research 75, 65–72.CrossRefGoogle ScholarPubMed
Montero, V.M. & Scott, G.L. (1981). Synaptic terminals in dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus. A light and electron microscope autoradiographic study. Neuroscience 6, 2561–2577.CrossRefGoogle ScholarPubMed
Montero, V.M. & Zempel, J. (1985). Evidence for two types of GABA-containing interneurons in the A-laminae of the cat lateral geniculate nucleus, a double-label HRP and GABA-immunocytochemical study. Experimental Brain Research 60, 603–609.Google ScholarPubMed
Mukhametov, L.M., Rizzolatti, G. & Tradardi, V. (1970). Spontaneous activity of nucleus reticularis thalami in freely moving cats. Journal of Physiology 210, 651–667.CrossRefGoogle ScholarPubMed
Murphy, P.C., Uhlrich, D.J., Tamamaki, N. & Sherman, S.M. (1989). Brainstem modulation of perigeniculate cells in cats. Society for Neuroscience A bstracts 15, 175.Google Scholar
Phillis, J.W., Tabecis, A.K. & York, D.H. (1967). A study of cholinoceptive cells in the lateral geniculate nucleus. Journal of Physiology 192, 695–713.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Fitzpatrick, D. (1989). The organization of cholinergic synapses in the cat’s dorsal lateral geniculate and perigeniculate nuclei. Journal of Comparative Neurology 288, 676–690.CrossRefGoogle ScholarPubMed
Sanderson, K.S. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. Journal of Comparative Neurology 143, 101–118.CrossRefGoogle Scholar
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Experimental Brain Research 63, 1–20.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Koch, C. (1990). Thalamus. Synaptic Organization of the Brain, third edition, ed. Shepherd, G.M., pp. 246–278. New York: Oxford University Press.Google Scholar
Sillito, A.M., Kemp, J.A. & Berardi, N. (1983). The cholinergic influence on the function of the cat dorsal lateral geniculate nucleus (dLGN). Brain Research 280, 299–307.CrossRefGoogle ScholarPubMed
Singer, W. (1973). The effect of mesencephalic reticular stimulation on intracellular potentials of cat lateral geniculate neurons. Brain Research 61, 35–54.CrossRefGoogle ScholarPubMed
Singer, W., Tretter, F. & Cynader, M. (1976). The effect of reticular stimulation on spontaneous and evoked activity in the cat visual cortex. Brain Research 102, 71–90.CrossRefGoogle ScholarPubMed
Smith, Y., Paré, D., Dreschênes, M., Parent, A. & Steriade, M. (1988). Cholinergic and non-cholinergic projections from the upper brainstem core to the visual thalamus in the cat. Experimental Brain Research 70, 166–180.CrossRefGoogle Scholar
So, Y.T. & Shapley, R. (1981). Spatial tuning of cells in and around lateral geniculate nucleus of the cat, X and Y relay cells and perigeniculate interneurons. Journal of Neurophysiology 45, 107–119.CrossRefGoogle Scholar
Steriade, M. & Deschênes, M. (1988). Intrathalamic and brainstemthalamic networks involved in resting and alert states. In Cellular Thalamic Mechanisms, ed. Bentivoglio, M. & Spreafico, R. pp. 37–62. New York: Elsevier Science Publishers BV (Biomedical Division).Google Scholar
Steriade, M., Domich, L. & Oakson, G. (1986). Reticularis thalami neurons revisited, activity changes during shifts in states of vigilance. Journal of Neuroscience 6, 68–81.CrossRefGoogle ScholarPubMed
Steriade, M. & Llinás, R.R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68, 649–742.CrossRefGoogle ScholarPubMed
Steriade, M., Oakson, G. & Ropert, N. (1982). Firing rates and patterns of midbrain reticular neurons during steady and transitional states of the sleep-waking cycle. Experimental Brain Research 46, 37–51.CrossRefGoogle ScholarPubMed
Trulson, M.F. & Jacobs, B.L. (1979). Raphe unit activity in freely moving cats, correlation with level of behavioral arousal. Brain Research 163, 135–150.CrossRefGoogle ScholarPubMed
Uhlrich, D.J., Cucchiaro, J.B., Humphrey, A.L. & Sherman, S.M. (1991). Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus. Journal of Neurophysiology 65, 1528–1541.CrossRefGoogle ScholarPubMed
Uhlrich, D.J., Cucchiaro, J.B. & Sherman, S.M. (1988). The projection of individual axons from the parabrachial region of the brain stem to the dorsal lateral geniculate nucleus in the cat. Journal of Neuroscience 8, 4565–4575.CrossRefGoogle Scholar
Uhlrich, D.J., Tamamaki, N., Murphy, P.C. & Sherman, S.M. (1989). Brainstem modulation of geniculate cells in cats. Society for Neuroscience Abstracts 15, 175.Google Scholar
Updyke, B.V. (1975). The patterns of projection of cortical area 17, 18, and 19 onto the laminae of the dorsal lateral geniculate nucleus in the cat. Journal of Comparative Neurology 163, 377–396.CrossRefGoogle Scholar
Vincent, S.R., Satoh, K., Armstrong, D.M., Panula, P., Vale, W. & Fibiger, H.C. (1986). Neuropeptides and NADPH-diaphorase activity in the ascending cholinergic reticular system of the rat. Neuroscience 17, 167–182.CrossRefGoogle ScholarPubMed
Wrobél, A. – Tarnecki, R. (1984). Receptive fields of cat’s non-relay lateral geniculate and perigeniculate neurons. Acta Neurobiologial Experimentalis 44, 289–299.Google ScholarPubMed