Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T07:05:58.598Z Has data issue: false hasContentIssue false
  • English
  • Français

Dual response modes in lateral geniculate neurons: Mechanisms and functions

Published online by Cambridge University Press:  02 June 2009

S. Murray Sherman
S. Murray Sherman
Affiliation:
Department of Neurobiology, State University of New York, Stony Brook
Get access Rights & Permissions [Opens in a new window]

Abstract

Relay cells of the lateral geniculate nucleus, like those of other thalamic nuclei, manifest two distinct response modes, and these represent two very different forms of relay of information to cortex. When relatively hyperpolarized, these relay cells respond with a low threshold Ca2+ spike that triggers a brief burst of conventional action potentials. These cells switch to tonic mode when depolarized, since the low threshold Ca2+ spike, being voltage dependent, is inactivated at depolarized levels. In this mode they relay information with much more fidelity. This switch can occur under the influence of afferents from the visual cortex or parabrachial region of the brain stem. It has been previously suggested that the tonic mode is characteristic of the waking state while the burst mode signals an interruption of the geniculate relay during sleep. This review surveys the key properties of these two response modes and discusses the implications of new evidence that the burst mode may also occur in the waking animal.

Keywords

Lateral geniculate nucleusLow threshold spikeSignal detectionBurst and tonic modesCorticogeniculate pathway
Type
Review Article
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 205 - 213
Copyright
Copyright © Cambridge University Press 1996

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

Baker, F.H. & Malpeli, J.G. (1977). Effects of cryogenic blockade of visual cortex on the responses of lateral geniculate neurons in the monkey. Experimental Brain Research 29, 433–444.Google ScholarPubMed
Bal, T., Von Krosigk, M. & McCormick, D.A. (1995). Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. Journal of Physiology (London) 483, 641–663.CrossRefGoogle ScholarPubMed
Bickford, M.E., GÜNlÜ-K, A.E., Guido, W. & Sherman, S.M. (1993). 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., GÜNlÜ-K, A.E., Van Horn, S.C. & Sherman, S.M. (1994). GABAergic projection from the basal forebrain to the visual sector of the thalamic reticular nucleus in the cat. Journal of Comparative Neurology 348, 481–510.CrossRefGoogle Scholar
BÜttner, U. & Fuchs, A.F. (1973). Influence of saccadic eye movements on unit activity in simian lateral geniculate and perigeniculate nuclei. Journal of Neurophysiology 36, 127–141.CrossRefGoogle Scholar
Cledland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. Journal of Physiology (London) 217, 473–496.CrossRefGoogle Scholar
Crick, F. (1984). Function of the thalamic reticular complex: The searchlight hypothesis. Proceedings of the National Academy of Sciences of the U.S.A. 81, 4586–4590.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1993). Ultrastructure of synapses from the pretectum in the A-laminae of the cat's lateral geniculate nucleus. Journal of Comparative Neurology 334, 618–630.CrossRefGoogle ScholarPubMed
Geisert, E.E., Langsetmo, A. & Spear, P.D. (1981). Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons. Brain Research 208, 409–415.CrossRefGoogle ScholarPubMed
Godwin, D.W., Vaughan, J.W. & Sherman, S.M. (1994). Metabotropic glutamate receptors switch firing mode of cat LGN cells in vivo from burst to tonic. Society for Neuroscience Abstracts 20, 7.Google Scholar
Green, D.M. & Swets, J.A. (1966). Signal Detection Theory and Psychophysics. New York: Wiley.Google Scholar
Guido, W., LU, S.-M. & Sherman, S.M. (1992). Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. Journal of Neurophysiology 68, 2199–2211.CrossRefGoogle Scholar
Guido, W., LU, S.-M., Vaughan, J.W., Godwin, D.W. & Sherman, S.M. (1995). Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode. Visual Neuroscience 12, 723–741.CrossRefGoogle ScholarPubMed
Guido, W. & Weyand, T.G. (1995). Burst responses in lateral geniculate neurons of the awake behaving cat. Journal of Neurophysiology 74, 1782–1786.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969 a). A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat. Zeitschrift für Zellforschung 96, 39–48.CrossRefGoogle Scholar
Guillery, R.W. (1969 b). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschrift für Zellforschung 96, 1–38.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1971). Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of cat and monkey: A brief review. Vision Research (Suppl.) 3, 211–227.CrossRefGoogle Scholar
Hartveit, E. & Heggelund, P. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. II. Nonlagged cells. Journal of Neurophysiology 63, 1361–1372.CrossRefGoogle ScholarPubMed
Heggelund, P. & Hartveit, E. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. I. Lagged cells. Journal of Neurophysiology 63, 1347–1360.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P., Stone, J. & Sherman, S.M. (1972). Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 35, 518–531.CrossRefGoogle ScholarPubMed
Hu, B., Steriade, M. & DeschÊNes, M. (1989 a). The cellular mechanism of thalamic ponto-geniculo-occipital waves. Neuroscience 31, 25–35.CrossRefGoogle ScholarPubMed
Hu, B., Steriade, M. & DeschÊNes, M. (1989 b). The effects of brainstem peribrachial stimulation on perigeniculate neurons: the blockage of spindle waves. Neuroscience 31, 1–12.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1961). Integrative action in the cat's lateral geniculate body. Journal of Physiology (London) 155, 385–398.CrossRefGoogle ScholarPubMed
Huguenard, J.R. & McCormick, D.A. (1992). Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. Journal of Neurophysiology 68, 1373–1383.CrossRefGoogle ScholarPubMed
Huguenard, J.R. & Prince, D.A. (1994). Intrathalamic rhythmicity studied in vitro: Nominal T-current modulation causes robust antioscillatory effects. Journal of Neuroscience 14, 5485–5502.CrossRefGoogle ScholarPubMed
Jahnsen, H. & LlinÁS, R. (1984 a). Electrophysiological properties of guinea-pig thalamic neurones: An in vitro study. Journal of Physiology (London) 349, 205–226.CrossRefGoogle ScholarPubMed
Jahnsen, H. & LlinÁS, R. (1984 b). Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. Journal of Physiology (London) 349, 227–247.CrossRefGoogle ScholarPubMed
Kalil, R.E. & Chase, R. (1970). Corticofugal influence on activity of lateral geniculate neurons in the cat. Journal of Neurophysiology 33, 459–474.CrossRefGoogle ScholarPubMed
Katz, L.C. (1987). Local circuitry of identified projection neurons in cat visual cortex brain slices. Journal of Neuroscience 7, 1223–1249.CrossRefGoogle ScholarPubMed
Kemp, J.A. & Sillito, A.M. (1982). The nature of the excitatory transmitter mediating X and Y cell inputs to the cat dorsal lateral geniculate nucleus. Journal of Physiology (London) 323, 377–391.CrossRefGoogle Scholar
Koch, C. (1987). The action of the corticofugal pathway on sensory thalamic nuclei: A hypothesis. Neuroscience 23, 399–406.CrossRefGoogle ScholarPubMed
Kwon, Y.H., Esguerra, M. & Sur, M. (1991). NMDA and non-NMDA receptors mediate visual responses of neurons in the cat's lateral geniculate nucleus. Journal of Neurophysiology 66, 414–428.CrossRefGoogle ScholarPubMed
Lal, R. & Friedlander, M.J. (1989). Gating of retinal transmission by afferent eye position and movement signals. Science 243, 93–96.CrossRefGoogle ScholarPubMed
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
LO, F.-S., LU, S.-M. & Sherman, S.M. (1991). Intracellular and extracellular in vivo recording of different response modes for relay cells of the cat's lateral geniculate nucleus. Experimental Brain Research 83, 317–328.CrossRefGoogle ScholarPubMed
LO, F.-S. & Sherman, S.M. (1993). ACh has voltage-independent effects on low threshold calcium spikes in LGN cells of the cat. Society for Neuroscience Abstracts 19, 527.Google Scholar
LU, S.-M., Guido, W. & Sherman, S.M. (1993). The brain-stem para-brachial region controls mode of response to visual stimulation of neurons in the cat's lateral geniculate nucleus. Visual Neuroscience 10, 631–642.CrossRefGoogle Scholar
Macmillan, N.A. & Creelman, C.D. (1991). Detection Theory: A User's Guide. Cambridge: Cambridge University Press.Google Scholar
McCarley, R.W., Benoit, O. & Barrionuevo, G. (1983). Lateral geniculate nucleus unitary discharge in sleep and waking: State- and rate-specific aspects. Journal of Neurophysiology 50, 798–818.CrossRefGoogle ScholarPubMed
McClurkin, J.W., Optican, L.M. & Richmond, B.J. (1994). Cortical feedback increases visual information transmitted by monkey parvocellular lateral geniculate nucleus neurons. Visual Neuroscience 11, 601–617.CrossRefGoogle ScholarPubMed
McClurkin, J.W. & Marrocco, R.T. (1984). Visual cortical input alters spatial tuning in monkey lateral geniculate nucleus cells. Journal of Physiology (London) 348, 135–152.CrossRefGoogle ScholarPubMed
McCormick, D.A. (1989). Cholinergic and noradrenergic modulation of thalamocortical processing. Trends in Neuroscience 12, 215–221.CrossRefGoogle ScholarPubMed
McCormick, D.A. (1992). Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Progress in Neurobiology 39, 337–388.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Bal, T. (1994). Sensory gating mechanisms of the thalamus. Current Opinions Neurobiology 4, 550–556.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Feeser, H.R. (1990). Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39, 103–113.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Huguenard, J.R. (1992). A model of the electrophysiological properties of thalamocortical relay neurons. Journal of Neurophysiology 68, 1384–1400.CrossRefGoogle Scholar
McCormick, D.A. & Pape, H.-C. (1990). Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. Journal of Physiology (London) 431, 291–318.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, in vitro. Journal of Physiology (London) 392, 147–165.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Von Krosigk, M. (1992). Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proceedings of the National Academy of Sciences of the U.S.A. 89, 2774–2778.CrossRefGoogle ScholarPubMed
Moody, C.I. & Sillito, A.M. (1988). The role of the N-methyl-D-aspartate (NMDA) receptor in the transmission of visual information in the feline dorsal lateral geniculate nucleus (dLGN). Journal of Physiology (London) 396, 62P.Google Scholar
Noda, H. (1975). Depression in the excitability of relay cells of lateral geniculate nucleus following saccadic eye movements in the cat. Journal of Physiology (London) 249, 87–102.CrossRefGoogle ScholarPubMed
Richard, D., Gioanni, Y., Kitsikis, A. & Buser, P. (1975). A study of geniculate unit activity during cryogenic blockade of the primary visual cortex in the cat. Experimental Brain Research 22, 235–242.CrossRefGoogle ScholarPubMed
Scharfman, H.E., LU, S.-M., Guido, W., Adams, P.R. & Sherman, S.M. (1990). N-methyl-D-aspartate (NMDA) receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proceedings of the National Academy of Sciences of the U.S.A. 87, 4548–4552.CrossRefGoogle ScholarPubMed
Schmielau, F. & Singer, W. (1977). The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Research 120, 354–361.CrossRefGoogle ScholarPubMed
Sherman, S.M. (1993). Dynamic gating of retinal transmission to the visual cortex by the lateral geniculate nucleus. In Thalamic Networks for Relay and Modulation, ed. Minciacchi, D., Molinari, M., Macchi, G. & Jones, E.G., pp. 61–79. Oxford: Pergamon Press.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. In The Synaptic Organization of the Brain, 3rd edition, ed. Shepherd, G.M., pp. 246–278. New York: Oxford University Press.Google Scholar
Sillito, A.M., Murphy, P.C., Salt, T.E. & Moody, C.I. (1990). Dependence of retinogeniculate transmission in cat on NMDA receptors. Journal of Neurophysiology 63, 347–355.CrossRefGoogle ScholarPubMed
Sillito, A.M., Jones, H.E., Gerstein, G.L. & West, D.C. (1994). Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479–482.CrossRefGoogle ScholarPubMed
Singer, W. (1977). Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiology Reviews 57, 386–420.CrossRefGoogle ScholarPubMed
Steriade, M., Jones, E.G. & LlinÁS, R. (1990). Thalamic Oscillations and Signalling. New York: Wiley.Google Scholar
Steriade, M. (1992). Basic mechanisms of sleep generation. Neurology 42, 9–18.Google ScholarPubMed
Steriade, M., McCormick, D.A. & Sejnowski, T.J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679–685.CrossRefGoogle ScholarPubMed
Steriade, M. & Contreras, D. (1995). Relations between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity. Journal of Neuroscience 15, 623–642.CrossRefGoogle ScholarPubMed
Steriade, M. & LlinÁS, R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68, 649–742.CrossRefGoogle ScholarPubMed
Steriade, M. & McCarley, R.W. (1990). Brainstem control of wakefulness and sleep. New York: Plenum Press.CrossRefGoogle Scholar
Tsumoto, T. & Suda, K. (1980). Three groups of cortico-geniculate neurons and their distribution in binocular and monocular segments of cat striate cortex. Journal of Comparative Neurology 193, 223–236.CrossRefGoogle ScholarPubMed
Uhlrich, D.J., Manning, K.A. & Pienkowski, T.P. (1993). The histaminergic innervation of the lateral geniculate complex in the cat. Visual Neuroscience 10, 225–235.CrossRefGoogle ScholarPubMed
Vaughan, J.W., Godwin, D.W. & Sherman, S.M. (1994). Metabotropic glutamate receptors increase visual response linearity of LGN cells in the cat. Society for Neuroscience Abstracts 20, 8.Google Scholar