Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback

Science

Volumn 274, Issue 5288, 1996, Pages 771-774

  Contreras, Diego ^a   Destexhe, Alain ^a   Sejnowski, Terrence J ^b,c   Steriade, Mircea ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CAT; DECORTICATION; FEEDBACK SYSTEM; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; THALAMUS; THALAMUS NUCLEUS;

ANESTHESIA; ANIMALS; CATS; CEREBRAL CORTEX; CORTICAL SYNCHRONIZATION; ELECTROPHYSIOLOGY; FEEDBACK; NEURAL PATHWAYS; SLEEP; SYNAPTIC TRANSMISSION; THALAMUS;

ANIMALIA; FELIS CATUS; MAMMALIA;

EID: 0029909130     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.274.5288.771     Document Type: Article

References (29)

1. M. Steriade, E. G. Jones, R. R. Llinás, Thalamic Oscillations and Signaling (Wiley, New York, 1990); M. Steriade, D. A. McCormick, T. J. Sejnowski, Science 262, 679 (1993).
2. M. Steriade, E. G. Jones, R. R. Llinás, Thalamic Oscillations and Signaling (Wiley, New York, 1990); M. Steriade, D. A. McCormick, T. J. Sejnowski, Science 262, 679 (1993).
3. R. S. Morison and D. L. Basset, J. Neurophysiol. 8, 309 (1945). Electrophysiological experiments in vivo demonstrated that spindles could be generated in a surgically isolated patch containing the rostral pole of the RE nucleus [M. Steriade, L. Domich, G. Oakson, M. Deschênes, ibid. 57, 260 (1987)] and that lesioning of the RE nucleus disrupted spindling in dorsal thalamic nuclei [M. Steriade, M. Deschênes, L. Domich, C. Mulle, ibid. 54, 1473 (1985)]. In slices from the caudal thalamus, disconnection between RE cells and dorsal thalamus disrupted spontaneous oscillations in the RE nucleus [M. von Krosigk, T. Bal, D. A. McCormick, Science 261, 361 (1993)), although RE cells generated intrinsic oscillations in the frequency range of spindling [T. Bal and D. A. Mc-Cormick, J. Physiol. (London) 468, 669 (1993)]. Modeling studies have proposed a scenario to explain the absence of spindles in RE cells studied in vitro, based on the absence of neuromodulation in thalamic slices [A. Destexhe, D. Contreras, T. J. Sejnowski, M. Steriade, Neuroreport 5, 2217 (1994)].
4. R. S. Morison and D. L. Basset, J. Neurophysiol. 8, 309 (1945). Electrophysiological experiments in vivo demonstrated that spindles could be generated in a surgically isolated patch containing the rostral pole of the RE nucleus [M. Steriade, L. Domich, G. Oakson, M. Deschênes, ibid. 57, 260 (1987)] and that lesioning of the RE nucleus disrupted spindling in dorsal thalamic nuclei [M. Steriade, M. Deschênes, L. Domich, C. Mulle, ibid. 54, 1473 (1985)]. In slices from the caudal thalamus, disconnection between RE cells and dorsal thalamus disrupted spontaneous oscillations in the RE nucleus [M. von Krosigk, T. Bal, D. A. McCormick, Science 261, 361 (1993)), although RE cells generated intrinsic oscillations in the frequency range of spindling [T. Bal and D. A. Mc-Cormick, J. Physiol. (London) 468, 669 (1993)]. Modeling studies have proposed a scenario to explain the absence of spindles in RE cells studied in vitro, based on the absence of neuromodulation in thalamic slices [A. Destexhe, D. Contreras, T. J. Sejnowski, M. Steriade, Neuroreport 5, 2217 (1994)].
5. R. S. Morison and D. L. Basset, J. Neurophysiol. 8, 309 (1945). Electrophysiological experiments in vivo demonstrated that spindles could be generated in a surgically isolated patch containing the rostral pole of the RE nucleus [M. Steriade, L. Domich, G. Oakson, M. Deschênes, ibid. 57, 260 (1987)] and that lesioning of the RE nucleus disrupted spindling in dorsal thalamic nuclei [M. Steriade, M. Deschênes, L. Domich, C. Mulle, ibid. 54, 1473 (1985)]. In slices from the caudal thalamus, disconnection between RE cells and dorsal thalamus disrupted spontaneous oscillations in the RE nucleus [M. von Krosigk, T. Bal, D. A. McCormick, Science 261, 361 (1993)), although RE cells generated intrinsic oscillations in the frequency range of spindling [T. Bal and D. A. Mc-Cormick, J. Physiol. (London) 468, 669 (1993)]. Modeling studies have proposed a scenario to explain the absence of spindles in RE cells studied in vitro, based on the absence of neuromodulation in thalamic slices [A. Destexhe, D. Contreras, T. J. Sejnowski, M. Steriade, Neuroreport 5, 2217 (1994)].
6. R. S. Morison and D. L. Basset, J. Neurophysiol. 8, 309 (1945). Electrophysiological experiments in vivo demonstrated that spindles could be generated in a surgically isolated patch containing the rostral pole of the RE nucleus [M. Steriade, L. Domich, G. Oakson, M. Deschênes, ibid. 57, 260 (1987)] and that lesioning of the RE nucleus disrupted spindling in dorsal thalamic nuclei [M. Steriade, M. Deschênes, L. Domich, C. Mulle, ibid. 54, 1473 (1985)]. In slices from the caudal thalamus, disconnection between RE cells and dorsal thalamus disrupted spontaneous oscillations in the RE nucleus [M. von Krosigk, T. Bal, D. A. McCormick, Science 261, 361 (1993)), although RE cells generated intrinsic oscillations in the frequency range of spindling [T. Bal and D. A. Mc-Cormick, J. Physiol. (London) 468, 669 (1993)]. Modeling studies have proposed a scenario to explain the absence of spindles in RE cells studied in vitro, based on the absence of neuromodulation in thalamic slices [A. Destexhe, D. Contreras, T. J. Sejnowski, M. Steriade, Neuroreport 5, 2217 (1994)].
7. R. S. Morison and D. L. Basset, J. Neurophysiol. 8, 309 (1945). Electrophysiological experiments in vivo demonstrated that spindles could be generated in a surgically isolated patch containing the rostral pole of the RE nucleus [M. Steriade, L. Domich, G. Oakson, M. Deschênes, ibid. 57, 260 (1987)] and that lesioning of the RE nucleus disrupted spindling in dorsal thalamic nuclei [M. Steriade, M. Deschênes, L. Domich, C. Mulle, ibid. 54, 1473 (1985)]. In slices from the caudal thalamus, disconnection between RE cells and dorsal thalamus disrupted spontaneous oscillations in the RE nucleus [M. von Krosigk, T. Bal, D. A. McCormick, Science 261, 361 (1993)), although RE cells generated intrinsic oscillations in the frequency range of spindling [T. Bal and D. A. Mc-Cormick, J. Physiol. (London) 468, 669 (1993)]. Modeling studies have proposed a scenario to explain the absence of spindles in RE cells studied in vitro, based on the absence of neuromodulation in thalamic slices [A. Destexhe, D. Contreras, T. J. Sejnowski, M. Steriade, Neuroreport 5, 2217 (1994)].
8. R. S. Morison and D. L. Basset, J. Neurophysiol. 8, 309 (1945). Electrophysiological experiments in vivo demonstrated that spindles could be generated in a surgically isolated patch containing the rostral pole of the RE nucleus [M. Steriade, L. Domich, G. Oakson, M. Deschênes, ibid. 57, 260 (1987)] and that lesioning of the RE nucleus disrupted spindling in dorsal thalamic nuclei [M. Steriade, M. Deschênes, L. Domich, C. Mulle, ibid. 54, 1473 (1985)]. In slices from the caudal thalamus, disconnection between RE cells and dorsal thalamus disrupted spontaneous oscillations in the RE nucleus [M. von Krosigk, T. Bal, D. A. McCormick, Science 261, 361 (1993)), although RE cells generated intrinsic oscillations in the frequency range of spindling [T. Bal and D. A. Mc-Cormick, J. Physiol. (London) 468, 669 (1993)]. Modeling studies have proposed a scenario to explain the absence of spindles in RE cells studied in vitro, based on the absence of neuromodulation in thalamic slices [A. Destexhe, D. Contreras, T. J. Sejnowski, M. Steriade, Neuroreport 5, 2217 (1994)].
9. R. S. Morison and E. W. Dempsey, Am. J. Physiol. 138, 297 (1943).
10. P. Andersen and S. A. Andersson, Physiological Basis of the Alpha Rhythm (Appleton-Century-Crofts, New York, 1968).
11. Thalamic spindles can be induced by cortical stimulation, even by stimulating the contralateral cortex to avoid backfiring of thalamocortical axons [M. Steriade, P. Wyzinski, V. Apostol, in Corticothalamic Projections and Sensorimotor Activities. T. L. Frigyesi, E. Rinvik, M. D. Yahr, Eds. (Raven, New York, 1972), pp. 221-272; D. Contreras and M. Steriade, J. Physiol. (London) 490, 159 (1996)).
12. Thalamic spindles can be induced by cortical stimulation, even by stimulating the contralateral cortex to avoid backfiring of thalamocortical axons [M. Steriade, P. Wyzinski, V. Apostol, in Corticothalamic Projections and Sensorimotor Activities. T. L. Frigyesi, E. Rinvik, M. D. Yahr, Eds. (Raven, New York, 1972), pp. 221-272; D. Contreras and M. Steriade, J. Physiol. (London) 490, 159 (1996)).
13. D. Contreras and M. Steriade, J. Neurosci. 15, 604 (1995).
14. C. Koch, Neuroscience 23, 399 (1987).
15. A. M. Sillito, H. E. Jones, G. L. Gerstein, D. C. West, Nature 369, 479 (1994).
16. M. A. L. Nicolelis, R. C. S. Lin, D. J. Woodward, J. K. Chapin, Proc. Natl. Acad. Sci. U.S.A. 90, 2212 (1993).
17. Propagation of spindle oscillations was observed in experiments on thalamic slices [U. Kim, T. Bal, D. A. McCormick, J. Neurophysiol. 74, 1301 (1995)] and in computational models of thalamic slices [D. Golomb, X. J. Wang, J. Rinzel, ibid. 75, 750 (1996); A. Destexhe, T. Bal, D. A. McCormick, T. J. Sejnowski, ibid. 76, 2049 (1996)]. In the present in vivo experiments, we have only observed propagation of spindles in the thalamus after decortication as an exception. Spindle sequences occasionally showed synchrony even among widely spaced thalamic territories (Fig. 1, bottom; Fig. 2, decorticated spectra).
18. Propagation of spindle oscillations was observed in experiments on thalamic slices [U. Kim, T. Bal, D. A. McCormick, J. Neurophysiol. 74, 1301 (1995)] and in computational models of thalamic slices [D. Golomb, X. J. Wang, J. Rinzel, ibid. 75, 750 (1996); A. Destexhe, T. Bal, D. A. McCormick, T. J. Sejnowski, ibid. 76, 2049 (1996)]. In the present in vivo experiments, we have only observed propagation of spindles in the thalamus after decortication as an exception. Spindle sequences occasionally showed synchrony even among widely spaced thalamic territories (Fig. 1, bottom; Fig. 2, decorticated spectra).
19. Propagation of spindle oscillations was observed in experiments on thalamic slices [U. Kim, T. Bal, D. A. McCormick, J. Neurophysiol. 74, 1301 (1995)] and in computational models of thalamic slices [D. Golomb, X. J. Wang, J. Rinzel, ibid. 75, 750 (1996); A. Destexhe, T. Bal, D. A. McCormick, T. J. Sejnowski, ibid. 76, 2049 (1996)]. In the present in vivo experiments, we have only observed propagation of spindles in the thalamus after decortication as an exception. Spindle sequences occasionally showed synchrony even among widely spaced thalamic territories (Fig. 1, bottom; Fig. 2, decorticated spectra).
20. Power spectra were calculated according to W. H. Press, B. Plannery, S. A. Teukolsky, and W. T. Vetterling [Numerical Recipes. The Art of Scientific Computing (Cambridge Univ. Press, Cambridge, 1986)].
21. E. G. Jones, The Thalamus (Plenum, New York, 1985).
22. 2 concentration at around 3.7%. Further stability was obtained by performing cisternal drainage, bilateral pneumothorax, and hip suspension, and by filling the hole left by the decortication with a 4% agar solution. Body temperature was maintained at 37° to 38°C. A constant state of deep anesthesia was obtained by additional doses of barbiturate and continuous monitoring of the electroencephalogram (EEG) from the contralateral hemisphere. A high-impedance amplifier with active bridge circuitry was used to record and inject current in the cells. The signals were recorded on an eight-channel tape with bandpass of 0 to 9 kHz and digitized off-line at 10 kHz for analysis and display.
23. Intracellular recordings in barbiturate-anesthetized cats have shown that, during spindles, the GABA-containing RE cells generate rhythmic spike-bursts within the frequency range of spindling, superimposed on a slowly rising and decaying depolarizing envelope (1). Spike-bursts of RE cells, particularly those in the rostral pole and rostrolateral sector of the nucleus, impose rhythmic IPSPs onto a large number of TC cells through their divergent connections in the dorsal thalamus [M. Steriade, A. Parent, J. Hada, J. Comp. Neurol. 229, 531 (1984)]. TC rebound bursts are generated at the offset of the IPSPs and transmitted back to RE cells, where they generate AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate)-kainate excitatory postsynaptic potentials (EPSPs) [T. Bal, M. von Krosigk, D. A. McCormick, J. Physiol. (London) 483, 641 (1995)], and to neocortical cells, where glutamatergic EPSPs are at the basis of the spindle oscillations observable in the EEG [M. Steriade and M. Deschênes, in Cellular Thalamic Mechanisms, M. Bentivoglio and R. Spreafico, Eds. (Elsevier, Amsterdam, 1988), pp. 51-76].
24. Intracellular recordings in barbiturate-anesthetized cats have shown that, during spindles, the GABA-containing RE cells generate rhythmic spike-bursts within the frequency range of spindling, superimposed on a slowly rising and decaying depolarizing envelope (1). Spike-bursts of RE cells, particularly those in the rostral pole and rostrolateral sector of the nucleus, impose rhythmic IPSPs onto a large number of TC cells through their divergent connections in the dorsal thalamus [M. Steriade, A. Parent, J. Hada, J. Comp. Neurol. 229, 531 (1984)]. TC rebound bursts are generated at the offset of the IPSPs and transmitted back to RE cells, where they generate AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate)-kainate excitatory postsynaptic potentials (EPSPs) [T. Bal, M. von Krosigk, D. A. McCormick, J. Physiol. (London) 483, 641 (1995)], and to neocortical cells, where glutamatergic EPSPs are at the basis of the spindle oscillations observable in the EEG [M. Steriade and M. Deschênes, in Cellular Thalamic Mechanisms, M. Bentivoglio and R. Spreafico, Eds. (Elsevier, Amsterdam, 1988), pp. 51-76].
25. Intracellular recordings in barbiturate-anesthetized cats have shown that, during spindles, the GABA-containing RE cells generate rhythmic spike-bursts within the frequency range of spindling, superimposed on a slowly rising and decaying depolarizing envelope (1). Spike-bursts of RE cells, particularly those in the rostral pole and rostrolateral sector of the nucleus, impose rhythmic IPSPs onto a large number of TC cells through their divergent connections in the dorsal thalamus [M. Steriade, A. Parent, J. Hada, J. Comp. Neurol. 229, 531 (1984)]. TC rebound bursts are generated at the offset of the IPSPs and transmitted back to RE cells, where they generate AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate)-kainate excitatory postsynaptic potentials (EPSPs) [T. Bal, M. von Krosigk, D. A. McCormick, J. Physiol. (London) 483, 641 (1995)], and to neocortical cells, where glutamatergic EPSPs are at the basis of the spindle oscillations observable in the EEG [M. Steriade and M. Deschênes, in Cellular Thalamic Mechanisms, M. Bentivoglio and R. Spreafico, Eds. (Elsevier, Amsterdam, 1988), pp. 51-76].
26. I. Timofeev and M. Steriade, J. Neurophysiol., in press.
27. C. Avendaño, E. Rausell, D. Perez-Aguilar, S. Isorna, J. Comp. Neurol. 278, 1 (1988).
28. The possibility that corticocortical connections, other than those disrupted by the cut in the suprasylvian gyrus, might account for the preserved synchrony of spindles is remote, because the same type of suprasylvian transection succeeded in immediately disrupting the synchrony of an intracortically generated slow oscillation [F. Amzica and M. Steriade, J. Neurosci. 15, 4658 (1995)].
29. We thank D. Drolet, P. Giguère, and G. Oakson for technical assistance. Supported by the Medical Research Council of Canada, Human Frontier Science Program, Fonds de la Recherche en Santé du Qué bec, and the Howard Hughes Medical Institute.