Abstract
The neocortex generates periods of recurrent activity, such as the slow (0.1–0.5 Hz) oscillation during slow-wave sleep. Here we demonstrate that slices of ferret neocortex maintained in vitro generate this slow (< 1 Hz) rhythm when placed in a bathing medium that mimics the extracellular ionic composition in situ. This slow oscillation seems to be initiated in layer 5 as an excitatory interaction between pyramidal neurons and propagates through the neocortex. Our results demonstrate that the cerebral cortex generates an ‘up’ or depolarized state through recurrent excitation that is regulated by inhibitory networks, thereby allowing local cortical circuits to enter into temporarily activated and self-maintained excitatory states. The spontaneous generation and failure of this self-excited state may account for the generation of a subset of cortical rhythms during sleep.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Steriade, M., McCormick, D. A. & Sejnowski, T. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679–685 (1993).
Steriade, M., Nunez, A. & Amzica, F. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252–3265 (1993).
Steriade, M., Contreras, D., Curro Dossi, R. & Nunez, A. 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, 3266–3283 (1993).
Steriade, M., Nunez, A. & Amzica, F. Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms in the electroencephalogram. J. Neurosci. 13, 3266–3283 (1993).
Contreras, D., Timofeev, I. & Steriade, M. Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J. Physiol. (Lond.) 494, 251–264 (1996).
Metherate, R. & Ashe, J. H. Ionic flux contributions to neocortical slow waves and nucleus basalis-mediated activation: whole-cell recordings in vivo. J. Neurosci. 13, 5312–5323 (1993).
Lampl, I., Reichova, I. & Ferster, D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22, 361–374 (1999).
Stern, E. A., Kincaid, A. E. & Wilson, C. J. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77, 1697–1715 (1997).
Achermann, P. & Borbely, A. A. Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81, 213–222 (1997).
von Krosigk, M., Bal, T. & McCormick, D. A. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261, 361–364 (1993).
Steriade, M. & Contreras, D. Relations between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity. J. Neurosci. 15, 623–642 (1995).
Yamaguchi, T. Cerebral extracellular potassium concentration change and cerebral impedance change in short-term ischemia in gerbil. Bull. Tokyo Med. Dent. Univ. 33, 1–8 (1986).
Zhang, E. T., Hansen, A. J., Wieloch, T. & Lauritzen, M. Influence of MK-801 on brain extracellular calcium and potassium activities in severe hypoglycemia. J. Cereb. Blood Flow Metab. 10, 136–139 (1990).
Connors, B. W. Initiation of synchronized neuronal bursting in neocortex. Nature 310, 685–687 (1984).
Telfeian, A. E. & Connors, B. W. Epileptiform propagation patterns mediated by NMDA and non-NMDA receptors in rat neocortex. Epilepsia 40, 1499–1506 (1999).
Avoli, M., Drapeau, C., Louvel, J., Olivier, A. & Villemure, J. G. Epileptiform activity induced by low extracellular magnesium in the human cortex maintained in vitro. Ann. Neurol. 30, 589–596 (1991).
Chagnac-Amitai, Y. & Connors, B. W. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61, 747–758 (1989).
McCormick, D. A., Connors, B. W., Lighthall, J. W. & Prince, D. A. Comparative electrophysiology of pyramidal and sparsely spiny neurons of the neocortex. J. Neurophysiol. 54, 782–806 (1985).
Raman, I. M. & Bean, B. P. Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J. Neurosci. 19, 1663–1674 (1999).
Haj-Dahmane, S. & Andrade, R. Ionic mechanism of the slow afterdepolarization induced by muscarinic receptor activation in rat prefrontal cortex. J. Neurophysiol. 80, 1197–1210 (1998).
Wang, X.-J. Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J. Neurosci. 19, 9587–9603 (1999).
Nowak, L. G. & Bullier, J. in Cerebral Cortex: Extrastriate Cortex in Primates Vol. 12 (eds. Rockland, K., Kaas, J. H. & Peters, A.) 205–241 (Plenum, New York 1997).
Amzica, F. & Steriade, M. Short- and long-range neuronal synchronization of the slow (< 1 Hz) cortical oscillation. J. Neurophysiol. 73, 20–38 (1995).
Tsodyks, M., Kenet, T., Grinvald, A. & Arieli, A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286, 1943–1946 (1999).
Sanchez-Vives, M. V., Nowak, L. G. & McCormick, D. A. Cellular mechanisms of long lasting adaptation in visual cortical neurons in vitro. J. Neurosci. 20, 4286–4299 (2000).
Schwindt, P. C., Spain, W. J. & Crill, W. E. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortex neurons. J. Neurophysiol. 61, 233–244 (1989).
Douglas, R. J., Koch, C., Mahowald, M., Martin, K. A. & Suarez, H. H. Recurrent excitation in neocortical circuits. Science 269, 981–985 (1995).
Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical cells. J. Neurosci. 15, 5449–5465 (1995).
Staley, K. J., Longacher, M., Bains, J. S. & Yee, A. Presynaptic modulation of CA3 network activity. Nat. Neurosci. 1, 201–209 (1998).
Foehring, R. C., Schwindt, P. C. & Crill, W. E. Norepinephrine selectively reduces slow Ca2+- and Na+- mediated K+ currents in cat neocortical neurons. J. Neurophysiol. 61, 245–256 (1989).
Arieli, A., Sterkin, A., Grinvald, A. & Aertsen, A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868–1871 (1996).
Steriade, M., Amzica, F. & Nunez, A. Cholinergic and noradrenergic modulation of slow (approximately 0.3 Hz) oscillation in neocortical cells. J. Neurophysiol. 70, 1385–1400 (1993).
Lewandowski, M. H., Muller, C. M. & Singer, W. Reticular facilitation of cat visual cortical responses is mediated by nicotinic and muscarinic cholinergic mechanisms. Exp. Brain Res. 96, 1–7 (1993).
Anderson, J., Lampl, I., Reichova, I., Carandini, M. & Ferster, D. Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nat. Neurosci. 3, 617–621 (2000).
Phillis, J. W. Acetylcholine release from the cerebral cortex: its role in cortical arousal. Brain Res. 7, 378–389 (1968).
Luck, S. J., Chelazzi, L., Hillyard, S. A. & Desimone, R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24–42 (1997).
Mountcastle, V. B., Motter, B. C., Steinmetz, M. A. & Sestokas, A. K. Common and differential effects of attentive fixation on the excitability of parietal and prestriate (V4) cortical visual neurons in the macaque monkey. J. Neurosci. 7, 2239–2255 (1987).
Goldman-Rakic, P. S. Cellular basis of working memory. Neuron 14, 477–485 (1995).
Hebb, D. O. The Organization of Behavior (John Wiley, New York, 1949).
Lorente de No, R. Analysis of the activity of the chains of internuncial neurons. J. Neurophysiol. 1, 207–244 (1938).
Snodderly, D. M. & Gur, M. Organization of striate cortex of alert, trained monkeys (Macaca fascicularis): Ongoing activity, stimulus selectivity, and widths of receptive field activating regions. J. Neurophysiol. 74, 2100–2125 (1995).
Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).
Reid, R. C. & Alonso, J. M. The processing and encoding of information in the visual cortex. Curr. Opin. Neurobiol. 6, 475–480 (1996).
Sanchez-Vives, M. V., Nowak, L. G. & McCormick, D. A. Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J. Neurosci. 20, 4267–4285 (2000).
Acknowledgements
We thank L. G. Nowak for participation in critical portions of these experiments. We thank L. Nowak, A. Luthi, J. Brumberg, H. Blumenfeld and R. Gallego for comments on the manuscript. This work was supported by the NIH and the McKnight Foundation. For movies and additional information see http://www.mccormicklab.org.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sanchez-Vives, M., McCormick, D. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3, 1027–1034 (2000). https://doi.org/10.1038/79848
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/79848
This article is cited by
-
The effects of different acetylcholinesterase inhibitors on EEG patterns in patients with Alzheimer’s disease: A systematic review
Neurological Sciences (2024)
-
A brain cytokine-independent switch in cortical activity marks the onset of sickness behavior triggered by acute peripheral inflammation
Journal of Neuroinflammation (2023)
-
Recurrent activity in neuronal avalanches
Scientific Reports (2023)
-
Somatostatin-expressing interneurons modulate neocortical network through GABAb receptors in a synapse-specific manner
Scientific Reports (2023)
-
Diversity of cortical activity changes beyond depression during Spreading Depolarizations
Nature Communications (2023)