Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep

Andrea Pigorini, Simone Sarasso, Paola Proserpio, Caroline Szymanski, Gabriele Arnulfo, Silvia Casarotto, Matteo Fecchio, Mario Rosanova, Maurizio Mariotti, Giorgio Lo Russo, J. Matias Palva, Lino Nobili, Marcello Massimini

Research output: Contribution to journalArticle

61 Citations (Scopus)

Abstract

During non-rapid eye movement (NREM) sleep (stage N3), when consciousness fades, cortico-cortical interactions are impaired while neurons are still active and reactive. Why is this? We compared cortico-cortical evoked-potentials recorded during wakefulness and NREM by means of time-frequency analysis and phase-locking measures in 8 epileptic patients undergoing intra-cerebral stimulations/recordings for clinical evaluation. We observed that, while during wakefulness electrical stimulation triggers a chain of deterministic phase-locked activations in its cortical targets, during NREM the same input induces a slow wave associated with an OFF-period (suppression of power. >. 20. Hz), possibly reflecting a neuronal down-state. Crucially, after the OFF-period, cortical activity resumes to wakefulness-like levels, but the deterministic effects of the initial input are lost, as indicated by a sharp drop of phase-locked activity. These findings suggest that the intrinsic tendency of cortical neurons to fall into a down-state after a transient activation (i.e. bistability) prevents the emergence of stable patterns of causal interactions among cortical areas during NREM. Besides sleep, the same basic neurophysiological dynamics may play a role in pathological conditions in which thalamo-cortical information integration and consciousness are impaired in spite of preserved neuronal activity.

Original languageEnglish
Pages (from-to)105-113
Number of pages9
JournalNeuroImage
Volume112
DOIs
Publication statusPublished - May 5 2015

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Eye Movements
Wakefulness
Sleep
Consciousness
Neurons
Sleep Stages
Evoked Potentials
Electric Stimulation

Keywords

  • Causality
  • Consciousness
  • Down-state
  • Intracranial
  • Phase-locking

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Neurology
  • Medicine(all)

Cite this

Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. / Pigorini, Andrea; Sarasso, Simone; Proserpio, Paola; Szymanski, Caroline; Arnulfo, Gabriele; Casarotto, Silvia; Fecchio, Matteo; Rosanova, Mario; Mariotti, Maurizio; Lo Russo, Giorgio; Palva, J. Matias; Nobili, Lino; Massimini, Marcello.

In: NeuroImage, Vol. 112, 05.05.2015, p. 105-113.

Research output: Contribution to journalArticle

Pigorini, A, Sarasso, S, Proserpio, P, Szymanski, C, Arnulfo, G, Casarotto, S, Fecchio, M, Rosanova, M, Mariotti, M, Lo Russo, G, Palva, JM, Nobili, L & Massimini, M 2015, 'Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep', NeuroImage, vol. 112, pp. 105-113. https://doi.org/10.1016/j.neuroimage.2015.02.056
Pigorini A, Sarasso S, Proserpio P, Szymanski C, Arnulfo G, Casarotto S et al. Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. NeuroImage. 2015 May 5;112:105-113. https://doi.org/10.1016/j.neuroimage.2015.02.056
Pigorini, Andrea ; Sarasso, Simone ; Proserpio, Paola ; Szymanski, Caroline ; Arnulfo, Gabriele ; Casarotto, Silvia ; Fecchio, Matteo ; Rosanova, Mario ; Mariotti, Maurizio ; Lo Russo, Giorgio ; Palva, J. Matias ; Nobili, Lino ; Massimini, Marcello. / Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. In: NeuroImage. 2015 ; Vol. 112. pp. 105-113.
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