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

• DOI: 10.1016/j.neuroimage.2015.02.056
• Publication Date: 2015-03-04T05:45:12Z
• Authors: 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
• Keywords: intracranial; Drug Resistant Epilepsy; causality; Consciousness; NREM SLEEP; Cognitive Neuroscience; Neuroscience (miscellaneous); BRAIN ACTIVITY; Neurosciences. Biological psychiatry. Neuropsychiatry; Unconsciousness; Cellular and Molecular Neuroscience; 03 medical and health sciences; 0302 clinical medicine; Developmental Neuroscience; Thalamus; NETWORK MECHANISMS; Neural Pathways; Down-state; Humans; VISUAL-CORTEX; Causality; Consciousness; Down-state; Intracranial; Phase-locking; Cerebral Cortex; Consciousness; Drug Resistant Epilepsy; Electric Stimulation; Electrodes, Implanted; Electroencephalography; Evoked Potentials; Humans; Neural Pathways; Neurons; Thalamus; Unconsciousness; Sleep; Cognitive Neuroscience; Neurology; Medicine (all); Evoked Potentials; IN-VIVO; Cerebral Cortex; Neurons; Causality; Consciousness; Down-state; Intracranial; Phase-locking; Neurosciences; NEOCORTICAL NEURONS; LESS-THAN-1 HZ; Electroencephalography; Intracranial; Electric Stimulation; Electrodes, Implanted; Causality; Neurology; SLOW-WAVE SLEEP; CORTICAL EFFECTIVE CONNECTIVITY; Phase-locking; phase-locking; Sleep; EYE-MOVEMENT SLEEP; RC321-571

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>20Hz), 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.