EEG-guided transcranial magnetic stimulation reveals rapid shifts in motor cortical excitability during the human sleep slow oscillation

TY - JOUR

T1 - EEG-guided transcranial magnetic stimulation reveals rapid shifts in motor cortical excitability during the human sleep slow oscillation

AU - Bergmann, Til O

AU - Mölle, Matthias

AU - Schmidt, Marlit A

AU - Lindner, Christoph

AU - Marshall, Lisa

AU - Born, Jan

AU - Siebner, Hartwig R

PY - 2012/1/4

Y1 - 2012/1/4

N2 - Evoked cortical responses do not follow a rigid input-output function but are dynamically shaped by intrinsic neural properties at the time of stimulation. Recent research has emphasized the role of oscillatory activity in determining cortical excitability. Here we employed EEG-guided transcranial magnetic stimulation (TMS) during non-rapid eye movement sleep to examine whether the spontaneous<1Hz neocortical slow oscillation (SO) is associated with corresponding fluctuations of evoked responses. Whereas the SO's alternating phases of global depolarization (up-state) and hyperpolarization (down-state) are clearly associated with fluctuations in spontaneous neuronal excitation, less isknownabout state-dependent shifts in neocortical excitability. In 12humanvolunteers, single-pulseTMSof the primary motor cortical hand area (M1 HAND) was triggered online by automatic detection of SO up-states and down-states in the EEG. Statedependent changes in cortical excitability were traced by simultaneously recording motor-evoked potentials (MEPs) and TMS-evoked EEG potentials (TEPs). Compared to wakefulness and regardless of SO state, sleep MEPs were smaller and delayed whereas sleep TEPs were fundamentally altered, closely resembling a spontaneous SO. However, both MEPs and TEPs were consistently larger when evoked during SO up-states than during down-states, and ampliudes within each SO state depended on the actual EEG potential at the time and site of stimulation. These results provide first-time evidence for a rapid state-dependent shift in neocortical excitability during a neuronal oscillation in the human brain. We further demonstrate that EEG-guided temporal neuronavigation is a powerful tool to investigate the phase-dependent effects of neuronal oscillations on perception, cognition, and motor control.

AB - Evoked cortical responses do not follow a rigid input-output function but are dynamically shaped by intrinsic neural properties at the time of stimulation. Recent research has emphasized the role of oscillatory activity in determining cortical excitability. Here we employed EEG-guided transcranial magnetic stimulation (TMS) during non-rapid eye movement sleep to examine whether the spontaneous<1Hz neocortical slow oscillation (SO) is associated with corresponding fluctuations of evoked responses. Whereas the SO's alternating phases of global depolarization (up-state) and hyperpolarization (down-state) are clearly associated with fluctuations in spontaneous neuronal excitation, less isknownabout state-dependent shifts in neocortical excitability. In 12humanvolunteers, single-pulseTMSof the primary motor cortical hand area (M1 HAND) was triggered online by automatic detection of SO up-states and down-states in the EEG. Statedependent changes in cortical excitability were traced by simultaneously recording motor-evoked potentials (MEPs) and TMS-evoked EEG potentials (TEPs). Compared to wakefulness and regardless of SO state, sleep MEPs were smaller and delayed whereas sleep TEPs were fundamentally altered, closely resembling a spontaneous SO. However, both MEPs and TEPs were consistently larger when evoked during SO up-states than during down-states, and ampliudes within each SO state depended on the actual EEG potential at the time and site of stimulation. These results provide first-time evidence for a rapid state-dependent shift in neocortical excitability during a neuronal oscillation in the human brain. We further demonstrate that EEG-guided temporal neuronavigation is a powerful tool to investigate the phase-dependent effects of neuronal oscillations on perception, cognition, and motor control.

KW - Adult

KW - Biological Clocks

KW - Electroencephalography

KW - Evoked Potentials

KW - Evoked Potentials, Motor

KW - Female

KW - Humans

KW - Male

KW - Motor Cortex

KW - Sleep

KW - Transcranial Magnetic Stimulation

KW - Young Adult

U2 - 10.1523/JNEUROSCI.4792-11.2012

DO - 10.1523/JNEUROSCI.4792-11.2012

M3 - Journal article

C2 - 22219286

SN - 0270-6474

VL - 32

SP - 243

EP - 253

JO - The Journal of neuroscience : the official journal of the Society for Neuroscience

JF - The Journal of neuroscience : the official journal of the Society for Neuroscience

IS - 1

ER -