TY - JOUR
T1 - Impedance Rhythms in Human Limbic System
AU - Mivalt, Filip
AU - Kremen, Vaclav
AU - Sladky, Vladimir
AU - Cui, Jie
AU - Gregg, Nicholas M.
AU - Balzekas, Irena
AU - Marks, Victoria
AU - St Louis, Erik K.
AU - Croarkin, Paul
AU - Lundstrom, Brian Nils
AU - Nelson, Noelle
AU - Kim, Jiwon
AU - Hermes, Dora
AU - Messina, Steven
AU - Worrell, Samuel
AU - Richner, Thomas
AU - Brinkmann, Benjamin H.
AU - Denison, Timothy
AU - Miller, Kai J.
AU - Van Gompel, Jamie
AU - Stead, Matthew
AU - Worrell, Gregory A.
N1 - Publisher Copyright:
© 2023 the authors.
PY - 2023/9/27
Y1 - 2023/9/27
N2 - The impedance is a fundamental electrical property of brain tissue, playing a crucial role in shaping the characteristics of local field potentials, the extent of ephaptic coupling, and the volume of tissue activated by externally applied electrical brain stimulation. We tracked brain impedance, sleep–wake behavioral state, and epileptiform activity in five people with epilepsy living in their natural environment using an investigational device. The study identified impedance oscillations that span hours to weeks in the amygdala, hippocampus, and anterior nucleus thalamus. The impedance in these limbic brain regions exhibit multiscale cycles with ultradian (;1.5–1.7 h), circadian (;21.6–26.4 h), and infradian (;20–33 d) periods. The ultradian and circadian period cycles are driven by sleep–wake state transitions between wakefulness, nonrapid eye movement (NREM) sleep, and rapid eye movement (REM) sleep. Limbic brain tissue impedance reaches a minimum value in NREM sleep, intermediate values in REM sleep, and rises through the day during wakefulness, reaching a maximum in the early evening before sleep onset. Infradian (;20–33 d) impedance cycles were not associated with a distinct behavioral correlate. Brain tissue impedance is known to strongly depend on the extracellular space (ECS) volume, and the findings reported here are consistent with sleep–wake–dependent ECS volume changes recently observed in the rodent cortex related to the brain glymphatic system. We hypothesize that human limbic brain ECS changes during sleep–wake state transitions underlie the observed multiscale impedance cycles. Impedance is a simple electrophysiological biomarker that could prove useful for tracking ECS dynamics in human health, disease, and therapy.
AB - The impedance is a fundamental electrical property of brain tissue, playing a crucial role in shaping the characteristics of local field potentials, the extent of ephaptic coupling, and the volume of tissue activated by externally applied electrical brain stimulation. We tracked brain impedance, sleep–wake behavioral state, and epileptiform activity in five people with epilepsy living in their natural environment using an investigational device. The study identified impedance oscillations that span hours to weeks in the amygdala, hippocampus, and anterior nucleus thalamus. The impedance in these limbic brain regions exhibit multiscale cycles with ultradian (;1.5–1.7 h), circadian (;21.6–26.4 h), and infradian (;20–33 d) periods. The ultradian and circadian period cycles are driven by sleep–wake state transitions between wakefulness, nonrapid eye movement (NREM) sleep, and rapid eye movement (REM) sleep. Limbic brain tissue impedance reaches a minimum value in NREM sleep, intermediate values in REM sleep, and rises through the day during wakefulness, reaching a maximum in the early evening before sleep onset. Infradian (;20–33 d) impedance cycles were not associated with a distinct behavioral correlate. Brain tissue impedance is known to strongly depend on the extracellular space (ECS) volume, and the findings reported here are consistent with sleep–wake–dependent ECS volume changes recently observed in the rodent cortex related to the brain glymphatic system. We hypothesize that human limbic brain ECS changes during sleep–wake state transitions underlie the observed multiscale impedance cycles. Impedance is a simple electrophysiological biomarker that could prove useful for tracking ECS dynamics in human health, disease, and therapy.
KW - brain impedance
KW - circadian rhythm
KW - extracellular space
KW - implantable neural stimulators
KW - long-term data
KW - sleep
UR - http://www.scopus.com/inward/record.url?scp=85173766612&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85173766612&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.0241-23.2023
DO - 10.1523/JNEUROSCI.0241-23.2023
M3 - Article
C2 - 37620157
AN - SCOPUS:85173766612
SN - 0270-6474
VL - 43
SP - 6653
EP - 6666
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 39
ER -