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Modeling regional changes in dynamic stability during sleep and wakefulness.

ABSTRACT: Global brain states are frequently placed within a unidimensional continuum by correlational studies, ranging from states of deep unconsciousness to ordinary wakefulness. An alternative is their multidimensional and mechanistic characterization in terms of different cognitive capacities, using computational models to reproduce the underlying neural dynamics. We explore this alternative by introducing a semi-empirical model linking regional activation and long-range functional connectivity in the different brain states visited during the natural wake-sleep cycle. Our model combines functional magnetic resonance imaging (fMRI) data, in vivo estimates of structural connectivity, and anatomically-informed priors to constrain the independent variation of regional activation. The best fit to empirical data was achieved using priors based on functionally coherent networks, with the resulting model parameters dividing the cortex into regions presenting opposite dynamical behavior. Frontoparietal regions approached a bifurcation from dynamics at a fixed point governed by noise, while sensorimotor regions approached a bifurcation from oscillatory dynamics. In agreement with human electrophysiological experiments, sleep onset induced subcortical deactivation with low correlation, which was subsequently reversed for deeper stages. Finally, we introduced periodic forcing of variable intensity to simulate external perturbations, and identified the key regions relevant for the recovery of wakefulness from deep sleep. Our model represents sleep as a state with diminished perceptual gating and the latent capacity for global accessibility that is required for rapid arousals. To the extent that the qualitative characterization of local dynamics is exhausted by the dichotomy between unstable and stable behavior, our work highlights how expanding the model parameter space can describe states of consciousness in terms of multiple dimensions with interpretations given by the choice of anatomically-informed priors.

SUBMITTER: Ipina IP

PROVIDER: S-EPMC7894985 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Modeling regional changes in dynamic stability during sleep and wakefulness.

Ipiña Ignacio Perez IP Kehoe Patricio Donnelly PD Kringelbach Morten M Laufs Helmut H Ibañez Agustín A Deco Gustavo G Perl Yonatan Sanz YS Tagliazucchi Enzo E

NeuroImage 20200411

Global brain states are frequently placed within a unidimensional continuum by correlational studies, ranging from states of deep unconsciousness to ordinary wakefulness. An alternative is their multidimensional and mechanistic characterization in terms of different cognitive capacities, using computational models to reproduce the underlying neural dynamics. We explore this alternative by introducing a semi-empirical model linking regional activation and long-range functional connectivity in the ...[more]

PMID: 32289454

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Project description:These studies address temporal changes in gene expression during spontaneous sleep and extended wakefulness in the mouse cerebral cortex, a neuronal target for processes that control sleep; and the hypothalamus, an important site of sleep regulatory processes. We determined these changes by comparing expression in sleeping animals sacrificed at different times during the lights on period, to that in animals sleep deprived and sacrificed at the same diurnal time. Experiment Overall Design: Experiments were performed on male mice (C57/BL6), 10 weeks of age Â±1 week. Animals were housed in a light/dark cycle of 12 hrs, in a pathogen free, temperature- and humidity-controlled room (22Â°C and 45-55%, respectively) with water available ad libitum. Food was accessible for 12 hrs only during the active period. Animals were subjected to 14 days of acclimatization during which a nighttime feeding pattern was established. This was done to avoid differential food intake between mice that were subsequently sleep deprived during the lights on period and those allowed to sleep. Mice were sacrificed following 3, 6, 9 and 12 hrs of total sleep deprivation (n=5 at each time point). Deprivation was initiated at lights-on, and performed through gentle handling. Sleeping animals, which were left undisturbed, were sacrificed at the same diurnal time points as sleep deprived mice (n=5 at each time point). An additional control group of mice were sacrificed at time zero, i.e., at the time of lights-on (n=5). All mice were behaviorally monitored using the AccuScan infrared monitoring system that detects movement when the mouse crosses electronic beams (Columbus Instruments). Mice were sacrificed by cervical dislocation. Brain sectioning was performed according to the mouse brain atlas of Franklin and Paxinos . The primary and secondary motor areas (M1 and M2) of the cerebral cortex and broadly defined regions and zones of the hypothalamus were sampled. RNA was isolated with Trizol (Invitrogen) and further purified using RNeasy columns (Qiagen) as per the manufacturer's instructions.

Dataset Information

Modeling regional changes in dynamic stability during sleep and wakefulness.

Publications

Modeling regional changes in dynamic stability during sleep and wakefulness.

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