Abstract
To understand how arousal state impacts cerebral hemodynamics and neurovascular coupling, we monitored neural activity, behavior, and hemodynamic signals in un-anesthetized, head-fixed mice. Mice frequently fell asleep during imaging, and these sleep events were interspersed with periods of wake. During both NREM and REM sleep, mice showed large increases in cerebral blood volume ([HbT]) and arteriole diameter relative to the awake state, two to five times larger than those evoked by sensory stimulation. During NREM, the amplitude of bilateral low-frequency oscillations in [HbT] increased markedly, and coherency between neural activity and hemodynamic signals was higher than the awake resting and REM states. Bilateral correlations in neural activity and [HbT] were highest during NREM, and lowest in the awake state. Hemodynamic signals in the cortex are strongly modulated by arousal state, and changes during sleep are substantially larger than sensory-evoked responses.
Highlights
Sleep is a ubiquitous state in animals (Anafi et al, 2019) that is controlled by an ensemble of nuclei and their brain-wide interactions (Pace-Schott and Hobson, 2002; Sakai, 2019; Saper et al, 2010)
We tracked whisker position (Kleinfeld and Deschênes, 2011; O’Connor et al, 2010), body movement, and nuchal muscle EMG (Datta and MacLean, 2007; Veasey et al, 2000), as spontaneous ‘fidgeting’ behaviors drive a substantial portion of neural activity and hemodynamic signals in the awake mouse (Drew et al, 2019; Musall et al, 2019; Stringer et al, 2019; Winder et al, 2017), and these measures can be used to determine the arousal state of the animal
It has previously been shown that neurovascular coupling is similar across awake arousal states (Winder et al, 2017) and that both spontaneous and sensory-evoked hemodynamics are most strongly correlated with gamma band power and multi-unit average (MUA – a measure of local spiking activity) in the absence of overt stimulation (Mateo et al, 2017; Schölvinck et al, 2010; Shmuel and Leopold, 2008; Winder et al, 2017). To see if these relationships held true for neurovascular coupling in other arousal states, we looked at the relationship between the power in different frequency bands of the local field potential (LFP) or multi-unit activity and ∆[HbT] during periods of contiguous NREM and REM sleep
Summary
Sleep is a ubiquitous state in animals (Anafi et al, 2019) that is controlled by an ensemble of nuclei and their brain-wide interactions (Pace-Schott and Hobson, 2002; Sakai, 2019; Saper et al, 2010). In mammals (Cirelli, 2009), sleep is broadly comprised of two stages: non-rapid eye movement (NREM or slow-wave sleep) and rapid eye movement (REM or paradoxical sleep) (Weber and Dan, 2016). Each of these states is associated with distinct patterns of electrical activity in the brain. During REM sleep, gamma band power (nominally 30-100Hz) is elevated in the cortex (Cantero et al., 2004; Van Quyen et al, 2010). REM sleep is associated with a marked increase in power in the theta band (nominally 4-10 Hz) in rodents (Montgomery et al, 2008; Sullivan et al, 2014)
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