Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally

Abstract

Slow waves (SWs) are globally propagating, low-frequency (0.5- to 4-Hz) oscillations that are prominent during sleep and anesthesia. SWs are essential to neural plasticity and memory. However, much remains unknown about the mechanisms coordinating SW propagation at the macroscale. To assess SWs in the context of macroscale networks, we recorded cortical activity in awake and ketamine/xylazine-anesthetized mice using widefield optical imaging with fluorescent calcium indicator GCaMP6f. We demonstrate that unilateral somatosensory stimulation evokes bilateral waves that travel across the cortex with state-dependent trajectories. Under anesthesia, we observe that rhythmic stimuli elicit globally resonant, front-to-back propagating SWs. Finally, photothrombotic lesions of S1 show that somatosensory-evoked global SWs depend on bilateral recruitment of homotopic primary somatosensory cortices. Specifically, unilateral lesions of S1 disrupt somatosensory-evoked global SW initiation from either hemisphere, while spontaneous SWs are largely unchanged. These results show that evoked SWs may be triggered by bilateral activation of specific, homotopically connected cortical networks.

Cortical mapping of sensory responses reveals strong brain-state dependence of the late component

“…Therefore, we sought to investigate these features in the spatiotemporal propagation of the evoked response. Consistent with previous studies 1,6 , monolateral whisker stimulation evoked a distributed cortical response with brain state dependency. We analyzed seventeen representative cortical regions per hemisphere to reconstruct topographic response maps based on the mean response.…”

Identifying the distinct spectral dynamics of laminar-specific interhemispheric connectivity with bilateral line-scanning fMRI

“…[90][91][92] Moreover, the reduced ultra-slow oscillation at contralateral FP-S1 upon stimulation is consistent with previous calcium imaging study to measure the low-frequency global signal fluctuation with periodic stimulation. 42 However, the ipsilateral ultra-slow oscillation was not suppressed by peripheral stimulation in our observation (Figures 2(e), 3(d) and (e)). Also, the spectral power plot between evoked 0.05 Hz responses in contralateral FP-S1 and layer-specific ultra-slow oscillation in the ipsilateral FP-S1 shows no linear correlation (Figure S7).…”

“…40,41 Also, by genetically encoded Ca 2þ indicator (GCaMP)-based recording of the Ca 2þ signal fluctuation across two hemispheres, the bilateral global neuronal oscillatory signal at the low frequency can be regulated by the evoked neuronal signals, presenting a more complex regulatory mechanism underlying interhemispheric FC detected by rs-fMRI. 42 High field fMRI reveals laminar-specific responses to either bottom-up or top-down tasks, indicating neuronal circuit-based laminar specificity in human [43][44][45][46][47] and animal brains. [48][49][50][51][52][53] In contrast, the laminarspecific fMRI signal correlation/coherence patterns, which can illustrate underlying neuronal circuits for FC, have not been thoroughly investigated using conventional fMRI methods given the limited spatiotemporal resolution.…”

“…40,41 Also, by genetically encoded Ca 2+ indicator (GCaMP)-based recording of the Ca 2+ signal fluctuation across two hemispheres, the bilateral global neuronal oscillatory signal at the low frequency can be regulated by the evoked neuronal signals, presenting a more complex regulatory mechanism underlying interhemispheric FC detected by rs-fMRI. 42…”

Mapping brain state-dependent sensory responses across the mouse cortex

“… 2 The propagation from sensory regions to the entire dorsal cortex was then explored by several groups using wide-field imaging. 1 , 5 , 6 , 7 , 8 Notably, a strong dependence of the evoked spatiotemporal dynamics on the brain state was demonstrated by comparing wakefulness and anesthesia. 9 , 10 , 11 , 12 This is in line with a significant body of evidence positing that anesthesia is primarily linked to the breakdown of long-range projections between cortical areas, leading to the impairment of cortical information integration.…”