Abstract
The basal forebrain delivers extensive axonal projections to the cortical mantle regulating brain states and cognitive processing. Recent evidence has established the basal forebrain as a subcortical node of the default mode network that directionally influences cortical dynamics trough gamma oscillations, yet their synaptic origin has not been established. Here, we used optogenetic stimulation and in vivo recordings of transgenic mice to show that somatostatin neurons exert an anatomically specialized role in the coordination of subcortical gamma oscillations of the rostral basal forebrain. Indeed, the spike timing of somatostatin cells was tightly correlated with gamma oscillations in the ventral pallidum, but not in the medial septum. Consequently, optogenetic inactivation of somatostatin neurons selectively disrupted the amplitude and coupling of gamma oscillations only in the ventral pallidum. Moreover, photosupression of somatostatin cells produced specific behavioral interferences, with the ventral pallidum regulating locomotor speed and the medial septum modulating spatial working memory. Altogether, these data suggest that basal forebrain somatostatin cells can selectively synchronize local neuronal networks in the gamma band directly impinging on cortical dynamics and behavioral performance. This further supports the role of the basal forebrain as a subcortical switch commanding transitions between internally and externally oriented brain states.
Highlights
The mammalian basal forebrain is a collection of subcortical structures which provides extensive axonal projections to the entire cerebral cortex[1,2] playing central roles in regulating cognition, movement, brain states[3,4,5,6,7,8] and damage to the basal forebrain is critical in major neurological disorders[9,10,11,12]
Somatostatin cells were identified in vivo by conspicuous inhibition of their spiking activity during photostimulation in two domains of the rostral basal forebrain: the ventral pallidum (VP) and medial septum (MS) (Fig. 1C, Supplementary Table 1)
Excited and non-responsive cells belong to several different cell types, yet we operationally defined them as somatostatin-negative cells in order to simplify analysis (Fig. 1C)
Summary
The mammalian basal forebrain is a collection of subcortical structures which provides extensive axonal projections to the entire cerebral cortex[1,2] playing central roles in regulating cognition, movement, brain states[3,4,5,6,7,8] and damage to the basal forebrain is critical in major neurological disorders[9,10,11,12]. Recent evidence has demonstrated that basal forebrain gamma oscillations are enhanced during quiet wakefulness and self-grooming, which are internally-oriented states characteristic of the default mode network[24]. This stands in contrast with the canonical role of the basal forebrain in promoting active sensory processing and goal-directed behavior. We have recently shown how somatostatin cells can gate basal forebrain synaptic output and regulate prefrontal cortex dynamics, with specific effects on gamma oscillations[26]. This posits somatostatin cells as a plausible candidate for the coordination of basal forebrain gamma oscillations. Our study further confirms the role of the basal forebrain as a dynamic switch between internally and externally oriented brain states
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