Functional integration across a gradient of corticostriatal channels controls UP state transitions in the dorsal striatum

Abstract

Coordinated near-threshold depolarized states in cortical and striatal neurons may contribute to form functionally segregated channels of information processing. Recent anatomical studies have identified pathways that could support spiraling interactions across corticostriatal channels, but a functional outcome of such spiraling remains to be identified. Here, we examined whether plateau depolarizations (UP states) in striatal neurons relate better to active epochs in local field potentials recorded from closely related cortical areas than to those recorded in less-related cortical areas. Our results show that, in anesthetized rats, the coordination between cortical areas and striatal regions obeys a mediolateral gradient and keeps track of slow wave trajectory across the neocortex. Moreover, activity in one cortical area induced phase advances in UP state onset and phase delays in UP state termination in nonmatching striatal regions, reflecting the existence of functional connections that could encode large-scale interactions between corticostriatal channels as subthreshold influences on striatal projection neurons.basal ganglia ͉ cerebral cortex ͉ in vivo intracellular recording ͉ medium spiny neuron ͉ slow waves T he corticostriatal network shows different large-scale dynamics during the wake-sleep cycle. During slow-wave sleep and anesthesia, alternating episodes of strong synaptic activity and membrane potential (V m ) depolarization (UP states) and periods of almost complete silence (DOWN states) spread coordinately across the neocortex every second, bringing up distinctive local field potential (LFP) modulations (1, 2). Subthreshold activity, evidenced either as waves of depolarization over restricted cortical areas or sustained depolarizations, is more intricate during the wake period (2-4). The depolarized states of wakefulness and sleep are an emergent feature of cortical networks (5) and allow online information processing and the reactivation of memory traces during slow-wave sleep (6). Striatal medium spiny neurons (MSNs) also show different depolarized states, the time course of which is linked to cortical activity (7-11), and replay experience-related activity in consonance with the cortex during slow wave sleep (12, 13). Thus, coordinated depolarized states in cortical and striatal neurons support the online and offline operation of corticostriatal circuits.It has long been thought that corticostriatal pathways are organized in functionally segregated channels (14,15). This view posits that functional integration occurs ''within, rather than between, corticostriatal circuits'' (14). However, recent anatomical studies suggest that diffuse corticostriatal projections and multisynaptic circuits linking nonreciprocal cortical and striatal areas could allow interactions across parallel channels (16)(17)(18)(19)(20). With the aim of unveiling functional connections between supposedly segregated corticostriatal channels, we examined the timing of UP states in MSNs located in three distinct striatal regi...

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