Disruption of the two‐state membrane potential of striatal neurones during cortical desynchronisation in anaesthetised rats

Abstract

Most striatal medium spiny neurones (MSNs) display 'up states' in anaesthetised animals. Up states are perceived as temporal gates invoked by afferent input, during which MSNs are in a 'ready-to-fire' condition (Wilson, 1993). During up states the membrane potential (V m ) of MSNs displays high-frequency low-amplitude modulations, presumably of synaptic origin, that can eventually provoke action potential firing (Stern et al. 1997(Stern et al. , 1998. There is convincing evidence supporting that up states are driven by excitatory input from the cerebral cortex and thalamus. First, decortication forces the V m of MSN neurones into a continuous down state (Wilson, 1993). Second, MSNs exhibit a persistent down state in acute brain slices, but display two-state transitions in chronic organotypic cortex-striatum cocultures (Plenz & Aertsen, 1996). Third, in anaesthetised rats, corticostriatal neurones exhibit two-state V m fluctuations that closely resemble those occurring in MSNs (Stern et al. 1997). In the absence of excitatory input, potassium inwardly rectifying currents hold the V m of MSNs close to the potassium equilibrium potential (reviewed by Wilson, 1993;Nicola et al. 2000).Recent findings revealing a strong correlation between a slow (~1 Hz) high-amplitude rhythm in the frontal electroencephalogram (EEG) and V m fluctuations in striatal MSNs (Mahon et al. 2001;Tseng et al. 2001), further indicate that up states are induced by strongly synchronous afferent input. The EEG waveform, which reflects population activity of cortical neurones, exhibits disparate shapes depending on vigilance states, sensory input and level of anaesthesia (reviewed by Steriade, 2000). The ~1 Hz EEG oscillation is produced by a widespread synchronisation of the thalamocortical network that is typical of slow wave In anaesthetised animals, the very negative resting membrane potential of striatal spiny neurones (down state) is interrupted periodically by depolarising plateaux (up states) which are probably driven by excitatory input. In the absence of active synaptic input, as occurs in vitro, potassium currents hold the membrane potential of striatal spiny neurones in the down state. Because striatal spiny neurones fire action potentials only during the up state, these plateau depolarisations have been perceived as enabling events that allow information processing through cerebral cortex-basal ganglia circuits. Recent studies have demonstrated that the robust membrane potential fluctuation of spiny neurones is strongly correlated to the slow electroencephalographic rhythms that are typical of slow wave sleep and anaesthesia. To further understand the impact of cortical activity states on striatal function, we studied the membrane potential of striatal neurones during cortical desynchronised states. Simultaneous in vivo recordings of striatal neurones and the electrocorticogram in urethane-anaesthetised rats revealed that rhythmic alternation between up and down states was disrupted during episodes of spontaneous or induced cortical ...

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

“…They reinforce novel views of slow waves as a global process spreading beyond the thalamocortical system in expanding loops (9,46,47). They also strengthen the view that the dynamics of depolarizing states in the striatum, which lacks an intrinsic excitatory driving force, depend highly on the dynamics of cortical networks (8)(9)(10)(11).…”

“…All methods were similar to those described in Kasanetz et al (9,11) and are described in more detail in the SI Text. Adult male Sprague-Dawley rats (n ϭ 46) were used and cared for in accordance with local institutional regulations on the use of laboratory animals (Servicio Nacional de Sanidad y Calidad Agroalimentaria, RS 617/ 2002, Argentina).…”

“…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)(8)(9)(10)(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.…”

Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat StriatumIn Vivo

“…The cortical field potential exhibited two spontaneous states in rats anesthetized with urethane: a dominant state characterized by slow waves (SWs) of large amplitude at ϳ1 Hz, called here SWϩ state, and periods of absence of slow waves (called here SWϪ state) (Tseng et al, 2001;Kasanetz et al, 2002). As observed by Kasanetz et al (2002), a tail pinch always disrupted the slowwave activity for a variable duration (Fig.…”

“…During cortical slow waves in anesthetized rats, the synchronous activity of corticostriatal neurons actually shapes the membrane potential of MSNs (Mahon et al, 2001;Tseng et al, 2001). These oscillations are disrupted by cortical desynchronization (Mahon et al, 2001;Kasanetz et al, 2002).…”