Brain State-Dependence of Coherent Oscillatory Activity along the Cortico-Striatal Axis of the Rat

Anatomically and physiologically, the cerebral cortex is tightly linked to the striatum, which is the head-end of cortico-basal ganglia circuits. However, the nature of cortico-striatal interactions is poorly understood. To assess the coupling between neuronal assemblies in the cerebral cortex and the striatum, we recorded single unit activity (SUA) and local field potentials (LFP) in healthy, halothane-anesthetized rats. To this end, we employed a bihemispherical multi-site approach with eight microelectrodes in the striatum together with simultaneous recordings of electro-corticographic activity (EcoG). EcoG served as the primary indicator of brain state. During halothane anesthesia, cortical field potentials are generally dominated by oscillatory activity in the delta range (2–5Hz). The fine structure of these delta oscillations revealed an alternating pattern of two different activation states. Phases with a more irregular high-amplitude slow wave activity („high-delta“) were interrupted by episodes dominated by regular, clockwork-like delta oscillations with low amplitudes („low-delta“). In addition to the spectral peak representing the slow wave activity, both cortical and striatal LFPs displayed a spectral peak in the upper gamma-frequency (range 45–75Hz). These high-frequency oscillations consistently showed a frequency shift coinciding at the transition from high-delta to low-delta episodes. Spontaneous activity in the cortex and striatum was significantly coherent in the delta range during high-delta episodes, encompassing both hemispheres. Cortico-striatal coherence in the delta frequency range was significantly lower during epochs of low δ. Interestingly, beta-band coherence (15–30Hz) between cortex and striatum was low, while coherence in the upper gamma band was significantly increased, irrespective of the prevailing cortical activation state. We found that during high-delta episodes, striatal single unit activity is synchronized even interhemispherically and shows a strong oscillatory modulation in the delta frequency range. In contrast to this, striatal spiking is desynchronized and tonic during low-delta epochs. Taken together, our results suggest that the cortex exerts a powerful influence on neuronal activity in the striatum. We propose that dynamic coupling and de-coupling of cortical and striatal neuronal assemblies is an important mechanism in the functional organization along the cortico-striatal axis.