Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum

Rhythmic brain activity is thought to reflect, and to help organize, spike activity in populations of neurons during on-going behavior. We report that during learning, a major transition occurs in task-related oscillatory activity in the ventromedial striatum, a striatal region related to motivation-dependent learning. Early on as rats learned a T-maze task, bursts of 70- to 90-Hz high-γ activity were prominent during T-maze runs, but these gradually receded as bursts of 15- to 28-Hz β-band activity became pronounced. Populations of simultaneously recorded neurons synchronized their spike firing similarly during both the high-γ–band and β-band bursts. Thus, the structure of spike firing was reorganized during learning in relation to different rhythms. Spiking was concentrated around the troughs of the β-oscillations for fast-spiking interneurons and around the peaks for projection neurons, indicating alternating periods of firing at different frequencies as learning progressed. Spike-field synchrony was primarily local during high-γ–bursts but was widespread during β-bursts. The learning-related shift in the probability of high-γ and β-bursting thus could reflect a transition from a mainly focal rhythmic inhibition during early phases of learning to a more distributed mode of rhythmic inhibition as learning continues and behavior becomes habitual. These dynamics could underlie changing functions of the ventromedial striatum during habit formation. More generally, our findings suggest that coordinated changes in the spatiotemporal relationships of local field potential oscillations and spike activity could be hallmarks of the learning process.