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

Abstract

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 taskrelated 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. Spikefield 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.basal ganglia | beta rhythm | gamma rhythm | neural circuit reorganization | network dynamics R hythmic field-potential activities in particular frequency bands are known to characterize different on-going behavioral states: low frequency (α-band) rhythms distinguish sleep from waking, higher (β-band) frequencies distinguish movement from rest, and high (γ-band) frequencies distinguish attentive from inattentive states. These activities in different frequency bands can be coordinated by phase or amplitude coupling, and especially when synchronous, such oscillations are proposed to represent on-line processing modes that can facilitate interactions across brain regions and binding of neural ensembles, and that can provide a temporal structure for neural activity related to memory processing and the creation or maintenance of brain states (1-4).It is well documented that spike activity can be organized relative to particular rhythms detected in local field potentials (LFPs), and can even be dependent on such rhythms (5, 6), yet little is known about how such oscillatory activity changes across learning, a dynamic state in which spike activity is reorganized. We explored the possibility that changes in the oscillatory structure of a network might reorganize local circuit activity as a behavior is learned and stamped in as habitual. We took as our starting point that learning-relate...

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

“…Numerous studies in mammals have shown that basal ganglia neurons change their task-related firing during learning (52,53), and that such changes can precede changes in cortical activity and behavior (54)(55)(56). Here, we extend these findings by directly demonstrating that the basal ganglia are required for specific, task-related cortical firing patterns that are critical for song motor plasticity.…”

Basal forebrain contributes to default mode network regulation

“…The relation between locomotion and BF gamma activity in the home cage is likely unrelated to the reported findings in the hippocampus and is probably a consequence of reduced gamma oscillations at very low movement-sensor levels that were not observed in the arena. Robust gamma oscillations have indeed been reported previously in the BF (31) as well as in nearby brain structures, notably including the VS, where other authors have observed gamma oscillations with a peak frequency around 50 Hz, similar to our study (62,64,(67)(68)(69)(70). However, VS 50-Hz gamma oscillation was observed during radial arm maze navigation (67,68) or rewarded decision making (63,64) and not during a "task-off," home-cage condition as in our study.…”

Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks

“…Here we focused on the postperformance period, following up on studies of the rodent basal ganglia in which accentuated postperformance beta bursting was documented (15,26). Numerous studies in nonhuman primates have demonstrated significant task-related effects in the low beta band (4,5,(27)(28)(29), but except for the elegant studies of Tan and colleagues (30,31), oscillation during the postmovement period has not been analyzed in detail.…”

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Studies of neural oscillations in the beta band (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) have demonstrated modulations in beta-band power associated with sensory and motor events on time scales of 1 s or more, and have shown that these are exaggerated in Parkinson's disease. However, even early reports of beta activity noted extremely fleeting episodes of beta-band oscillation lasting <150 ms. Because the interpretation of possible functions for beta-band oscillations depends strongly on the time scale over which they occur, and because of these oscillations' potential importance in Parkinson's disease and related disorders, we analyzed in detail the distributions of duration and power for beta-band activity in a large dataset recorded in the striatum and motor-premotor cortex of macaque monkeys performing reaching tasks.

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“…basal ganglia | local field potentials | beta band | sequential movement | synchronization O scillations of brain activity in the beta band (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) Hz) have been implicated in sensorimotor control and integration (1)(2)(3)(4)(5) and are pathologically synchronized and exaggerated in Parkinson's disease (6)(7)(8)(9)(10)(11). Although reports have published examples of very brief (<150 ms) bursts of beta-band oscillation (12)(13)(14)(15), the analysis of beta-band activity has focused primarily on data averaged over trials, which show variations in average beta-band power occurring on a time scale of seconds.…”