Oscillatory rhythms in different frequency ranges mark different behavioral states and are thought to provide distinct temporal windows that coherently bind cooperating neuronal assemblies. However, the rhythms in different bands can also interact with each other, suggesting the possibility of higher-order representations of brain states by such rhythmic activity. To explore this possibility, we analyzed local field potential oscillations recorded simultaneously from the striatum and the hippocampus. As rats performed a task requiring active navigation and decision making, the amplitudes of multiple high-frequency oscillations were dynamically modulated in task-dependent patterns by the phase of cooccurring theta-band oscillations both within and across these structures, particularly during decision-making behavioral epochs. Moreover, the modulation patterns uncovered distinctions among both high-and low-frequency subbands. Cross-frequency coupling of multiple neuronal rhythms could be a general mechanism used by the brain to perform networklevel dynamical computations underlying voluntary behavior.amplitude modulation ͉ gamma ͉ theta O scillations in neural population voltage activity are universal phenomena (1). Among brain rhythms, theta oscillations in local field potentials (LFPs) recorded in the hippocampus are prominent during active behaviors (2-5), and these have long been intensively analyzed in the rodent in relation to spatial navigation (6), memory (7), and sleep (8). Theta-band rhythms (4-12 Hz) are now known to occur in other cortical (9-12) and subcortical (12-15) regions, however, including the striatum (14-17), studied here. Gamma oscillations (30-100 Hz) have also received special attention because of their proposed role in functions such as sensory binding (18), selective attention (19-21), transient neuronal assembly formation (22), and information transmission and storage (23-25). The existence of physiologically meaningful neocortical oscillations at even higher frequencies, above the traditional gamma range, has been reported as well (10,(26)(27)(28). In rodents, for example, brief sharp-wave associated ripples (120-200 Hz) appear in the hippocampal formation during slow wave sleep, immobility and consummatory behavior, characteristically in the absence of theta waves (2, 29).The oscillatory activities conventionally assigned to different frequency bands are not completely independent (2-4, 9, 10, 30). In one type of interaction, the phase of low-frequency rhythms modulates the amplitude of higher-frequency oscillations (9, 10, 30). For example, theta phase is known to modulate gamma power in rodent hippocampal and cortical circuits (2-4, 31), and the phase of theta rhythms recorded in the human neocortex can modulate wide-band (60-200 Hz) high-frequency oscillations (10). Such theta-gamma nesting is thought to play a role in sequential memory organization and maintenance of working memory, and more generally in ''phase coding' ' (25, 31). Based on evidence suggesting that theta rhythms i...

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. Both regions exhibited typical beta-band suppression during movement and postmovement rebounds of up to 3 s as viewed in data averaged across trials, but single-trial analysis showed that most beta oscillations occurred in brief bursts, commonly 90-115 ms long. In the motor cortex, the burst probabilities peaked following the last movement, but in the striatum, the burst probabilities peaked at task end, after reward, and continued through the postperformance period. Thus, what appear to be extended periods of postperformance beta-band synchronization reflect primarily the modulated densities of short bursts of synchrony occurring in region-specific and task-time-specific patterns. We suggest that these short-time-scale events likely underlie the functions of most beta-band activity, so that prolongation of these beta episodes, as observed in Parkinson's disease, could produce deleterious network-level signaling.basal ganglia | local field potentials | beta band | sequential movement | synchronization O scillations of brain activity in the beta band (13-30 Hz) have been implicated in sensorimotor control and integration (1-5) and are pathologically synchronized and exaggerated in Parkinson's disease (6-11). Although reports have published examples of very brief (<150 ms) bursts of beta-band oscillation (12-15), 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.To address the apparent discrepancy in time scales between the single-trial results and the trial-averaged results, we analyzed the relationship of brief beta bursts as viewed at a single-trial level to the substantially slower variations in trial-averaged power that are conventionally referred to as periods of "synchronization" or "desynchronization" of beta-band activity. We examined betaband activity recorded in two regions of prime clinical interest, the motor-premotor regions of the neocortex and the striatum, in macaque monkeys performing well-learned movement sequences. Our findings suggest that these regions exhibit different peak times of synchronization of beta bursting during...

The striatum and hippocampus are conventionally viewed as complementary learning and memory systems, with the hippocampus specialized for fact-based episodic memory and the striatum for procedural learning and memory. Here we directly tested whether these two systems exhibit independent or coordinated activity patterns during procedural learning. We trained rats on a conditional T-maze task requiring navigational and cue-based associative learning. We recorded local field potential (LFP) activity with tetrodes chronically implanted in the caudoputamen and the CA1 field of the dorsal hippocampus during 6 -25 days of training. We show that simultaneously recorded striatal and hippocampal theta rhythms are modulated differently as the rats learned to perform the T-maze task but nevertheless become highly coherent during the choice period of the maze runs in rats that successfully learned the task. Moreover, in the rats that acquired the task, the phase of the striatal-hippocampal theta coherence was modified toward a consistent antiphase relationship, and these changes occurred in proportion to the levels of learning achieved. We suggest that rhythmic oscillations, including theta-band activity, could influence not only neural processing in cortico-basal ganglia circuits but also dynamic interactions between basal ganglia-based and hippocampus-based forebrain circuits during the acquisition and performance of learned behaviors. Experience-dependent changes in coordination of oscillatory activity across brain structures thus may parallel the well known plasticity of spike activity that occurs as a function of experience.basal ganglia ͉ hippocampus ͉ local field potential ͉ oscillations ͉ striatum T he striatum and the hippocampus are both forebrain structures implicated in the learning and memory of behavioral sequences, but behavioral sequences of different sorts. The striatum, as part of basal ganglia circuitry, is associated with learning sequences of actions that make up goal-directed procedures and habits (1-4). The hippocampus and adjoining cortical structures are recognized as critical for encoding and storing sequences on the basis of episodic, context-cued events (5-8). Lesion studies have dissociated striatum-dependent and hippocampus-dependent forms of learning and memory (9-11), supporting the view that these systems work independently or even competitively. In humans, there is evidence that one system can substitute for another (12). Other evidence, however, suggests that ''hippocampal'' deficits can follow damage in regions of the dorsal striatum interconnected with hippocampal/limbic circuits (13,14). Furthermore, part of the ventral striatum receives direct projections from the hippocampus.Rhythmic activity in the theta range (Ϸ7-14 Hz in the rodent) has been proposed to be crucial for mnemonic coding in the hippocampus and related limbic structures. Pathways interconnecting the hippocampus and neocortex are thought to use these rhythms for transferring and coordinating neural representations in cort...