Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task

Abstract

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...

Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task

“…A relation between behavioral learning and patterns of striatalhippocampal theta coherence has been suggested because high levels of cross-structure theta coherence were found in rats that learned the T-maze task used here but not in rats that failed to learn the task (14). In our analysis, we found clear examples of correlations between the phase-amplitude modulation and learning scores (Fig.…”

“…The presence of phase-amplitude coupling during the midrun period suggested that the coupling might be related to the presence of heightened coherence between the striatal and the hippocampal rhythms, which also tends to occur during this epoch (14). As shown in Fig.…”

“…5C, see also ref. 14). By contrast, it was the low-frequency striatal theta band (3-8 Hz) that modulated the striatal 80-to 120-Hz oscillations, frequencies at which the striatal and hippocampal theta rhythms were less coherent (Fig.…”

“…We analyzed the LFP oscillatory activity recorded in the dorsal caudoputamen and the CA1 field of the dorsal hippocampus as rats (n ϭ 6) navigated a T-maze in which they turned right or left in response to auditory instruction cues indicating which of the 2 end arms was baited with chocolate (14,15) (Fig. 1A).…”

“…Among brain rhythms, theta oscillations in local field potentials (LFPs) recorded in the hippocampus are prominent during active behaviors (2)(3)(4)(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)(5)(6)(7)(8)(9)(10)(11)(12) are now known to occur in other cortical (9)(10)(11)(12) and subcortical (12)(13)(14)(15) regions, however, including the striatum (14)(15)(16)(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)(20)(21), transient neuronal assembly formation (22), and information transmission and storage (23)(24)(25).…”