Interindividual differences in memory system local field potential activity predict behavioral strategy on a...

Individuals can use diverse behavioral strategies to navigate their environment including hippocampal-dependent place strategies reliant upon cognitive maps and striatal-dependent response strategies reliant upon egocentric body turns. The existence of multiple memory systems appears to facilitate successful navigation across a wide range of environmental and physiological conditions. The mechanisms by which these systems interact to ultimately generate a unitary behavioral response, however, remain unclear. We trained 20 male, Sprague-Dawley rats on a dual-solution T-maze while simultaneously recording local field potentials that were targeted to the dorsolateral striatum and dorsal hippocampus. Eight rats spontaneously exhibited a place strategy while the remaining 12 rats exhibited a response strategy. Interindividual differences in behavioral strategy were associated with distinct patterns of LFP activity between the dorsolateral striatum and dorsal hippocampus. Specifically, striatal-hippocampal theta activity was in-phase in response rats and out-of-phase in place rats and response rats exhibited elevated striatal-hippocampal coherence across a wide range of frequency bands. These contrasting striatal-hippocampal activity regimes were (a) present during both maze-learning and a 30 min premaze habituation period and (b) could be used to train support vector machines to reliably predict behavioral strategy. Distinct patterns of neuronal activity across multiple memory systems, therefore, appear to bias behavioral strategy selection and thereby contribute to interindividual differences in behavior.