Local or Not Local: Investigating the Nature of Striatal Theta Oscillations in Behaving Rats

In the cortex and hippocampus, neuronal oscillations of different frequencies can be observed in local field potentials (LFPs). LFPs oscillations in the theta band (6-10 Hz) have also been observed in the dorsolateral striatum (DLS) of rodents, mostly during locomotion, and have been proposed to mediate behaviorally-relevant interactions between striatum and cortex (or between striatum and hippocampus). However, it is unclear if these theta oscillations are generated in the striatum. To address this issue, we recorded LFPs and spiking activity in the DLS of rats performing a running sequence on a motorized treadmill. We observed an increase in rhythmical activity of the LFP in the theta-band during run compared to rest periods. However, several observations suggest that these oscillations are mainly generated outside of the striatum. First, theta oscillations disappeared when LFPs were rereferenced against a striatal recording electrode and the imaginary coherence between LFPs recorded at different locations within the striatum was null. Second, 8% of the recorded neurons had their spiking activity phase-locked to the theta rhythm. Third, Granger causality analyses between LFPs simultaneously recorded in the cortex and the striatum revealed that the interdependence between these two signals in the theta range was mostly accounted for by a common external source. The most parsimonious interpretation of these results is that theta oscillations observed in striatal LFPs are largely contaminated by volume-conducted signals. We propose that striatal LFPs are not optimal proxies of network dynamics in the striatum and should be interpreted with caution.