Corticostriatal Field Potentials Are Modulated at Delta and Theta Frequencies during Interval-Timing Task in Rodents

Abstract

Organizing movements in time is a critical and highly conserved feature of mammalian behavior. Temporal control of action requires corticostriatal networks. We investigate these networks in rodents using a two-interval timing task while recording LFPs in medial frontal cortex (MFC) or dorsomedial striatum. Consistent with prior work, we found cue-triggered delta (1-4 Hz) and theta activity (4-8 Hz) primarily in rodent MFC. We observed delta activity across temporal intervals in MFC and dorsomedial striatum. Rewarded responses were associated with increased delta activity in MFC. Activity in theta bands in MFC and delta bands in the striatum was linked with the timing of responses. These data suggest both delta and theta activity in frontostriatal networks are modulated during interval timing and that activity in these bands may be involved in the temporal control of action.

Keywords: Parkinson’s disease; dorsomedial striatum; interval timing; local field potential; medial frontal cortex; prefrontal cortex; striatum; temporal control.

FIGURE 1

Interval-timing task and histological validation. (A) Rats estimated a 3 or 12 s interval by pressing a lever. The first response after the end of the interval was rewarded with water. Multiple responses per trial were permitted. (B) Average response-timing curves from all eight animals included in the study. Responses were normalized within both 3 s (Int3) and 12 s (Int12) trials. (C) Representative photomicrograph of electrode tracts in the left hemisphere of medial frontal cortex (MFC) and dorsomedial striatum (STR) from a coronal view. M, Medial, L, Lateral. (D) Horizontal image of histological reconstruction from the four animals implanted with multielectrode arrays either in the MFC or STR. L, Left, R, Right. Red circles correspond to the locations of electrodes used in the study.

FIGURE 2

Cue-related low-frequency activity in MFC and dorsomedial striatum (STR). (A) LFPs recorded from MFC in four rats showed a cue-evoked ERP following the Int3 cue (blue) and Int12 cue (green). (B) Time-frequency analysis of LFPs revealed a delta/theta (3–12 Hz) burst triggered by the Int3 stimulus when the animal responded and was rewarded. (C) A delta/theta burst was visible after the Int12 stimulus on rewarded trials. (D) There was a significant increase in power in Int3 (blue) and Int12 (green) trials over their respective baselines (black) in the delta (left) and theta (right) frequency bands. Error bars denote variance across subjects. (E) LFPs recorded from STR in four rats showed a subtle ERP on Int3 reward trials (blue) and Int12 reward trials (green). Cue-related delta/theta activity in STR on Int3 (F) and Int12 (G) trials. (H) There was a significant increase from baseline at the delta frequency band but not at the theta band on Int3 reward trials (blue) and not at either frequency on Int12 reward trials (green). Error bars denote variance across subjects; Asterisk indicates p < 0.05.

FIGURE 3

Low-frequency activity power increased in trials with reward in MFC and dorsomedial striatum (STR) across the entire interval. (A) On Int3 trials, time-frequency analysis showed cue-related delta/theta activity and elevated delta activity throughout the interval. (B) Time-frequency analysis in MFC revealed ∼4-Hz activity over Int12 trials. (C) A significant increase in power over their respective baselines was visible in the delta and theta frequency bands on Int12 reward trials. Error bars denote variance across subjects. (D) Delta/theta activity was visible in STR on Int3 and (E) Int12 trials. (F) Significantly greater power was visible on Int3 and Int12 trials in the delta band in STR. Theta power was not significantly higher than baseline on either trial type. Error bars denote variance across subjects. Asterisk indicates p < 0.05.

FIGURE 4

Local field potential response-related activity in MFC and dorsomedial striatum (STR) during interval timing. (A) An ERP was visible in MFC on rewarded (green) vs. unrewarded (red) responses. (B) Time-frequency analysis around press events showed an increase in delta/theta power around rewarded press events. (C) Relatively low power was visible around unrewarded presses. (D) There was a significant increase in delta power prior to rewarded presses over both baseline and delta power prior to unrewarded presses. Error bars denote variance across subjects. (E) ERPs in STR both with rewarded (green) and unrewarded (red) presses. (F) An increase in delta power was visible prior to and especially after rewarded presses. (G) An increase in delta/theta power was also visible around unrewarded presses. (H) There was a significant increase in delta power over baseline prior to both rewarded and unrewarded presses. Error bars denote variance across subjects. Asterisk indicates p < 0.05.