Cortico-striatal action control inherent of opponent cognitive-motivational styles

Turning on cue or stopping at a red light requires the detection of such cues to select action sequences, or suppress action, in accordance with cue-associated action rules. Cortico-striatal projections are an essential part of the brain’s attention-motor interface. Here, we used glutamate-sensing microelectrode arrays to measure glutamate transients in the dorsomedial striatum (DMS) of male and female rats walking a treadmill and executing cued turns and stops. Prelimbic-DMS projections were chemogenetically inhibited to determine their behavioral necessity and the cortico-striatal origin of cue-evoked glutamate transients. Furthermore, we investigated rats exhibiting preferably goal-directed (goal trackers, GTs) versus cue-driven attention (sign trackers, STs), to determine the impact of such cognitive-motivational biases on cortico-striatal control. GTs executed more cued turns, and initiated such turns more slowly, than STs. During turns, but not missed turns or cued stops, cue-evoked glutamate concentrations were higher in GTs than in STs. In conjunction with turn cue-evoked glutamate spike levels, the presence of a single spike rendered GTs to be almost twice as likely to turn than STs. In contrast, multiple glutamate spikes predicted STs to be robustly more likely to turn than GTs. In GTs, inhibition of prelimbic-DMS projections attenuated turn rates and turn cue-evoked glutamate peaks and increased the number of spikes. These findings suggest that turn cue-evoked glutamate release dynamics in GTs are tightly controlled by cortico-striatal neuronal activity. In contrast, in STs, glutamate release from DMS glutamatergic terminals is regulated by other striatal circuitry, preferably mediating cued suppression of action and reward tracking.