Interaction between limbic circuits and basal ganglia in behaviour inhibition

Abstract

Changing behaviour in response to changing internal and external situations is crucial for survival. In particular, we need to inhibit ongoing, unwanted or inappropriate behaviour. Behavioural inhibition includes inhibition of an ongoing action, thought or emotion (in the basal ganglia; BG). But it can also involve inhibition of goals (in the limbic system) – which is much slower. A better understanding of the neural mechanisms controlling inhibition of behaviour is important for cognitive neuroscience, particularly in relation to problems of impulsivity. This thesis aims to fill a gap in our understanding of behavioural inhibition and to elucidate the parallel circuits that control its different types.

Several lesion, neuroimaging, and electrophysiological studies have been conducted to understand the role of brain regions in behavioural inhibition. Previous research has identified roles for the BG, orbitofrontal cortex (OFC) and hippocampus (HPC) in generation of various frequencies of rhythmicity during behavioural inhibition. However, the interaction between these regions has not been studied in rats during simple learning, simple action inhibition and complex behavioural inhibition. The stop signal task (SST) is the most commonly used paradigm to study simple behavioural inhibition. In this study, I recorded local field potentials (LFPs) simultaneously from BG (particularly striatum; STR and subthalamic nucleus; STN), OFC and HPC while rats performed the SST to assess how simple action inhibition differs from complex behavioural inhibition linked to goal-conflict.

The data show increases in the STN LFP spectral beta power and coherence with OFC after stopping an ongoing action (simple stopping). In contrast, stop failure increased HPC-STN coherent activity in the theta frequency band. In addition to the HPC, goal-conflict also activates OFC and STN during high conflict at higher theta frequency (11-12 Hz). In contrast, the conflict induced coherence effect was seen at lower theta frequencies (5-8 Hz) between two pairs of STN (HPC-STN and OFC-STN).

The results from the various experiments suggest that part of BG (STR and STN) and limbic system work in parallel and in a dynamic way for learning, response inhibition and complex behavioural inhibition (approach-avoidance conflict). The HPC is not involved in simple motor learning but may receive motivational information form STR and OFC. Simple inhibition involves mainly cortex and BG, while complex inhibition during goal-conflict also involves HPC, OFC and STN. Interestingly, goal inhibition appears to access circuits involved in simple stopping via OFC. In conclusion, functional connections between limbic and BG provides an adaptive control, so that goal selection (limbic structures) and programming of motor action (BG) can operate in parallel.