The basal ganglia and the cerebellum in human emotion

Abstract

The basal ganglia (BG) and the cerebellum historically have been relegated to a functional role in producing or modulating motor output. Recent research, however, has emphasized the importance of these subcortical structures in multiple functional domains, including affective processes such as emotion recognition, subjective feeling elicitation and reward valuation. The pathways through the thalamus that connect the BG and cerebellum directly to each other and with extensive regions of the cortex provide a structural basis for their combined influence on limbic function. By regulating cortical oscillations to guide learning and strengthening rewarded behaviors or thought patterns to achieve a desired goal state, these regions can shape the way an individual processes emotional stimuli. This review will discuss the basic structure and function of the BG and cerebellum and propose an updated view of their functional role in human affective processing.

Keywords: basal ganglia; cerebellum; connectivity; emotion; learning.

Fig. 1

Motor, associative and limbic functional subdivisions in the cortex, BG and cerebellum. The colored portions of each brain region highlight the major areas associated with each general function, illustrating the most distinct connectivity of each subcortical subdivision with widespread cortical areas. The cerebral cortex is shown from a lateral and midsagittal view, the BG from a coronal view and the cerebellum from a midsagittal view. GPi/GPe, internal/external globus pallidus; STN, subthalamic nucleus; VIII, IX, X, cerebellar hemispheric lobules VIII, IX, X. Adapted from Krack et al. (2010) with permission.

Fig. 2

Connections and select functions of the BG, cerebellum and cortex. This diagram shows the structural organization and functions of relevant pathways in the BG, cerebellum and cortex. During processing of an emotional stimulus, these regions (as well as, e.g. amygdala, hippocampus) cooperatively analyze the incoming information and generate an appropriate response, which includes action tendencies, physiological changes and subjective feelings. Green arrows indicate excitatory pathways, red arrows indicate inhibitory pathways, and the blue arrow indicates the dopaminergic pathway from the SN. SN, substantia nigra; GPi/GPe, internal/external globus pallidus; STN, subthalamic nucleus; PN, pontine nuclei; DCN, deep cerebellar nuclei; IO, inferior olive.

Fig. 3

Example of the chunking process in the limbic domain using vocal emotion processing. As proposed by Schirmer and Kotz (2006), processing of an emotional utterance proceeds in three steps from primary auditory cortex to superior temporal cortex to inferior frontal cortex. Simultaneously, connections with the BG allow them to iteratively assess contexts and select actions to form or control the expression of emotional (or motor/cognitive) sequences, explaining the BG’s sensitivity to the temporal and structural organization of events. When the emotional sequences are recurrent, the BG creates units of these sequence representations called ‘chunks’ at each level of the limbic auditory processing stream. These smaller chunks then can be combined into a larger representative chunk for a single sequenced response to a given stimulus that is activated without the need for attentional control of each step. Meanwhile, the cerebellum monitors prediction errors of internal models relying upon the performance of these chunks and can trigger adjustments to the ongoing sequenced behavior and recruit controlled processing as needed for optimal responding. Adapted with permission from Schirmer and Kotz (2006).