The Basal Ganglia and the Cerebellum in Human Emotion

Jordan E. Pierce; Julie Péron

Disclosures

Soc Cogn Affect Neurosci. 2020;15(5):599-613. 

In This Article

Abstract and Introduction

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.

Introduction

The basal ganglia (BG) and the cerebellum traditionally have been assigned to roles within the motor domain, yet recent research has recognized their contributions to a variety of functions, including affective processing. Specifically, the roles of these subcortical structures have expanded beyond simple motor control to diverse limbic and cognitive processes including emotion recognition, reward- and error-based learning, language, decision-making, working memory and spatial attention (Haber and Knutson, 2010; Cavanagh et al., 2011; Bostan et al., 2013; Buckner, 2013; Péron et al., 2017; Wojtecki et al., 2017; Bostan and Strick, 2018; Eisinger et al., 2018; Schmahmann, 2019). The current review will focus on the aspects of affective processing supported by each of these structures via their connections with a broad limbic network and on how recently identified direct subcortical connections between them may allow for coordinated modification of cortical responses to emotion in humans.

In general, limbic cortical and subcortical regions supporting emotion allow individuals to identify and prepare reactions to salient environmental stimuli, shaping how one perceives the world and interacts with positive or negative cues (Scherer, 2009; Brosch et al., 2013). The amygdala has long been recognized as a central structure for the detection of salient emotional stimuli, modifying responses in sensory cortex to favor relevant items, recruiting top-down attention in frontal-parietal cortex, driving hypothalamic and brainstem autonomic reactions and biasing hippocampal memory formation (Sander et al., 2003; Vuilleumier, 2005; Brosch et al., 2013). Neocortical regions such as ventromedial and orbitofrontal cortex, anterior cingulate cortex and anterior insula also are involved in emotion and reward processing, further guiding the recognition of relevant sensory input, motivation for action and generation of an appropriate emotional response (Dolan, 2002; Thielscher and Pessoa, 2007; Haber and Knutson, 2010; Rudebeck and Rich, 2018).

Recent evidence from neuroimaging studies suggests that these core limbic regions are supported by the BG and cerebellum during affective tasks (Tanaka et al., 2004; Baumann and Mattingley, 2012; Schraa-Tam et al., 2012). Additionally, clinical assessments have highlighted the deficits in emotion processing following lesions to the BG or cerebellum (Schmahmann and Sherman, 1997; Le Jeune et al., 2008; Péron et al., 2017; Thomasson et al., 2019), while structural and functional alterations have been reported in several psychiatric disorders (Gunaydin and Kreitzer, 2016; Lupo et al., 2018). These findings support the idea that the BG and cerebellum contribute to a range of affective functions including recognition of emotional stimuli such as faces or voices, reward processing, generation of autonomic responses, inferring the emotional state of others (theory of mind) and awareness of subjective feelings (Clausi et al., 2019b; Cox and Witten, 2019; Ferrari et al., 2018; Péron et al., 2010; Schmahmann, 2019; Strata, 2015).

Furthermore, connections exist between many parts of the limbic network (e.g. amygdala, orbitofrontal cortex) and the BG and cerebellum, which, in addition to the direct connection between these two regions, allow for a modulatory influence on affective processing across the brain (Hoshi et al., 2005; Habas et al., 2009; Lambert et al., 2012). Historically, these multisynaptic connections between the BG and cerebellum, and with the neocortex, have been difficult to identify, but newer viral tracing procedures have allowed researchers to isolate their input/output channels in animal studies (Hoshi et al., 2005; Bostan et al., 2010). In humans, advances in neuroimaging techniques have provided evidence of similar connectivity between the BG, cerebellum and cortex (Habas et al., 2009; Pelzer et al., 2013; Milardi et al., 2016). The BG and cerebellum, indeed, are connected structurally and functionally with most of the neocortex and contain sensorimotor, associative and limbic functional domains organized in multiple input/output loops (Figure 1; Buckner et al., 2011; Mathai and Smith, 2011). The highly connected nature of the BG and cerebellum (Hoshi et al., 2005; Bostan and Strick, 2018) allows them to perform parallel and integrated processing of cortical inputs to select and modify behavioral response patterns, resulting in a broad influence on emotion, informed by higher cognition, and with ready access to the motor network. The following sections of this review will describe the anatomy and function of the BG and cerebellum in relation to emotion processing, focusing primarily on human studies from healthy individuals as well as clinical populations, before highlighting their direct connectivity and proposed combined influence on cortical affective responses.

Figure 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.

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