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

Combined Functional Role of the BG and Cerebellum in Emotion

The direct connections between the BG and cerebellum allow these regions to work together to modulate processes such as motor control and emotion recognition or expression, with the two regions guiding the selection and precision of behavioral output. Both structures participate in learning appropriate responses (Box 1), primarily using reward feedback in the BG and prediction error feedback in the cerebellum to adjust response selection and execution (Doya, 2000; Tanaka et al., 2004; Bostan et al., 2013; Taylor and Ivry, 2014; Fermin et al., 2016; Bostan and Strick, 2018; Eisinger et al., 2018; Caligiore et al., 2019). Importantly, their functions are not entirely distinct, however, but overlapping, with the BG also encoding prediction error (Cox and Witten, 2019; Pine et al., 2018) and the cerebellum responding to reward presentation (Kostadinov et al., 2019). The reward-related BG circuitry with differential dopaminergic sensitivity in the direct and indirect pathways allows for the selection and strengthening of an appropriate cortical response and inhibition of other, unrewarding responses. In conjunction with this selection process, the cerebellum's uniform cellular architecture performs fine-tuning of the selected response (whether it be an emotional reaction, linguistic rehearsal or motor movement) to optimize the outcome based on the internal model of the individual's current state.

Subcortical Synchronization and Modulation of Cortical Emotional Responses

The ventromedial STN, based on its advantageous position in the hyperdirect pathway consisting of closed loop connections with limbic frontal cortex, may be critical for (de)synchronizing cortical neural oscillations that produce an emotion response pattern following a salient environmental cue (Péron et al., 2013). The BG's sensitivity to the temporal characteristics of a stimulus (Buhusi and Meck, 2005; Péron et al., 2017) allows for precise control of distant cortical activity with the inhibitory effect of increased STN output modulating cortical responses to emotional stimuli to generate an appropriate response while limiting competing signals from task-irrelevant or task-incidental co-activations. This modulatory effect on cortical targets is influenced further by dopaminergic input to the BG, which increases cortical excitability following rewarding stimuli or behaviors (Costa et al., 2006).

By gating the starting and stopping of emotional response patterns (Ory et al., 2017), the BG influence cortical learning as the relevant neural populations increase their connectivity strength through synchronous firing. Over time, repetition of this selection process leads to the creation of sequences of cortical representations that are 'chunked' together into habit-like responses that can occur nearly automatically following an emotional cue (as in the motor domain; Graybiel, 2008). As such, the BG may be particularly important during the acquisition of new emotional response patterns or in new emotional contexts when strong rewards or prediction errors lead to the formation or alteration of cortical response chunks. This chunking process allows for more rapid access to holistic sequenced responses without the need for costly attentional intervention, which is crucial when interacting with emotional stimuli such as a fearful facial expression.

The limbic cerebellum, on the other hand, modulates the amplitude of cortical oscillations based on prediction error feedback of the selected response relative to the given context (Booth et al., 2007; Schmahmann, 2019). Input to the cerebellum regarding the salience and motivational value of emotional stimuli guides internal models to determine how an emotional response benefits individuals in their current state and, thus, shapes how output from the cerebellum modifies the limbic response pattern. By continuously monitoring performance of the individual in terms of prediction error, the cerebellum ensures that large deviations from the expected response/outcome are quickly corrected (Peterburs and Desmond, 2016). In cases of cerebellar lesions, however, a lack of cerebellar amplification of emotional networks may lead to the blunted affect and decreased subjective experience of emotions often reported in patients (Adamaszek et al., 2017).

An example of the contribution of the BG and cerebellum to emotion processing can be found during perception of an angry voice (Figure 3). The recognition of relevant emotional prosody information begins in primary auditory cortex with extraction of basic acoustic features and then proceeds to more anterior regions of superior temporal cortex for identification of general emotional cues and then to the inferior frontal cortex for elaborated processing of the emotional salience and semantic content of the voice (Schirmer and Kotz, 2006). Throughout this processing pathway, the BG enhances activity within the neural representation (i.e. a habit-like 'chunk') corresponding to a previously reinforced experience with a similar angry voice, more quickly activating downstream regions to reach a decision threshold or generate a motor response that matches what was rewarded in the earlier encounter. Simultaneously, the cerebellum checks whether the state of the individual varies from the expected state at any time during the emotion recognition process. If this prediction error exceeds a given threshold defined by the context (e.g. the individual's goals, familiarity with the speaker, stress levels), then the cerebellum can refine the cortical/BG response and recalibrate the internal model. Nonetheless, since the BG and cerebellum do not directly store or produce emotional response patterns themselves, lesions to these regions do not necessarily cause gross emotional deficits (but see Section 3.2 and Schmahmann and Sherman, 1998; Levisohn et al., 2000, for significant clinical symptoms). Instead such damage leads to a more subtle neural miscoordination that may hinder efficient emotion recognition by introducing additional noise into the system (Péron et al., 2013; Schmahmann, 2019).

Figure 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).

Overall, in the healthy brain, repeated synchronization of cortical regions by the BG and fine-tuning by the cerebellum strengthen representations of a given response pattern and allow learned emotional responses to be generated more automatically in the future, just as with motor behaviors. Furthermore, studies suggest that this emotional synchronization occurs regardless of the valence (positive or negative) or modality (auditory or visual) of the emotional stimuli (Turner et al., 2007; Baumann and Mattingley, 2012; Péron et al., 2013,, 2017), and during emotion recognition as well as production, assuming the limbic network reactivates in a similar fashion during perception without executing the motor expression of an emotional response (Ferrari et al., 2018). Connections with regions controlling motivation (nucleus accumbens, substantia nigra, ventral tegmental area), relevance detection (amygdala) and physiological responses (brainstem) also imply a broad influence on emotion (Ikai et al., 1992; Baumann and Mattingley, 2012; Péron et al., 2013; Bostan and Strick, 2018; Habas, 2018) and warrant further attention in future neuroimaging studies.

The synchronization mechanism proposed above is consistent with the general function of the BG and cerebellum in other domains, suggesting that subdivisions of these structures perform similar processing in different tasks depending on the pattern of cortical and subcortical connectivities with different functional networks. Limbic, cognitive and motor functional domains in the BG and cerebellum could allow for integration of multiple cortical inputs within or across domains, perhaps occurring within the STN (Mathai and Smith, 2011; Péron et al., 2013) and the DCN (Habas, 2010), respectively, as these small structures receive converging input from other parts of the BG or cerebellar hemispheres. Most evidence, however, indicates largely distinct processing streams for each functional domain that output to the same cortical regions from which they receive input (Middleton and Strick, 2000; Kuper et al., 2011; Stoodley and Schmahmann, 2018). Additionally, different neural subpopulations could utilize distinct oscillation frequencies to gate activity for short- or long-range connections and to increase the computing power of limited neural resources. Ultimately, affective processing, like many other brain functions, relies on the selection and inhibition of response patterns by the BG and fine-tuning of the selected response by the cerebellum to minimize mismatch between one's expected and actual internal state in a given context.

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