The Cerebellum as an Embodying Machine

Abstract

Whereas emotion theorists often keep their distance from the embodied approach, theorists of embodiment tend to treat emotion as a mainly physiologic process. However, intimate links between emotions and the body suggest that emotions are privileged phenomena to attempt to reintegrate mind and body and that the body helps the mind in shaping emotional responses. To date, research has favored the cerebrum over other parts of the brain as a substrate of embodied emotions. However, given the widely demonstrated contribution of the cerebellum to emotional processing, research in affective neuroscience should consider embodiment theory as a useful approach for evaluating the cerebellar role in emotion and affect. The aim of this review is to insert the cerebellum among the structures needed to embody emotions, providing illustrative examples of cerebellar involvement in embodied emotions (as occurring in empathic abilities) and in impaired identification and expression of embodied emotions (as occurring in alexithymia).

Keywords: affective neuroscience; alexithymia; embodiment; emotions; empathy; internal models.

Figure 1.

Interoception and predictive coding. Motor and autonomic signals evoke interoceptive responses, “intero (actual),” which are compared with predicted responses, “intero (pred).” These predictions are generated by hierarchically organized forward models informed by motor and autonomic efference copy signals. The comparison might take place in the inferior olive and generates a prediction error to be sent to the cerebellum. Adapted from Seth and others (2012).

Figure 2.

Schematics of the internal model control. (A) A forward model is implemented in the cerebellum. It mimics the dynamic properties of the controlled object: a body part or a mental model. The sensory system (SS) mediates feedback (indicated by –). Circles indicate junctions at which signals converge or are relayed. In the inferior olive (IO), the outputs of (a) the controlled object (monitored by the SS) and (b) the cerebellum are compared to produce the error signals that are then sent to the cerebellum to eventually modify its internal models. (B) An inverse model is implemented in the cerebellum. It mimics the reciprocal of the dynamic properties of the controlled object. The oblique arrows in panels A and B represent the pathway signals that tune the dynamics of the forward model or the inverse dynamics of the inverse model. pRN = parvocellular red nucleus. Adapted from Ito (2008).

Figure 3.

Macro- and microanatomy of the human cerebellum. (A) Unfolded view of the cerebellar cortex shows lobes, lobules by name and number, and main fissures. Hemispherical lobules are designed by the prefix “H” according to Larsell’s classification and are followed by Roman numerals indicating the corresponding vermian lobules. Adapted from Manni and Petrosini (2004). (B) Cellular and fiber elements of the cerebellar cortex. A vertical section of a single cerebellar folium, in longitudinal and transverse planes, illustrates the general organization of the cerebellar cortex. The cellular architecture of the cerebellar cortex is uniform throughout the folia. Purkinje cells, the sole output of the cerebellar cortex, mainly project to the deep cerebellar nuclei and receive excitatory input on their extensive arborization from a beam of parallel fibers arising from several granule cells and from a single climbing fiber arising from the inferior olive.

Figure 4.

Functional specialization in the cerebellum. Cerebellar task activation maps (A) and resting-state networks (B). Adapted from Schmahmann (2021).

Figure 5.

Positive associations between cerebellar gray matter volumes and empathy and alexithymia. Coordinates are in Montreal Neurological Institute space. Z below color bar indicates normalized t values. In figure left is left. FWE = familywise error rate.

Figure 6.

Forward models and prediction. (A) To predict the sensory consequences of actions, a forward model is implemented in the motor cerebellum by interacting with the motor cortex and using efference copies of motor commands, which reach the cerebellum through the mossy fibers (MF) originating in the pontine nuclei (Pons). The difference between the predicted and actual motor outcome (prediction errors) reaches the cerebellum through the climbing fibers (CF) originating in the inferior olive (IO). (B) Because the uniformity of cellular organization across the cerebellar cortex suggests identity in the computations, the cerebellar forward models may even provide computational mechanisms for cognitive/emotional processes. The cerebellum models interoceptive and cognitive prediction errors, given its connectivity with the cingulate cortex, hypothalamus, and amygdala, as well as with frontal and parietal cortices via the thalamus (Th). A copy of the output of the prefrontal and frontal cortex is sent via the pontine nuclei to the interconnected cerebellar lobules. The predictions generated from cerebellar lobules are transmitted from the Purkinje cells via the deep cerebellar nuclei (DCN) and the thalamus back to the same neocortical areas. Predicted and actual consequences of the process copied by these cerebellar lobules are compared in the inferior olive, and any mismatch between the two are fed via climbing fibers to the cerebellar cortex as an error signal. Long-term depression is triggered at the parallel fiber to Purkinje cell synapses, updating the internal model.

Figure 7.

Emotional awareness and putative mechanism of alexithymia and alexisomia. Proprioceptive, visceral, hormonal, immune, and metabolic signals on the bodily physiologic state constitute interoception, which is the basis of the core affect. The core affect represents the basic affective state with specific properties of valence (pleasure or displeasure) and arousal (agitation or calmness). Emotions are constructed and categorized through bodily internal information (core affect), information from past experiences, and external sensory information (visual, auditory, olfactive). Emotional awareness has different levels: at the lower level, there is the interoceptive awareness, which is strongly connected to bodily state and core affect. Difficulty in interoceptive awareness is called alexisomia. At higher levels of emotional awareness, there is the categorization process that integrates the three sources of information and constructs an emotional state. The difficulty in categorization results in a reduced cognitive awareness, which is called alexithymia.