The Role of the Cerebellum in Unconscious and Conscious Processing of Emotions: A Review

: Studies from the past three decades have demonstrated that there is cerebellar involvement in the emotional domain. Emotional processing in humans requires both unconscious and conscious mechanisms. A signiﬁcant amount of evidence indicates that the cerebellum is one of the cerebral structures that subserve emotional processing, although conﬂicting data has been reported on its function in unconscious and conscious mechanisms. This review discusses the available clinical, neuroimaging, and neurophysiological data on this issue. We also propose a model in which the cerebellum acts as a mediator between the internal state and external environment for the unconscious and conscious levels of


Introduction
Emotional alterations have long been recognized in patients affected by cerebellar pathology, but have received little attention [1][2][3].
In 1998, the characterization of 'cerebellar cognitive affective syndrome' (CCAS) by Schmahmann and Sherman [4] extended the function of the cerebellum to the cognitive and emotional domains, demonstrating that these alterations are unrelated to cerebellar motor deficits [4][5][6][7].
There has been considerable progress in cerebellar research over the past decade and an increasing number of studies have reported the function of the cerebellum in sensory and perceptual mechanisms [8][9][10][11] and in components of the motor hierarchy, which are separate from mere motor control [12,13].
The link between the cerebellum and the emotional domain is also supported by findings of structural and functional cerebellar abnormalities in pathologies that are characterized by emotional disorders, such as schizophrenia, autism, and mood disorders [16,[21][22][23][24]].

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Emotional processing implies the existence of unconscious and conscious components.

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The cerebellum is connected to cerebral structures that are involved in unconscious and conscious emotional processing.

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In the unconscious component of emotions, cerebellar involvement is supported by its influence in modulating autonomic reactions, the automatic component of emotional learning, and implicit processing of facial expressions.

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In the conscious component of emotions, the involvement of the cerebellum is supported by its influence on the emotional content of fear conditioning, conscious processing of emotional facial expression, the ability to recognize negative emotions, and self-perception of negative emotions.

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In the emotional domain, measuring cerebellar function with regards to state estimation and its ability to process and predict sequential events allows us to compare internal and external events on the unconscious and conscious levels.

Emotional Unconscious and Conscious Circuits
It is generally recognized that emotional behaviors imply the existence of unconscious and conscious mechanisms [28,32,[40][41][42]. These components can be defined separately using concepts and neuroanatomy, although they should be considered on the same continuum that subtends emotional awareness [32].
The unconscious process comprises the sensory and motor components of an emotional response that precedes an emotional feeling state. In comparison, the conscious process includes the bodily states on the periphery of awareness (background feelings), the attention to one's subjective emotional state (focal attention to feelings) and thoughts about the contents of conscious emotional experience (reflective awareness) [42]. The two systems share most neuroanatomical substrates, but additional networks are involved in conscious processing [32,41].
Among the various theoretical models of the neural substrates of emotional processing, it has been proposed that emotional processing arises in subcortical networks and then influences cortical activity. Automatic and unconscious emotional processing is mediated by the amygdala, pulvinar, and superior colliculus [43]. These structures process basic emotional stimuli to orient and initiate the physiological arousal that characterizes emotions [44][45][46]. Other structures that are involved in the processing of unconscious emotional information include the hypothalamus, basal ganglia, brainstem nuclei, and the ascending neurotransmitter systems [32]. The cortico-pulvinar-cortical pathway has been suggested to link fast subcortical processing and the cortical structures that participate in higher-order conscious processing of emotions [40]. The pulvinar is connected to the extrastriate cortex (occipital cortex), inferior temporal cortex, and temporo-occipital area [47]. It is also associated with the insula [48], posterior parietal cortex [49], medial frontal cortex [49,50], superior temporal gyrus [51], and cingulate gyrus [50]. Most of these structures are involved in conscious processing of emotions and are part of the well-known default-mode network (DMN) [52], which has been linked to cognitive-emotional integration [53], emotional regulation [54], and emotional valence identification [55].
The neuronal networks between subcortical and cortical areas are bi-directional, indicating that bottom-up and top-down processes must be considered: i.e., that conscious processing of emotional information can alter the operation of subcortical structures and vice versa [32].
The cerebellum is strongly connected to cerebral structures that are involved in unconscious and conscious emotional components: the reticular system (arousal), hypothalamus (autonomic function and emotional expression), limbic structures (emotional experience and expression), and cortical association areas (cognitive processing of emotions) [56]. In particular, it receives afferent nerves from the medial mammillary bodies [57,58] and multi-modal deep layers of the superior colliculus in addition to being connected bi-directionally to the hypothalamus [59] and the brainstem areas (ventral tegmental area, periaqueductal gray, and locus ceruleus) that are related to the limbic and paralimbic regions [60]. The cerebellum receives information from the paralimbic cortices in the cingulate gyrus [61] via their projections to the pontine nuclei [62,63]. The caudal inferior parietal lobule, multi-modal portions of the superior temporal gyrus, and posterior parahippocampus contribute to the cortico-pontine projections through their connections with paralimbic structures [64,65]. Moreover, the cerebellum makes reciprocal connections with the prefrontal cortex [26]. Consistent with neuroanatomical findings, functional magnetic resonance imaging (fMRI) studies have demonstrated functional coherence between the cerebellum; the cerebral areas that mediate the processing of emotional information, such as the amygdala, hippocampus, hypothalamus, insula and anterior cingulate cortex; and cortical associative areas [27, [66][67][68].
In the following paragraphs, we will present data that support the hypothesis of cerebellar involvement in the unconscious and conscious components of emotional processing (summarized in Table 1).

Cerebellar Involvement in the Unconscious Component of Emotions
Cerebellar function in emotional responses at the unconscious level is supported by its influence on the modulation of autonomic reactions and the automatic components of emotional learning.
Based on clinical observations in patients affected by cerebellar damage, there is a lowered skin conduction response to negative stimuli [14] and an impaired blink reflex to fear stimuli [74]. Reports of impaired responsiveness of arterial blood pressure to aversive stimuli in animals [87] and a less extensive increase in heart rate during fear conditioning tasks in subjects with vermal lesions [75] indicate that the cerebellum is also involved in the autonomic neural pathways that subserve the cardiovascular system in emotion regulation [87][88][89]. Furthermore, fMRI studies have implicated that the cerebellar vermis is involved in autonomic responses that are associated with fear conditioning [78][79][80]83].
Fear is a crucial emotion and the capacity to develop fear-related memories has an important evolutionary advantage. The regulation of fear and fear memories consists of motor/autonomic components (changes in blood pressure and heart rate, dilation of pupils), endocrine, behavioral responses (freezing behavior, potentiated startle reflex) [90], and the affective component. It has been proposed that the cerebellar vermis mediates the conditioning of fear-related changes in autonomic functions, even in the absence of contingency awareness [90][91][92]. The central autonomic nuclei in the brainstem and cerebellum control the sympathetic and parasympathetic axes of the autonomic nervous system, allowing for the production of integrated somatic response patterns that are necessary for the metabolic support of emotional behavior [78].
The cerebellum is an important component in the central autonomic network [93], because the vermis is connected to the brainstem (catecholamine neurons) and hypothalamus [60].
Taking into account these connections, the vermis can be viewed as the interface between the sensory stimuli, emotional state, and motor responses of a subject. Thus, in the vermis, learning-related plasticity might be crucial for relaying the appropriate emotional and motor behaviors in response to sensory stimuli and maintaining this information for long periods. Consistent with this hypothesis, various animal studies have shown that the potentiation of excitatory [98,99] and inhibitory [100] synapses that impinge on the same Purkinje cells correlates with associative fear learning. These changes at the cellular level have long-lasting effects and are related to associative processes.
Other data support cerebellar function in the unconscious components of emotional processes with regards to its involvement in the implicit processing of facial expression [37]. Schutter et al. [37] found that repetitive Transcranial Magnetic Stimulation (rTMS) over the midline cerebellum enhances the implicit processing of happy facial expressions, with no changes in consciously experienced mood. These findings have been explained by projections from the cerebellar vermis to the ventral tegmental area of the midbrain, thus modulating the mesolimbic areas through ventral tegmental dopaminergic projections [60] (see Table 1 for details on reported studies).
These data from various experimental approaches suggest that the cerebellum automatically modulates emotional behavior to remain within homeostatic baseline levels and according to the context.

Cerebellar Involvement in the Conscious Component of Emotions
As discussed in the previous section, although the cerebellar vermis participates in fear-related somatic and autonomic aspects, the posterolateral hemispheres have been proposed to mediate the emotional content of fear conditioning at higher cognitive levels [114]. This assumption is supported by the presence of connections between the cerebellar hemispheres and the more ventral and caudal areas of the dentate nucleus, which in turn are connected to the temporal, parietal, and prefrontal cortices [115], which are involved in cognitive elaboration of emotional content [32].
Posterior regions of the cerebellum are activated during the anticipation [80], conscious feelings, and empathy of pain [82].
Furthermore, activation of the posterolateral cerebellar hemispheres is observed in the late acquisition phase of fear conditioning that is linked to the conscious elaboration of emotional content of associative learning [79,114].
Consistent with these findings, the cerebellum appears to be involved in more complex functions that are inherent to emotions and affects. This idea is supported by neurophysiological data that show a connection between the cerebellum and higher-order cerebral domains [84,85]. Whereas cerebellar input to autonomic pathways travels along a closed neuronal loop, event-related potentials (ERP) data has characterized the cerebellum in higher-order emotional processing as an active interface with large-scale cerebral pathways that are involved in emotionally conscious processes, including recognition and response to cues with emotional valence. Impairments in visual emotional attention [84] and emotional face recognition [85] have been reported in subjects affected by cerebellar hemispheres damage.
Moreover, neuroimaging and neurostimulation studies have shown the involvement of the cerebellum in conscious processing of emotional facial expressions [69,81,85].
The processing of emotion from facial expressions requires various psychological processes that are controlled by a wide array of cerebral structures [116], which involve both unconscious and conscious processes [17,78]. Facial perception is defined as "higher-level visual processing of faces" [117], involving perception and recognition of the emotional meaning [118]. Facial expressions are crucial to non-verbal social interactions and are markers of an internal state or an intention [119,120]. Recognizing facial expressions is vital in a complex social world as it permits one to detect the emotional state of another person and provides cues on how to respond in social situations [121,122].
As discussed in the previous section, the cerebellum has been linked to the implicit processing of facial expressions. However, fMRI studies have shown that the cerebellum is also activated in addition to the amygdala and prefrontal cortex during conscious processing of emotional faces [17,36].
These findings are not surprising, considering that the cerebellum belongs to a widespread network, including the amygdala-medial prefrontal circuitry, which contributes to determine the meaning of external stimuli and to facilitate cortical processes to react to them coherently [17,123]. Specifically, the medial prefrontal cortex is involved in emotional self-awareness, playing a key role in complex aspects of emotional processing, such as social interaction [124]. The amygdala is associated with the perception of emotion, specifically faces [118] and emotional arousing effects [125][126][127][128].
Direct support of the hypothesis of cerebellar function in the conscious processing of emotional faces comes from stimulation studies that have observed a greater ability to recognize negative facial expressions after transcranial direct current stimulation (tDCS) is performed over the cerebellum [86].
Clinical studies in patients with cerebellar damage have also highlighted the involvement of the cerebellum in emotional recognition, allowing proper social cognition regardless of stimulus (visual or auditory), particularly for negative emotions [69,72], and in more complex social cognition domains. This has become known as the Theory of Mind (ToM) [73,76,77].
Cerebellar function in the conscious mechanisms of emotional processing has been evidenced by its incorporation into the complex neural circuits that are involved in the cognitive functions [5,26] needed for defining and expressing the emotional state in oneself or in others. The experience of feeling is fundamentally influenced by one's conscious awareness and interpretation of one's mood [129], requiring interdependence between emotion and cognition that is sustained by the extensive interconnections between the limbic system and the cortical association areas [130] to which the cerebellum is strongly connected.
Cerebellar recruitment in the conscious component of emotional behavior, related to the awareness of one's affective state and the interpretation of one's mood, has been observed as a loss in self-perception of emotions in the presence of cerebellar pathology [70,71,131]. In recent studies, we found that patients with cerebellar damage were unable to feel conscious emotions of regret as a consequence of their disadvantageous choices in a gambling task [71] or to explicitly recognize their bad mood in the presence of clinically relevant depressive disorder [70,131] (see Table 1 for details on reported studies).

Discussion
To understand cerebellar function in the various mechanisms that underlie emotions, we must consider that emotional processing involves various physiological, cognitive, and behavioral components. As discussed, emotional processing is usually triggered by the unconscious and conscious perception of internal or external events, and by cognitive judgments [132,133]. It is associated with changes in body states (i.e., skeletal muscle activity, visceral organs, facial expressions) that are preparatory for adaptive behavioral responses [134][135][136][137]. These alterations can result in conscious feelings that imply a cognitive understanding of their conceptual emotional meaning. The internal states might be generated by our own choices or by external events and are characterized by emotional valence (positive or negative) [138,139] that influences behavioral actions [140]. Emotional processing is also modulated by other cognitive systems, such as attention, reasoning, and memory [141,142].
Overall, the processing of emotional information implies bottom-up and top-down mechanisms that ensure coherence between emotional states following internal or external events and suitable behaviors for various social contexts.
These mechanisms are controlled by complex neuronal networks in which the cerebellum functions, as reported in the previous sections [26,57,60,61,115].
Thus, the cerebellum might be a central component at which various information streams from and to the cerebral structures converge, subtending unconscious and conscious mechanisms of emotional processing.
The cerebellar vermis has been reported as the hub that perceives and forwards emotional cues in the subcortical-cortical networks [56] that are primarily involved in the unconscious stage of emotion, whereas the cerebellar hemispheres have been argued to be involved in high-order cognitive functions that allow conscious emotional processing to be linked to the internal state and perception of the external environment [56,143].
Thus, the cerebellum is equipped for unconscious and conscious processing, contributing to internal representations of emotions in addition to the monitoring and integration of interoceptive and exteroceptive information.
We recently proposed the "sequence detection model" as an operational mode in which the cerebellum processes information that is related to several domains, including the emotional domain [144,145]. According to this model, the cerebellum compares disparate states, regardless of the domains that are involved (motor, cognitive, or emotional) [146]. In particular, the cerebellum detects and simulates repetitive patterns of temporally or spatially structured events, allowing the creation of internal models [147] and the prediction of incoming events [148]. Thus, this constantly tunes motor, behavioral, and emotional responses, based on the ever-changing environment [149].
Considering the function of the cerebellum in state estimation [146], we propose that in the emotional domain, this structure mediates the comparison between the internal state and external event, contributing to self-perception of an emotion that is coherent with the environment. Essentially, it intervenes when the subject must compare the basic emotional state (internal state) and the possible effect of an action or context (external event).
In this framework, we have demonstrated that in estimating regret, a subject with cerebellar damage fails to compare the basic emotional state (internal state) that follows his decision and the state that is determined by the external event, based on a gambling result [71]. Similarly, in estimating mood state by a mood monitoring (MoMo) device [150], a subject who is affected by cerebellar damage is unable to recognize his bad mood state (internal state), which shows his inability to compare the internal state with the external negative or positive event [70,131].
These observations are consistent with the cerebellar involvement in optimizing internal and external responses according to the environment, akin to a master regulatory structure for integrating motor, emotional, and sensory information that affects "mind-world synchronization" [151]. When cerebellar function is altered, the processing of information streams becomes desynchronized [147,151,152], providing a breeding ground for various psychopathological disorders, such as schizophrenia, autism, and depressive disorders, in which cerebellar dysfunctions have been reported [153][154][155]. For example, certain symptoms of schizophrenia and the dysregulation of mood homeostasis in depression disorders have been linked to a failure to compare internal and external representations [151].
The cerebellar dysfunction in these diseases further supports the hypothesis that cerebellar processing also participates in generating coherent and conscious representations of self-perception and the external world [39,71,146,156].
Overall, the emotional and behavioral impairments in cerebellar patients and psychopathologies, in which structural and functional changes occur at the cerebellar level, might arise from an internal discrepancy between internally perceived and externally generated signals. This internal coherence at the unconscious and conscious levels is necessary to ensure an emotional behavior that is coherent with the environment and a self-perception of one's emotional state that is consistent with the context.

Conclusions
Following the theoretical framework above, emotional processing implies the existence of unconscious and conscious components that require complex bottom-up and top-down interactions [32]. These interactions are necessary to compare the expectations that are related to past emotional experiences or a social situation, with sensory inputs from the body states through feedforward and feedback signals. As evidenced in this review, the cerebellum participates in modulating the unconscious and conscious levels of emotional processing. This is understandable in the sequence detection theory, which implicates the cerebellum as a structure that compares disparate states to create internal models and predict events [144,145]. Thus, in the emotional domain, measuring cerebellar function with regards to state estimation and its ability to process and predict sequential events allows one to compare different states, integrating internal and external events at the unconscious and conscious levels. This is allowed by the cerebellar integrated functioning in the complex neural networks that subserve the unconscious and conscious components of the emotional domain [56][57][58][59][60][61][62][63][64][65].
This proposal opens new perspectives on cerebellar function in the etiopathology of neuropsychiatric and mood disorders and novel neuromodulatory therapeutic approaches.