Implicit vs. Explicit Emotion Processing in Autism Spectrum Disorders: An Opinion on the Role of the Cerebellum
Human beings are continuously exposed to external and internal emotional stimuli which are processed to create adaptive social relations. Based on the nature of emotional phenomena and on the effort required for their elaboration, emotional processing could be viewed along a continuum, ranging from an implicit/unconscious level to an explicit/conscious level (Lane, 2000) The implicit processing of emotions is meant to be an automatic, procedural, and non conceptual process that does not require conscious access to be executed. Instead, explicit processing requires declarative evaluation and involves higher cognitive resources to define conscious emotional states (Damasio, 1994; Lane, 2000) Within the extended neural network involved in the emotional field, the implicit processing of emotions has been linked to the amygdala and the anterior cingulated cortex (Critchley et al. 2005; Webb et al. 2010) while the temporoparietal junction and the medial prefrontal cortex have been reported to be mainly involved when the conscious attribution of emotions and intentions is required (Saxe and Kanwisher, 2003; Saxe and Powell, 2006) However, the neural networks underpinning these processes are still far from being well defined (Schaller and Rauh, 2017) Over the years, many scientific studies have recognized the cerebellum as being part of these brain networks (Stoodley and Schmahmann, 2010; Baumann and Mattingley, 2012; Leggio and Olivito, 2018; Clausi et al. 2019a; Van Overwalle et al. 2019a) and have evidenced its role in affective and emotional functioning (Adamaszek et al. 2015; Clausi et al. 2015, 2019b; Lupo et al. 2015, 2018) Accordingly, functional and anatomical connections have been found between the cerebellum and the cortical and subcortical structures involved in both implicit and explicit emotional processing (Critchley et al. 2000; Singer et al. 2004; Schutter et al. 2009; Stoodley and Schmahmann, 2010; Schraa Tam et al. 2012) The contribution of the cerebellum to implicit and explicit mechanisms underlying emotion processing has been recently acknowledged (Clausi et al. 2017) Indeed, the cerebellum is involved in implicit aspects such as the modulation of autonomic reactions, the automatic component of emotional learning associated, e.g. with fear conditioning (Critchley et al. 2000; Sacchetti et al. 2005; Timmann et al. 2010) and in the implicit processing of emotional facial expression (Schutter et al. 2009; Clausi et al. 2017) The cerebellar vermis might play a role in this stage of emotion elaboration through its connections with the brainstem (catecholamine neurons) the hypothalamus (Snider and Maiti, 1976) and the limbic areas, such as the amygdala and hippocampus (Sacchetti et al. 2005) Instead, regarding the explicit aspects, the cerebellum is involved in the self perception of negative emotions and in the integration of internal state information with external environmental stimuli to consciously and adaptively elaborate emotions (Timmann et al. 2010; Clausi et al. 2017, 2019a) The posterior portions of the cerebellum might contribute to these aspects by means of their connections with cortical areas involved in more complex features of emotional evaluation (i.e. the medial prefrontal cortex and temporoparietal junction) (Rudebeck et al. 2008; Buckner et al. 2011) Evidence about the "emotional cerebellum" has also been conveyed by clinical studies. Indeed, a pattern of emotional and affective disorders has been found in patients with cerebellar damage as part of the well known cerebellar cognitive affective syndrome (Schmahmann and Sherman, 1998; Tavano et al. 2007) Intriguingly, converging clinical and neuroimaging evidence points to a cerebellar involvement in the emotional disturbances and social cognition impairments described in people with autism spectrum disorders (ASD) (Fatemi et al. 2012; D'Mello and Stoodley, 2015) ASD are clinically complex and heterogeneous neurodevelopmental conditions characterized by core impairments in social interaction, repetitive behaviors, and restricted interests (American Psychiatric Association, 2013; Goldson, 2016) Emotional processing is a challenge for people with ASD, whose impairments have been reported for both implicit and explicit components (Senju, 2013; Lozier et al. 2014; Kana et al. 2016) Nevertheless, these aspects are often separately investigated, leading to controversial conclusions (Ben Shalom et al. 2006) Indeed, while most of the literature on people with ASD agrees on the existence of implicit emotional processing impairment, i.e. when the task requires the elaboration of emotional facial expression (Baron Cohen et al. 1997, 2001) controversial results emerge when the task requires the explicit elaboration of emotions. In the latest case, the heterogeneous nature of the ASD condition and camouflaging phenomena due to learned compensatory strategies might lead to the fallacious assumption that people with high functioning ASD (hf ASD) do not show such deficits (Senju, 2012; Schuwerk et al. 2014; Schaller and Rauh, 2017) For example, this could happen in tasks in which context information can help the person explicitly attribute emotions to others (Frith and Frith, 2012; Senju, 2012; Schaller and Rauh, 2017) However, it must be considered that when the amount of context information increases, the environment becomes more confusing, and the compensation ability may no longer guarantee the processing of emotional information (Frith and Frith, 2012) Indeed, when the complexity increases, the person has to integrate emotional processing with mentalizing ability to correctly infer emotional states (Mier et al. 2010) This complex social elaboration is impaired in people with hf ASD when dynamic video based stimuli close to everyday life are used or when various aspects of social situations are analyzed (Dziobek et al. 2006; Schaller and Rauh, 2011, 2017) Thus, the heterogeneity of capacities shown in a complex condition such as ASD, together with the variety of tasks used in different studies, may lead to controversial results. The complex behavioral outcome of people with ASD has been linked to the functional alteration of complex neural circuits encompassing several brain areas, such as the parietal, temporal, and frontal regions (Abell et al. 1999; Carper et al. 2002; Hazlett et al. 2006; Minshew and Williams, 2007) as well as subcortical structures (Sparks et al. 2002; Amaral et al. 2008; Cauda et al. 2011) Among these, the cerebellum has been consistently recognized as part of the distributed neural networks affected in people with ASD (Wang et al. 2014; D'Mello and Stoodley, 2015; Olivito et al. 2017; Stoodley et al. 2017) Indeed, evidence of structural and functional alterations in specific cerebellar regions and in cerebello cortical networks underlying emotional processing has been reported in this population (Courchesne et al. 1988; Khan et al. 2015; Stoodley et al. 2017; Arnold Anteraper et al. 2019) In particular, a decrease in the Purkinje cell number in the cerebellar vermis and a gray matter reduction in the posterior cerebellum have been found in people with ASD (Ritvo et al. 1986; Bauman and Kemper, 2005; Fatemi et al. 2012) together with altered functional connectivity between the posterior cerebellum and the frontal and temporal areas involved in mentalizing abilities (Olivito et al. 2017) In this framework, considering the suggested connections between the cerebellum and the cortical and subcortical structures involved in implicit and explicit emotional processing (Schutter et al. 2009; Stoodley and Schmahmann, 2010; Clausi et al. 2017) and the association between the cerebellum and the social emotional impairments in ASD (Wang et al. 2014; D'Mello and Stoodley, 2015) in the present opinion, we will provide some novel insights into the possible nature of implicit and explicit emotion processing deficits in ASD related to cerebellar specific involvement. To this aim, we will take into account the most primitive ability to process facial emotions to analyze the implicit emotional process and the capacity to integrate intricate environmental information with the theory of mind abilities to explicitly infer complex emotional states.
Frontiers in Psychology