Cerebellum (2015) 14:43–46 DOI 10.1007/s12311-014-0631-y

SHORT REPORT

Cerebellum and Personality Traits Laura Petrosini & Debora Cutuli & Eleonora Picerni & Daniela Laricchiuta

Published online: 15 December 2014 # Springer Science+Business Media New York 2014

Abstract Personality traits are multidimensional traits comprising cognitive, emotional, and behavioral characteristics, and a wide array of cerebral structures mediate individual variability. Differences in personality traits covary with brain morphometry in specific brain regions. A cerebellar role in emotional and affective processing and on personality characteristics has been suggested. In a large sample of healthy subjects of both sexes and differently aged, the macro- and micro-structural variations of the cerebellum were correlated with the scores obtained in the Temperament and Character Inventory (TCI) by Cloninger. Cerebellar volumes were associated positively with Novelty Seeking scores and negatively with Harm Avoidance scores. Given the cerebellar contribution in personality traits and emotional processing, we investigated the cerebellar involvement even in alexithymia, construct of personality characterized by impairment in cognitive, emotional, and affective processing. Interestingly, the subjects with high alexithymic traits had larger volumes in the bilateral Crus 1. The cerebellar substrate for some personality dimensions extends the relationship between personality and brain areas to a structure up to now thought to be involved mainly in motor and cognitive functions, much less in emotional processes and even less in personality individual differences. The enlarged volumes of Crus 1 in novelty seekers and alexithymics support the tendency to action featuring both personality constructs. In fact, Novelty Seeking and alexithymia are rooted in behavior and inescapably have a strong action component, resulting in stronger responses in the L. Petrosini : D. Cutuli : E. Picerni : D. Laricchiuta I.R.C.C.S. Santa Lucia Foundation, via Ardeatina 306, 00179 Rome, Italy L. Petrosini (*) : D. Cutuli : E. Picerni : D. Laricchiuta Department of Psychology, University “Sapienza” of Rome, Via dei Marsi 78, 00185 Rome, Italy e-mail: [email protected]

structures more focused on action and embodiment, as the cerebellum is. Keywords Personality traits . Alexithymia ROI- and voxel-based morphometry . Diffusion tensor imaging . Emotion regulation . Embodiment On the basis of family background, longitudinal developmental, psychometrical, neuropharmacological, and neuroanatomical studies, Cloninger identified primary-basic personality temperament and character traits. In his Temperament and Character Inventory (TCI), four temperamental traits, Novelty Seeking (NS), Harm Avoidance (HA), Reward Dependence (RD), and Persistence (P) are described [1]. In particular, NS refers to a proclivity to action and exploration in response to novelty, to impulsive decision-making, to extravagant approach to reward cues. The advantages of high NS scores are excitability, curiosity, enthusiasm, and quick engagement with whatever is new. Conversely, the disadvantages are indifference, lack of reflection, and intolerance to monotony, anger, and inconsistence in relationships. HA refers to a proclivity to inhibit behaviors, acting with caution and apprehensiveness, to respond intensively to aversive stimuli, to be worried, fearful, shy, and rapidly fatigable. The advantages of high HA scores are cautiousness and careful planning when hazard is likely. Conversely, the disadvantages occur when hazard is unlikely but still anticipated which leads to maladaptive inhibition and anxiety. Because personality traits are multidimensional traits comprising cognitive, emotional, and behavioral characteristics, a wide array of cerebral circuits mediates the individual variability. Associations have been demonstrated between personality factors and neurobiological measures, as neurotransmitter metabolites and various markers associated with in vivo neuroimaging [2]. Furthermore, personality traits covary with

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brain morphometry, as cortical thickness and gray matter volume in specific brain regions. Namely, high HA scores are associated with less efficient micro-structure in widely distributed fiber tracts, including cortico-limbic pathways, and they covary negatively with volumes of prefrontal, parietal and occipital cortices, and hippocampal structures [3, 4]. Conversely, NS scores are positively associated with the strength of fiber tracts from the hippocampus and amygdala to the striatum and with orbito-frontal and cingulate cortices as well as caudate and pallidum volumes [3, 5, 6]. And yet, these interesting studies have almost ignored the cerebellar involvement in the personality traits. Anatomo-clinical analyses indicated the cerebellum as a critical neuromodulator of intellect and mood and revealed that the posterior vermis, the so-called limbic cerebellum, is mainly involved in the regulation of emotion and affect [7]. Subjects affected by the cerebellar cognitive-affective syndrome originating from lesions of the posterior lobe and vermis exhibit executive dysfunctions, blunting of affect, and disinhibited and inappropriate behavior. The psychopathological profile of patients affected by cerebellar diseases of different etiology describes them as impulsive, obsessive, hyperactive, and with ruminative and stereotypical behaviors, all features affecting their personality style. Neuroimaging studies showed structural or functional abnormalities of the cerebellum in patients with personality, depression, or anxiety disorders [8]. Even data obtained in healthy subjects reported reduced capacities of emotional regulation following inhibitory repetitive transcranial magnetic stimulation to the cerebellum [9]. This evidence indicates a cerebellar role in affective processing, which has an effect on personality characteristics. On such a basis, by using neuroimaging techniques, in a large cohort of healthy and differently aged subjects of both sexes, we tested whether macro- and micro-structural variations in cerebellar areas were correlated with scores obtained in the TCI scales [10, 11]. Region of interest (ROI)-based analysis and voxel-based morphometry (VBM) analysis were used to detect macro-structural organization, while diffusion tensor imaging (DTI) protocol measuring the diffusion of water molecules through tissues was employed to detect micro-structural organization. The main results of these researches indicated that increased cerebellar volumes were associated with higher NS scores, while decreased cerebellar volumes were associated with higher HA scores [10]. Noteworthy, these associations were evidenced either in the white matter or in the cortex of both cerebellar hemispheres. No relationship between cerebellar volumes and the other two TCI scales (RD and P) was found. Furthermore, positive associations between volumes of the vermian lobules VIIb, VIII, and Crus 2 and NS scores were found (Fig. 1a). The relationship between NS scores and cerebellar structures was found also at micro-structural level,

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as indicated by the DTI data [11]. These micro-structural analyses indicated high cerebellar integrity and efficiency in relation to NS scores. As a whole, these innovative findings demonstrate that both macro- and micro-structural features of posterior vermis support some personality traits. The involvement of the cerebellar regions in the neuroanatomical geography of the personality appears reasonable, as the cortico-basal-cerebellar circuit is involved in emotional processing, attentional focus, and inhibitory control, all functions heavily associated with temperament traits. The cerebellar activity signals when sensory input differs from memory-driven expectations, providing thus a sensory prediction error, guides exploratory drive in novel environments, allows a flexible switching among multiple tasks or alternatives, and makes functions fast and adaptive. Cerebellum performs these roles by refining the rate, rhythm, and force of behavior and adjusting it for given situations. Intriguingly, cerebellum could play a similar role in facilitating motivation that sustains and reinforces the temperamental features. The positive correlation between cerebellar volumes and NS scores and the negative one between cerebellar volumes and HA scores are consistent with the different engagement the subjects with different styles of personality require to cerebellar circuitries. In fact, a subject searching for unfamiliar situations, making the unknown known, exploring new environments, displaying increased tendency toward risk-taking, sensation-seeking, and immediate reward-seeking, as novelty seekers do, needs very rapid detection of unfamiliar events, flexible switching among tasks, alternatives, and contexts, and fast adaptation to change. All these functions require heavy engagement of the cerebellum. Whether as hypothesized “larger is more powerful,” the higher requests a seeker makes to his cerebellum, could enlarge it, and vice versa the lower requests an avoiding subject makes to his cerebellum, could reduce it. However, it is far to be clarified whether temperamental traits determine the size of brain regions or conversely, the differently sized brain regions determine temperamental traits. Given the cerebellar contribution in personality traits and emotional processing, we investigated the cerebellar involvement even in alexithymia, construct of personality characterized by impairment in cognitive, emotional, and affective processing. It describes people with deficiencies in identifying, processing, or describing subjective feelings or emotional aspects of social interaction, difficulty in distinguishing between feelings and bodily sensations of emotional arousal, and limited affect-related fantasy and imagery [12]. Neuroimaging studies indicated that alexithymics show less activation and reduced volumes in brain areas associated with emotional awareness, as the anterior cingulate cortex, amygdala, parahippocampal gyrus and insula [13].

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Fig. 1 Cerebellar correlates of personality dimensions. Bilateral volumes in Crus 1 (Gray matter GM) were associated with novelty seeking (a) and alexithymia (b) scores and used as regions of interest (ROI) to extract raw data and create scatterplot where equation, R2, r, and p value, as well as fits (solid lines) are reported. Above colorbar, F is indicated. In figure left is left. Coordinates are in Montreal Neurological Institute (MNI) space

To further analyze the neurostructural bases of personality, we investigated whether in the alexithymics the altered cognitive experience of emotion evaluated by means of the Toronto Alexithymia Scale [12] was associated with cerebellar macro- (VBM) and micro- (DTI) structural measures [14]. The main result of this research demonstrated that cerebellar gray matter volumes were positively associated with alexithymia scores. The subjects with high alexithymic traits had larger volumes in the bilateral Crus 1 in comparison to the subjects with middle or low alexithymic traits (Fig. 1b). These increased volumes were not accompanied by significant alterations in density, surface, and orientation of cells as indicated by DTI values. Further, volumes of the right amygdala, left insula, and left parahippocampal gyrus were negatively associated with the alexithymia scores. Thus, alexithymia scores were linked directly with cerebellar areas and inversely with the limbic and paralimbic system, suggesting a possible functional modality for the cerebellar involvement in emotional processing. The increased volumes of Crus 1 could result in an enhanced inhibitory output of Purkinje cells on the deep cerebellar nuclei, modulating their excitatory activity. The inhibited activity of the cerebellar nuclei projecting to extracerebellar targets including the limbic system could result in a reduced excitatory input to limbic and paralimbic structures that in turn could undergo a volumetric reduction because of the diminished activation level. These structural data fit with the functional findings reported by Moriguchi and Komaki [15], who advance that alexithymics show neural responses to external and internal emotional stimuli reduced in the limbic system and increased in sensorimotor areas.

Given the network comprising the cerebellum and limbic system (and also the sensorimotor cortex) is involved in sensing and monitoring the physiological bodily condition and in feeling self- and externally induced emotions, the increased volumes in Crus 1 of alexithymics could be related to an altered embodiment process leading to not-cognitively interpreted emotions. On this vein, alexithymia may be considered an embodiment process related to altered perception of physiological correlates (viscero- and somato-motor responses) of the emotional activation resulting in a deficit in the emotional awareness. In conclusion, the enlarged volumes of Crus 1 in novelty seekers and alexithymics support the tendency to action featuring both personality constructs. In fact, NS and alexithymia are rooted in behavior and inescapably have a strong action component, resulting in stronger responses in the structures more focused on action and embodiment, as the cerebellum is. Conflict of Interest No conflict of interest is declared.

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Cerebellum (2015) 14:43–46 10. Laricchiuta D, Petrosini L, Piras F, Macci E, Cutuli D, Chiapponi C, et al. Linking novelty seeking and harm avoidance personality traits to cerebellar volumes. Hum Brain Mapp. 2014;35:285–96. 11. Picerni E, Petrosini L, Piras F, Laricchiuta D, Cutuli D, Chiapponi C, et al. New evidence for the cerebellar involvement in personality traits. Front Behav Neurosci. 2013;7:133. 12. Bagby RM, Parker JD, Taylor GJ. The 20-item Toronto Alexithymia Scale-I. Item selection and cross-validation of the factor structure. J Psychosom Res. 1994;38:23–32. 13. Reker M, Ohrmann P, Rauch AV, Kugel H, Bauer J, Dannlowski U, et al. Individual differences in alexithymia and brain response to masked emotion faces. Cortex. 2010;46:658–67. 14. Laricchiuta D, Petrosini L, Picerni E, Cutuli D, Iorio M, Chiapponi C, et al. The embodied emotion in cerebellum: a neuroimaging study of alexithymia. Brain Struct Funct. 2014. doi:10.1007/s00429-0140790-0. 15. Moriguchi Y, Komaki G. Neuroimaging studies of alexithymia: physical, affective, and social perspectives. Biopsychosoc Med. 2013;7:8.

Cerebellum and personality traits.

Personality traits are multidimensional traits comprising cognitive, emotional, and behavioral characteristics, and a wide array of cerebral structure...
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