Neuroimaging studies on the associations between neurobiological measures in specific brain regions and attachment styles have only occasionally reported the involvement of cerebellar circuits 18–20,37−39, and often have described it almost as an anecdotical finding. The present research, specifically aimed at analyzing the participation of cerebellar regions in the attachment behavioral system, found powerfully significant positive associations between the scores of the Preoccupation with Relationships, an ASQ subscale associated to insecure/anxious attachment, with extended clusters in cerebellar (right lobule VI and left Crus 2) and cortical (right mOFC) regions. The increased cerebellar and cortical volumes were not accompanied by modifications in DTI values. The positive associations between Preoccupation with Relationships scores and volumes in brain areas related to emotional and social processing are consistent with the increased efforts at processing the emotional stimulus and the hypervigilant nature of individuals with anxious/preoccupied attachment. In fact, these people are characterized by intense emotional responses and sustained search for security/predictability in the relationships. Despite their strong desire to achieve intimacy and approval in relationships, because of low opinion of themselves as deserving of salient relationship, they are mistrustful of others and their availability, and anxiously expect rejection or abandonment by relationship partners 5,40.
Although healthy, all participants were also evaluated by HAM-D and HAM-A scales 41,42. Positive correlations were found between scores of Need for Approval ASQ subscale and both HAM scales, and between scores of Relationships as Secondary ASQ subscale and HAM-A scale. Thus, the more anxious and depressive tendencies were evident, the more insecure attachment patterns were present, once more indicating that emotional reactions are modulated by individual differences in the social bonding 5.
Our present findings fit with previous structural data describing that anxious attachment is associated with increased volumes in cerebellar areas 18,20 and lateral orbital gyrus 18,43. Also, they fit with functional data describing that anxiously attached adults display enhanced activation to positive approach-related facial expression in the cerebellar and prefrontal areas involved in perception of facial emotion, assessment of affective value and social distance 19,20. Interestingly, enhanced cerebellar activation was observed in adolescents with a high negativity of the self-model, typical for the anxious attachment dimension 38. Furthermore, increased cerebellar activation has been described in a study investigating grief through the exposure of bereaved women to pictures of their deceased loved one 44. Bowlby 4 viewed grief related to affective loss as a natural expression of the attachment behavioral system evoked to discourage prolonged separation from a primary attachment figure. Such a kind of grief implies the coordination of multiple functions, as affect processing, mentalizing, episodic memory retrieval, processing of familiar faces, visual and motor imagery, autonomic regulation, automatic motor responses. Notably, most of these functions are mediated by a distributed neuronal network of which the cerebellum (especially, its posterior regions) is part 45. Cerebellar areas then might be rightfully inserted in the attachment behavioral system described by Bowlby 2. The cerebellar contribution to the attachment system may be interpreted as concomitant to a “feeling of being drawn toward” the affective stimulus, and reflects the more general cerebellar engagement in regulation of emotional and social behaviors (Laricchiuta et al., 202126,46,47. Given the neuronal circuits putatively responsible for social processes are closely associated with, and virtually inextricable from, those devoted to emotional regulation 48, it is not surprising that the same regions of the posterior cerebellum and prefrontal cortex are involved in both emotional regulation and social interaction.
According to psychological models of adult attachment 3, the complex interactions of thoughts and behaviors required for sensitive parenting of offspring enable formation of individual’s first social bonds, critically shape infants’ behavior, and deeply influence the adult social behavior. Such an assumption is strongly supported by animal and human studies indicating that early attachment experiences influence brain development and result in permanent structural and functional brain changes and in individual differences in cognitive performance and social behavior 11,49−51. In fact, in rodents, maternal experiences exert a marked transgenerational impact and influence offspring’s phenotype at behavioral (learning and memory abilities, attentional performance, coping response to stress, social behavior, anxiety levels) and neurobiological (synaptic plasticity, methylation in frontal and hippocampal areas, hippocampal neurogenesis, striatal and cerebellar neurotrophins) levels (Cutuli et al., 2018; Berretta et al., 2021). Noteworthy, the first mother-infant relationships influence not only infant’s developmental processes, but also mother’s neurobiological and behavioral processes. A recent study 52 on the maternal brain functional connectivity in the early postpartum phases reports changes in cerebello-cortical connectivity associated with changes in maternal anxiety toward her child, providing insight into the mother-infant bond in the specific context of anxiety. Analogously, fMRI studies on maternal brain during processing of infant affective cues have repeatedly implicated the cerebellum 53–55, suggesting that enhanced cerebello-cortical connectivity may increase prioritization of processing infant cues in the maternal brain. Very recently, in child-rearing mothers it has been described a significant association of increased resting-state functional activity in lobule VI with increased maternal trait anxiety and poorly adaptive sensory processing 56. Such a finding has been interpreted as an indicator of maternal trait anxiety and risk of parenting stress. The positive association between volumes of lobule VI-Crus 2 and Preoccupation with Relationships scores reported in the present research is consistent with neuroimaging findings 57 describing the activation of cerebellar and neocortical areas belonging to the default mode network that regulates the switch from an internal reference state to external target-oriented behaviors, once more emphasizing the cerebellar role of interface between internal and external environments. Since lobule VI-Crus 2 activation is associated with negative emotions 58, it is not surprising that just these cerebellar areas exhibit enhanced volume in individuals with anxious attachment. Considering the property of cerebellar networks in building internal models of internal or external environments through signal error processing 59, anxiously attached subjects could display continuous error signals to the cerebellum that thus does not habituate 60. These unremitting inputs could provoke a compensatory increase in cerebellar volumes.
In addition to increased volumes in lobule VI and Crus 2, Preoccupation with Relationships scores were associated with increased volumes of right mOFC, a prefrontal area critically involved in operational control of emotional and social stimuli 61,62. More specifically, OFC role in emotion is to decode the reward/punishment goals for action, by representing reward value and transmitting the resulting representations to other brain regions which implement the learning of actions to obtain the reward outcomes signaled by the OFC. Patients with OFC lesions are less sensitive to reward, and are unable to ‘‘think through’’ the consequences of their actions, relying conversely on ingrained habits or immediate information to guide their actions 63,64. Cerebellar properties of timing, prediction, and learning well integrate with OFC processing to control social and emotional functions 65–67.
Neuroimaging findings indicate that cerebellum and OFC are both involved in the pathophysiology of psychiatric disorders associated with dysregulation of affect, such as schizophrenia, mood disorders (major depression and bipolar disorder), anxiety disorders (such as phobias), and obsessive-compulsive disorder, post-traumatic stress disorder and attention deficit hyperactivity disorder 61,68,69. Moreover, while secure attachment is the foundation for psychological well-being 5, insecure patterns leading to self-doubts, anxiety and distress may represent a risk factor for psychopathology with the specific symptomatology depending on genetic, developmental, and environmental factors 50,70. Consistently, in adults and adolescents, preoccupied and fearful attachment styles are associated with heightened chronic pain, depression, pain catastrophizing and anxiety 71–73. The significant relationship between anxious attachment and borderline personality disorder features has been reported in both nonclinical and clinical samples 74.
In conclusion, we propose that in addition to OFC even the specific cerebellar areas previously demonstrated to be involved in emotional regulation have to be included in the current neurobiological models of human attachment 75. The present research may represent a step forward in mapping out the attachment process and improving our understanding of the pathophysiology of the attachment-related disorders.
The main strength of the present study is that it is the first macro- and micro-structural (VBM and DTI) study specifically aimed at analyzing the engagement of cerebellar structures in the attachment behavioral system.
Another strength is represented by the rather large sample of non-clinical subjects of both sexes (although exclusively whites) with a wide range of educational level.
However, the current study has some limitations leaving opportunities for future research.
The main limitation of the present research is the application of only a self-report measure of attachment, which may be subject to respondent bias and may potentially over-emphasize attachment as a conscious and detectable process 70. Although some research suggests self-report measures are reliable and valid sources of participant information 76, self-reported engagement in attachment-related processes may be of questionable accuracy. Conversely, the usage of informant measures of attachment, such as the Adult Attachment Interview (AAI; George et al., 1985), would have allowed evaluating conscious and unconscious memories related to childhood relationships with caregivers. Furthermore, this interview technique would have allowed assessing the perceived effects of these occurrences on adult personality.
An additional limitation could be that the usage of a VBM correlational approach does not permit to infer causal relationships between brain structural variations and psychological measures, as the ASQ. Furthermore, VBM findings do not allow clarifying the relationships among brain areas potentially involved in the same functions. Finally, the image transformations required for VBM might introduce artifactual volumetric differences, such as a partial volume error. In spite of these limitations, VBM represents a useful approach since it is a user-independent, unbiased exploration of the whole brain.
On such a basis, future studies may benefit from using multi-method approaches to explore the processes underlying the relationship between temperament, attachment and affective stories by using informant measures, interview techniques, and functional neuroimaging methods to capture these complex processes.