Structural differences in the cortex of individuals who experience the autonomous sensory meridian response

Abstract Background and purpose The autonomous sensory meridian response (ASMR) is a multimodal perceptual phenomenon in which specific sensory triggers evoke tingling sensations on the scalp, neck, and shoulders; these sensations are accompanied by a positive and calming affective state. Previous functional neuroimaging research has shown that ASMR experiences involve medial prefrontal and sensorimotor brain areas. The purpose of the current study was to examine whether there are structural differences in the cortex of individuals who experience ASMR. Methods Seventeen individuals with ASMR and 17 matched control participants completed an MPRAGE structural MRI scan. These data were analyzed to determine if group differences were present for measures of cortical thickness, cortical complexity, sulcal depth, and gyrification. Results ASMR was associated with reduced cortical thickness in a number of regions including the left precuneus, precentral gyrus, and insula, and the right orbitofrontal cortex, superior frontal cortex, and paracentral lobule. Reduced thickness was observed bilaterally in the supramarginal gyrus. Individuals with ASMR also showed less cortical complexity in the pars opercularis and pars triangularis. Conclusions The differences in cortical thickness and complexity were in brain areas whose functions relate to the ASMR experience. These differences include neural regions related to phonological processing, sensorimotor functions, and attention.

The subjective reports of ASMR experiences have been corroborated by research examining its neural substrates. Psychophysiology researchers reported that ASMR involves an increase in skin conductance responses and a reduced heart rate (Engelbregt et al., 2022, Poerio et al., 2018. Functional MRI studies have demonstrated that ASMR videos elicit activity in the anterior cingulate gyrus and sensorimotor regions including the paracentral lobule, supplementary motor area, and spinal cord (Lochte et al., 2018, Smith et al., 2019, Smith et al., 2022. Finally, research using electroencephalography has indicated that ASMR is associated with increased alpha wave activity in medial frontal regions and increased gamma wave activity in sensorimotor cortex (Smith et al., 2022), as well as with increased beta wave activity in the left temporal lobe (Engelbregt et al., 2022); decreased theta wave activity was also observed in left frontal and right temporal regions (Engelbregt et al., 2022). Together, these early investigations indicate that the experience of ASMR produces verifiable changes in neural activity in several regions of the nervous system.
Although these task-based neuroimaging studies have helped identify the brain areas involved in the ASMR response itself, less is known about why some individuals experience ASMR "tingles" while others do not. Resting-state functional MRI studies have demonstrated that individuals with ASMR have a greater "blending" of resting-state networks than people who do not experience ASMR (Fredborg et al., 2021).
However, these studies did not examine whether there are structural differences between individuals who experience ASMR and those who do not. The goal of the current research is to measure cortical thickness and complexity, sulcal depth, and gyrification to determine whether ASMR is associated with unique neural morphology, and to examine whether any detected differences are in brain regions identified in earlier studies as being relevant to the phenomenology of the ASMR experience (Lochte et al., 2018, Smith et al., 2019, Smith et al., 2022. Reduced cortical thickness and complexity are typically associated with less efficient neural processing. Indeed, these cortical surface measures can reflect neuroplastic changes associated with aging (Frangou et al., 2019, Lin et al., 2021, cognition (Gautam et al., 2015), intellect and education (Im et al., 2006), and neuropsychiatric conditions (Ha et al., 2005). Importantly, differences in cortical surface measures have been shown in individuals who experience atypical conscious states similar to ASMR, with both mindfulness meditators (Kang et al., 2013) and synesthetes (Rouw et al., 2011) showing increases in cortical thickness compared with matched controls. If ASMR is associated with meditation-like benefits, we would expect to see increased cortical thickness in frontal regions. In contrast, if ASMR is associated with less efficient control of attention-as was speculated previously (Smith et al., 2019b)then reduced cortical thickness would be present in the lateral prefrontal cortex and parietal regions. Impaired attentional control may also be related to reduced sulcal depth (Voorhies et al., 2021); however, because less is known about the cognitive correlates of gyrification and sulcal depths, these analyses were exploratory in nature.

Data analysis
Data were converted from dicom to nii format in MRIcroGL (Rorden & Brett, 2000). All preprocessing and analyses were run in CAT12 (expert mode) version 12.8.1(r1987 The statistical design specification and estimation were run in CAT12. A whole-brain analysis was conducted which assessed the measures voxel-wise rather than being parcellated into regions-of-interest.
Separate analyses were run for the resampled and smoothed thickness,

RESULTS
The analysis of cortical thickness revealed several significant differences between ASMR and control participants (all p values < .001, with an extent threshold of k = 19; see Figure 1). In the left hemisphere, The analysis of cortical complexity also revealed a significant difference between groups (p < .001 and extend threshold, k = 42, applied).
ASMR was associated with significantly less cortical complexity in a 48-voxel (T = 3.7), left-hemisphere region comprising parts of the pars opercularis and pars triangularis (see Figure 2). No significant increases in cortical complexity were detected for the ASMR group as compared with the HC group.
ASMR participants also showed greater sulcal depth in a 50-voxel (T = 3.7) region of the left inferior temporal lobe and increased gyrification in a 36-voxel (T = 3.9) cluster in the right fusiform gyrus (p < .001).
However, these results were not significant when the extent threshold calculated for these maps (k = 58) was applied to correct for multiple comparisons.

DISCUSSION
The current research provides the first evidence of structural differences in the brains of individuals with ASMR. ASMR was associated with reduced cortical thickness in several areas involved with phonological processing, sensorimotor functions, and attention. Two of these regions-the precuneus and precentral gyrus-also showed atypical functional connectivity in earlier research with these participants (Smith et al., 2019b). This link between cortical thickness and atypical functional connectivity is consistent with previous research with different populations [e.g., (de la Cruz et al., 2021)].
The specific brain areas showing reduced cortical thickness are also relevant to the phenomenology of ASMR. Both the left and right supramarginal gyri were thinner in individuals sensitive to ASMR stimuli. The supramarginal gyrus is involved with a number of phonological functions including the perception of pitch and rhythm (Schaal et al., 2017) and phonological working memory (Deschamps et al., 2014). The lower cortical thickness found in the ASMR participants in our study suggests that phonological information may be processed differently by this population. This supposition is consistent with the fact that auditory stimuli such as whispering and repetitive noises can elicit ASMR tingles in these individuals [e.g., ].
Reduced cortical thickness was also detected in several regions related to movement and bodily awareness. The left precuneus is associated with a number of ASMR-relevant functions including body part localization and awareness (Felician et al., 2004), as well as perspective taking (Cavanna & Trimble, 2006, Petrini et al., 2014.  (Craig, 2009). Given that this region is a cortical "hub" with dense projections to numerous regions related to sensorimotor, attentional, and emotional processes, it is possible that the differences in cortical thickness could influence several other cognitive and emotional functions (Ghaziri et al., 2017).
Our analyses also indicated that two regions of the right prefrontal cortex were thinner in individuals with ASMR. One cluster included portions of the medial and lateral orbitofrontal cortex. This cortical region is associated with numerous sensory and emotional functions (Rolls et al., 2020); neuroimaging studies have also shown that these areas are active during some forms of social cognition (Grossmann, 2013), including an analysis of social interactions similar to those found in many ASMR videos. We also detected reduced cortical thickness in a cluster including the right superior frontal gyrus, extending into the paracentral lobule. This result is noteworthy for two reasons. First, the paracentral lobule was active when these participants viewed ASMR videos in a functional neuroimaging study (Smith et al., 2019); it is possible, therefore, that the ASMR-relevant neural activity is related to cortical thickness. Second, this brain area has also been linked with inhibitory attentional processes and to the analysis of motor urgency (Hu et al., 2016). We could therefore speculate that ASMR is related to reduced attentional inhibition. Consistent with this hypothesis, Wang et al. (2020) found that ASMR-sensitive individuals had slower inhibitory control and set-shifting abilities after exposure to ASMR videos.
The analyses of cortical complexity revealed that ASMR was associated with less complexity in regions that comprise Broca's area. This region is typically associated with language production; however, functional neuroimaging studies have shown that it serves some motoric functions as well, including the interpretation of others' actions (Fadiga et al., 2006). It is therefore possible that differential sensitivity to the social movements seen in many ASMR videos is related to differences in Broca's area. Future research could address this possibility by examining cortical complexity in ASMR-sensitive individuals who do or do not respond to this particular ASMR trigger (see Smith et al., 2020 for an examination of functional connectivity differences associated with sensitivity to different ASMR trigger types).
Although the current research provides the first investigation of structural brain differences in ASMR, it is important to acknowledge its limitations. Additional studies with larger sample sizes are necessary in order to detect further differences. Additionally, it is unclear whether the groups differed on cognitive abilities, mood, or personality variables; these factors could have weakened our ability to detect differences between the two groups of participants. Finally, this study focused on cortical brain areas. Future studies using volumetric analyses to measure subcortical structures and diffusion tensor imaging to measure white-matter pathways would allow researchers to provide a complete depiction of the neural architecture underlying ASMR.

ACKNOWLEDGMENT
This research was supported by a grant from the Natural Sciences and Engineering Research Council of Canada. The authors wish to acknowledge the helpful feedback from two anonymous reviewers.

CONFLICT OF INTEREST
This statement confirms that none of the authors report any conflict of interest related to the performance of this research.

DATA AVAILABILITY STATEMENT
Data are available from the corresponding author upon reasonable request.