Malin Björnsdotter

Somatotopic organization of gentle touch processing in the posterior insular cortex.

A network of thin (C and Aδ) afferents relays various signals related to the physiological condition of the body, including sensations of gentle touch, pain, and temperature changes. Such afferents project to the insular cortex, where a somatotopic organization of responses to noxious and cooling stimuli was recently observed. To explore the possibility of a corresponding body-map topography in relation to gentle touch mediated through C tactile (CT) fibers, we applied soft brush stimuli to the right forearm and thigh of a patient (GL) lacking Aβ afferents, and six healthy subjects during functional magnetic resonance imaging (fMRI). For improved fMRI analysis, we used a highly sensitive multivariate voxel clustering approach. A somatotopic organization of the left (contralateral) posterior insular cortex was consistently demonstrated in all subjects, including GL, with forearm projecting anterior to thigh stimulation. Also, despite denying any sense of touch in daily life, GL correctly localized 97% of the stimuli to the forearm or thigh in a forced-choice paradigm. The consistency in activation patterns across GL and the healthy subjects suggests that the identified organization reflects the central projection of CT fibers. Moreover, substantial similarities of the presently observed insular activation with that described for noxious and cooling stimuli solidify the hypothesized sensory-affective role of the CT system in the maintenance of physical well-being as part of a thin-afferent homeostatic network.

Feeling good: on the role of C fiber mediated touch in interoception

The human skin is innervated by a network of thin, slow-conducting afferent (C and Aδ) fibers, transmitting a diverse range of information. Classically, these fibers are described as thermo-, noci- or chemoreceptive, whereas mechanoreception is attributed exclusively to thick, fast-conducting (Aβ) afferents. A growing body of evidence, however, supports the notion that C tactile afferents comprise a second anatomically and functionally distinct system signaling touch in humans. This review discusses established as well as recent findings which highlight fundamental differences in peripheral and central information coding and processing between Aβ and C mechanoreception. We conclude that from the skin through the brain, C touch shares more characteristics with interoceptive modalities (e.g. pain, temperature, and itch) than exteroceptive Aβ touch, vision or hearing. In this light, we discuss the motivational-affective role of C touch as an integral part of a thin-fiber afferent homeostatic network for the maintenance of physical and social well-being.

Altered C-tactile processing in human dynamic tactile allodynia

Summary Psychophysical and fMRI findings suggest reduced C‐tactile mediated hedonic processing in tactile allodynia. However, Aβ signaling is required for the perception of allodynic pain. ABSTRACT Human unmyelinated (C) tactile afferents signal the pleasantness of gentle skin stroking on hairy (nonglabrous) skin. After neuronal injury, that same type of touch can elicit unpleasant sensations: tactile allodynia. The prevailing pathophysiological explanation is a spinal cord sensitization, triggered by nerve injury, which enables Aβ afferents to access pain pathways. However, a recent mouse knockout study demonstrates that C‐tactile afferents are necessary for allodynia to develop, suggesting a role for not only Aβ but also C‐tactile afferent signaling. To examine the contribution of C‐tactile afferents to the allodynic condition in humans, we applied the heat/capsaicin model of tactile allodynia in 43 healthy subjects and in 2 sensory neuronopathy patients lacking Aβ afferents. Healthy subjects reported tactile‐evoked pain, whereas the patients did not. Instead, patients reported their C‐touch percept (faint sensation of pleasant touch) to be significantly weaker in the allodynic zone compared to untreated skin. Functional magnetic resonance imaging in 18 healthy subjects and in 1 scanned patient indicated that stroking in the allodynic and control zones evoked different responses in the primary cortical receiving area for thin fiber signaling, the posterior insular cortex. In addition, reduced activation in the medial prefrontal cortices, key areas for C‐tactile hedonic processing, was identified. These findings suggest that dynamic tactile allodynia is associated with reduced C‐tactile mediated hedonic touch processing. Nevertheless, because the patients did not develop allodynic pain, this seems dependent on Aβ signaling, at least under these experimental conditions.

Development of brain mechanisms for processing affective touch

Affective tactile stimulation plays a key role in the maturation of neural circuits, but the development of brain mechanisms processing touch is poorly understood. We therefore used functional magnetic resonance imaging (fMRI) to study brain responses to soft brush stroking of both glabrous (palm) and hairy (forearm) skin in healthy children (5–13 years), adolescents (14–17 years), and adults (25–35 years). Adult-defined regions-of-interests in the primary somatosensory cortex (SI), secondary somatosensory cortex (SII), insular cortex and right posterior superior temporal sulcus (pSTS) were significantly and similarly activated in all age groups. Whole-brain analyses revealed that responses in the ipsilateral SII were positively correlated with age in both genders, and that responses in bilateral regions near the pSTS correlated significantly and strongly with age in females but not in males. These results suggest that brain mechanisms associated with both sensory-discriminative and affective-motivational aspects of touch are largely established in school-aged children, and that there is a general continuing maturation of SII and a female-specific increase in pSTS sensitivity with age. Our work establishes a groundwork for future comparative studies of tactile processing in developmental disorders characterized by disrupted social perception such as autism.

Patterns of neural activity in the human ventral premotor cortex reflect a whole-body multisensory percept.

Previous research has shown that the integration of multisensory signals from the body in fronto-parietal association areas underlies the perception of a body part as belonging to ones physical self. What are the neural mechanisms that enable the perception of ones entire body as a unified entity? In one behavioral and one fMRI multivoxel pattern analysis experiment, we used a full-body illusion to investigate how congruent visuo-tactile signals from a single body part facilitate the emergence of the sense of ownership of the entire body. To elicit this illusion, participants viewed the body of a mannequin from the first-person perspective via head-mounted displays while synchronous touches were applied to the hand, abdomen, or leg of the bodies of the participant and the mannequin; asynchronous visuo-tactile stimuli served as controls. The psychometric data indicated that the participants perceived ownership of the entire artificial body regardless of the body segment that received the synchronous visuo-tactile stimuli. Based on multivoxel pattern analysis, we found that the neural responses in the left ventral premotor cortex displayed illusion-specific activity patterns that generalized across all tested pairs of body parts. Crucially, a tripartite generalization analysis revealed the whole-body specificity of these premotor activity patterns. Finally, we also identified multivoxel patterns in the premotor, intraparietal, and lateral occipital cortices and in the putamen that reflected multisensory responses specific to individual body parts. Based on these results, we propose that the dynamic formation of a whole-body percept may be mediated by neuronal populations in the ventral premotor cortex that contain visuo-tactile receptive fields encompassing multiple body segments.

Posterior Superior Temporal Sulcus Responses Predict Perceived Pleasantness of Skin Stroking

Love and affection is expressed through a range of physically intimate gestures, including caresses. Recent studies suggest that posterior temporal lobe areas typically associated with visual processing of social cues also respond to interpersonal touch. Here, we asked whether these areas are selective to caress-like skin stroking. We collected functional magnetic resonance imaging data from 23 healthy participants and compared brain responses to skin stroking and vibration. We did not find any significant differences between stroking and vibration in the posterior temporal lobe; however, right posterior superior temporal sulcus (pSTS) responses predicted healthy participant’s perceived pleasantness of skin stroking, but not vibration. These findings link right pSTS responses to individual variability in perceived pleasantness of caress-like tactile stimuli. We speculate that the right pSTS may play a role in the translation of tactile stimuli into positively valenced, socially relevant interpersonal touch and that this system may be affected in disorders associated with impaired attachment.

Evaluation of Quantified Social Perception Circuit Activity as a Neurobiological Marker of Autism Spectrum Disorder.

IMPORTANCE Autism spectrum disorder (ASD) is marked by social disability and is associated with dysfunction in brain circuits supporting social cue perception. The degree to which neural functioning reflects individual-level behavioral phenotype is unclear, slowing the search for functional neuroimaging biomarkers of ASD. OBJECTIVE To examine whether quantified neural function in social perception circuits may serve as an individual-level marker of ASD in children and adolescents. DESIGN, SETTING, AND PARTICIPANTS The cohort study was conducted at the Yale Child Study Center and involved children and adolescents diagnosed as having ASD and typically developing participants. Participants included a discovery cohort and a larger replication cohort. Individual-level social perception circuit functioning was assessed as functional magnetic resonance imaging brain responses to point-light displays of coherent vs scrambled human motion. MAIN OUTCOMES AND MEASURES Outcome measures included performance of quantified brain responses in affected male and female participants in terms of area under the receiver operating characteristic curve (AUC), sensitivity and specificity, and correlations between brain responses and social behavior. RESULTS Of the 39 participants in the discovery cohort aged 4 to 17 years, 22 had ASD and 30 were boys. Of the 75 participants in the replication cohort aged 7 to 20 years, 37 had ASD and 52 were boys. A relative reduction in social perception circuit responses was identified in discovery cohort boys with ASD at an AUC of 0.75 (95% CI, 0.52-0.89; P = .01); however, typically developing girls and girls with ASD could not be distinguished (P = .54). The results were confirmed in the replication cohort, where brain responses were identified in boys with ASD at an AUC of 0.79 (95% CI, 0.64-0.91; P < .001) and failed to distinguish affected and unaffected girls (P = .82). Across both cohorts, boys were identified at an AUC of 0.77 (95% CI, 0.64-0.86) with corresponding sensitivity and specificity of 76% each. Additionally, brain responses were associated with social behavior in boys but not in girls. CONCLUSIONS AND RELEVANCE Quantified social perception circuit activity is a promising individual-level candidate neural marker of the male ASD behavioral phenotype. Our findings highlight the need to better understand effects of sex on social perception processing in relation to ASD phenotype manifestations.

Neural correlates of gentle skin stroking in early infancy

Highlights • The infant brain is sensitive to gentle skin stroking within the first weeks of age.• The postcentral gyrus and posterior insular cortex are responsive to stroking.• Social touch activates both somatosensory and socio-affective brain areas in infancy.

Decoding illusory self-location from activity in the human hippocampus

Decades of research have demonstrated a role for the hippocampus in spatial navigation and episodic and spatial memory. However, empirical evidence linking hippocampal activity to the perceptual experience of being physically located at a particular place in the environment is lacking. In this study, we used a multisensory out-of-body illusion to perceptually ‘teleport’ six healthy participants between two different locations in the scanner room during high-resolution functional magnetic resonance imaging (fMRI). The participants were fitted with MRI-compatible head-mounted displays that changed their first-person visual perspective to that of a pair of cameras placed in one of two corners of the scanner room. To elicit the illusion of being physically located in this position, we delivered synchronous visuo-tactile stimulation in the form of an object moving toward the cameras coupled with touches applied to the participant’s chest. Asynchronous visuo-tactile stimulation did not induce the illusion and served as a control condition. We found that illusory self-location could be successfully decoded from patterns of activity in the hippocampus in all of the participants in the synchronous (P < 0.05) but not in the asynchronous condition (P > 0.05). At the group-level, the decoding accuracy was significantly higher in the synchronous than in the asynchronous condition (P = 0.012). These findings associate hippocampal activity with the perceived location of the bodily self in space, which suggests that the human hippocampus is involved not only in spatial navigation and memory but also in the construction of our sense of bodily self-location.

A Memetic Algorithm for Selection of 3D Clustered Features with Applications in Neuroscience

We propose a Memetic algorithm for feature selection in volumetric data containing spatially distributed clusters of informative features, typically encountered in neuroscience applications. The proposed method complements a conventional genetic algorithm with a local search utilizing inherent spatial relationships to efficiently identify informative feature clusters across multiple regions of the search volume. First, we demonstrate the utility of the algorithm on simulated data containing informative feature clusters of varying contrast-to-noise-ratios. The Memetic algorithm identified a majority of the relevant features whereas a conventional genetic algorithm detected only a subset sufficient for fitness maximization. Second, we applied the algorithm to authentic functional magnetic resonance imaging (fMRI) brain activity data from a motor task study, where the Memetic algorithm identified expected brain regions and subsequent brain activity prediction in new individuals was accurate at an average of 76% correct classification. The proposed algorithm constitutes a novel method for efficient volumetric feature selection and is applicable in any 3D data scenario. In particular, the algorithm is a promising alternative for sensitive brain activity mapping and decoding.