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Perception in Action: Neural Dynamics of Sensorimotor Interactions in Touch

Periodic Reporting for period 1 - SELF-TOUCH (Perception in Action: Neural Dynamics of Sensorimotor Interactions in Touch)

Reporting period: 2022-06-01 to 2024-05-31

The brain has an extraordinary ability to swiftly distinguish between self-generated and externally generated sensations. The key to this ability is the brain’s strategy of predicting future sensory information in real-time. During self-touch, before your body parts even make contact, information about when and where the touch will occur is precisely predicted from your motor command. This prediction allows the brain to safely ignore sensations that are caused by your own actions. The predictive attenuation of self-generated sensations is referred to as sensory attenuation (SA) and it’s thought to be the reason why you do not relentlessly startle or tickle yourself when you often touch your skin. Current neurobiological theories propose that when prediction mechanisms fail it can have powerful consequences for our perception, from mild perceptual disturbances to more extreme hallucinations and delusions that are characteristic of psychotic episodes in schizophrenia. Thus, accurately predicting the future allows the brain to construct a coherent representation of the present. Predicting the sensory consequences of our actions requires temporally dynamic neural mechanisms that modulate the perception of our touch with millisecond-level precision; however, very little is known about how these mechanisms operate in the brain. Predicted tactile sensations are likely signaled via specific neural oscillations, which are known to subserve brain connectivity, within a well-defined network. A proper understanding of the temporal dynamics underlying the prediction of self-generated sensations could reveal how perceptual disturbances manifest in psychosis and may be important for the development of biomarkers for early intervention in the prodromal phase of schizophrenia.

The “SELF-TOUCH” project builds upon well-established models of motor control with systematic behavioural and neuroimaging experiments benefitting from millisecond-level temporal precision. The project’s objectives are:

Objective 1: To elucidate how the brain dynamically predicts tactile sensations during the time-course of self-touch.
Objective 2: To investigate how the brain treats violations of these predictions.
Objective 3: To examine how these predictive mechanisms operate in relation to trait schizotypy.
The SELF-TOUCH project has achieved its objectives for the first 24-month period including the collection of behavioural, neuroimaging (MEG and MRI) and trait schizotypy datasets in addition to several highly complementary studies arising from fruitful collaborations. The main work performed and associated results are summarised below:

1. Behavioural results have replicated previous demonstrations that self-touch is perceived as weaker than externally generated touch, but with important additional controls. Specifically, unlike the previous studies we included a control condition in which the same action was performed, that elicited an identical tactile stimulus, but a spatial separation between the action and its sensory consequence was introduced. A spatial separation condition controls for time-locked movement and touch of the active hand which is not possible when comparing only externally generated and self-generated touch conditions. Furthermore, a spatial separation control condition is also matched in the temporal predictability of the stimulus, divided attention between the two hands, and the dual-task requirement of the self-generated condition, all of which are not matched in externally generated touch conditions. The results demonstrate that self-touch is perceptually attenuated and rules out the confounds associated with the previous research.

2. The results show that neural responses in the primary somatosensory cortex are attenuated for self-generated touch compared to externally generated touch and compared to a control condition in which the same action is performed, but a spatial separation between the hands is introduced. This is the first demonstration, to our knowledge, of early neural somatosensory attenuation that cannot be explained by confounds associated with comparing only self-generated touch to externally generated touch.

3. The results also indicate that modulations of oscillations reflect the prediction of self-generated touch and that connectivity between key brain areas including the somatosensory cortex and the cerebellum may mediate predictions during self-touch.

4. Violating expectations of self-generated touch by unexpectedly omitting the stimulus results in a (prediction-related) signal over somatosensory areas following the omitted stimulus, which may directly reflect predictive signals in the brain.

These results are currently being investigated with respect to the participant's schizotypal personality traits to elucidate how individuals who are low versus high on schizotypal personality traits predict and process self-generated touch. Manuscripts are currently in preparation for a comprehensive dissemination of the findings.

In addition to the main work performed, highly complementary behavioural research was also performed by the fellow in collaborations including i) research challenging recent theoretical accounts of prediction during self-touch (Job & Kilteni, 2023), ii) research showing that the positive dimension of schizotypy is associated with reduced attenuation and precision of self-generated touch (Asimakidou, Job & Kilteni, 2022), ii) research investigating the perception of self-generated touch in healthy ageing (Timar, Job, Orban de Xivry & Kilteni (2023) and iv) research investigating the temporal tuning of somatosensory perception during self-touch.
The SELF-TOUCH project went beyond the state-of-the-art. The findings provide a better understanding of how the human brain dynamically predicts and determines the causes of sensory information. This knowledge is important for testing and updating current neurobiological models of perceptual prediction and motor control. We anticipate the results will have an important impact in the fields of somatosensation, predictive processing, motor control, and computational psychiatry more widely.

Furthermore, the findings may impact our current understanding of how disruptions of predictive processing in the brain operate in individuals with high schizotypal traits, a population thought to be at increased risk for schizophrenia. This knowledge may have important future societal impact by aiding in the development of novel bio-behavioral markers for early intervention in schizophrenia. Given that schizophrenia is one of the top 15 leading causes of disability worldwide and the financial costs associated with with schizophrenia are disproportionately high relative to other chronic mental and physical health conditions, far-reaching economic impact could be achieved through the ability to identify and intervene early in the pathogenesis of the disorder.
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