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Self and others in the sensorimotor system: a computational neuroanatomy of sensory attenuation

Periodic Reporting for period 1 - TICKLE ME (Self and others in the sensorimotor system: a computational neuroanatomy of sensory attenuation)

Período documentado: 2017-01-01 hasta 2018-12-31

Try to tickle yourself. No matter how hard you try, the resulting sensation will always feel less ticklish and less intense compared to the sensation produced by somebody else tickling you. Since the early 70s, several behavioural studies have shown that self-generated touch – as when touching our hand with the other– feels systematically less intense and less ticklish compared to touch of the exact same intensity and frequency applied to our hand but generated by another person or machine. Sensory attenuation (SA) refers to this phenomenon and TICKLEME was an EU project funded by the Marie Skłodowska-Curie actions that aimed to a better computational and neuroanatomical understanding of SA.

From a computational perspective, prevalent theories of motor control have proposed that SA is due to the ability of our brain to predict the sensory feedback of our movements. That is, when we move one hand to touch (or tickle) the other, our brain predicts that our two hands will get in contact and thus, tactile sensations are expected. Consequently, when we perform the movement and we touch our hands, the received touch feels less intense because it has been predicted. In contrast, externally generated touch cannot be predicted and therefore it is not attenuated. However, how and when the brain computes these tactile predictions remains unknown. From a neuroanatomical perspective, earlier neuroimaging studies on SA have provided conflicting results about which brain areas are involved in the phenomenon and the pattern of their activations. Consequently, we know too little about the brain processes that are responsible for SA.

TICKLEME had three objectives:
1. to clarify (a) whether an active movement is necessary for SA, (b) whether mental simulation of a movement would be sufficient for SA and (c) whether an illusion of having the two hands in contact –while they are physically distant– would elicit SA.
2. to identify the brain areas that are involved in SA by studying the brain activation and brain connectivity in relation to the participants’ perception.
3. to study whether a prolonged experience of delays between a movement and its tactile feedback can reverse SA and make self-generated touch feel more intense.

By understanding when and how the brain computes these movement-related tactile predictions, TICKLEME was expected to bring novel insights into the human motor control field in general. Moreover, SA was shown to be reduced in schizophrenic patients that report auditory hallucinations (i.e. the patients hear ‘voices’) or delusions of control (i.e. the patients report that their actions are controlled by external forces). Therefore, TICKLEME was expected to show strong clinical relevance, since understanding the SA mechanism within the healthy population could substantially benefit our understanding about which processes are disturbed in the schizophrenic brain.
During the reporting period, we conducted all experiments described in the three work packages of the research proposal. We further conducted few additional experiments to address related research questions that were raised during the project.

In summary, TICKLEME has demonstrated so far that:
1. when using a hand-held tool to apply forces on the body, participants show the same level of attenuation as when using their own finger to touch their body (Kilteni and Ehrsson, 2017b).
2. participants can attenuate forces generated by a fake hand that feels like their own right hand, when this is under control and seen to press on their left hand (Kilteni and Ehrsson, 2017a). Critically, SA depends on the strength of the illusion: the more participants experience the fake hand as their own hand, the stronger is SA.
3. when we imagine (and not execute) a movement that would produce touch if executed, we attenuate simultaneously applied real tactile stimulation (Kilteni et al., 2018a).
4. the functional connectivity between the cerebellum and the somatosensory cortex may constitute the mechanism of SA (Kilteni and Ehrsson, in preparation).
5. systematic exposure to delays between our movements and their somatosensory feedback recalibrate the brain’s predictive processes to attenuate delayed somatosensory feedback (Kilteni et al., 2018b).

The results of TICKLEME were disseminated in three (3) scientific publications while two (2) others are in preparation/submitted, seven (7) invited oral presentations at academic institutions and eight (8) oral and poster presentations at international conferences and workshops.

The public engagement actions of TICKLEME included serving as Marie Skłodowska-Curie Ambassador, performing lab demonstrations for undergraduate students, organizing a press release for the findings of the project, conducting experimental demonstrations during the European Researchers’ Friday and being interviewed in the National Swedish radio for the findings of the project.

References
Kilteni, K., Andersson, B. J., Houborg, C., and Ehrsson, H. H. (2018a). Motor imagery involves predicting the sensory consequences of the imagined movement. Nat. Commun. 9, 1617. doi:10.1038/s41467-018-03989-0.
Kilteni, K., and Ehrsson, H. (in preparation). Functional connectivity between cerebellum and somatosensory areas reflects the attenuation of self-generated touch.
Kilteni, K., and Ehrsson, H. H. (2017a). Body ownership determines the attenuation of self-generated tactile sensations. Proc. Natl. Acad. Sci., 201703347. doi:10.1073/PNAS.1703347114.
Kilteni, K., and Ehrsson, H. H. (2017b). Sensorimotor predictions and tool use: Hand-held tools attenuate self-touch. Cognition 165, 1–9. doi:10.1016/j.cognition.2017.04.005.
Kilteni, K., Houborg, C., and Ehrsson, H. H. (2018b). Rapid learning and unlearning of sensory delays in self-touch. in Society for Neuroscience (San Diego, CA).
The impact of the project findings was significant and concerned both the computational and neuroanatomical understanding of SA.

Specifically, our findings on
1. SA and hand-held tools are important because they suggest that during tool use, the brain treats the tool as an extension of the finger. That is, when we hold a tool, the brain computes the tactile predictions based on the tip of the tool and not our finger.
2. SA and the fake hand demonstrate that when computing the tactile predictions, the brain considers the state of the body that is currently experienced.
3. SA and mental simulation of a movement bring novel evidence that the predictive processes in the brain can operate offline, in the absence of overt movements. This result has important implications for motor learning and rehabilitation, because it explains why mental rehearsal is a popular strategy amongst elite athletes and professional musicians, and suggests that motor imagery could be beneficial for the motor rehabilitation of neurological patients that cannot move.
4. the neuroanatomical correlates of SA are important because they reveal the key role of the cerebellum in predicting self-generated somatosensory input and communicating its predictions to the somatosensory cortex.
5. sensorimotor delays and SA bring novel evidence that the brain can dynamically adjust its predictions to the given environmental statistics. Moreover, this result has important clinical relevance since recent findings have shown that schizophrenic patients attenuate delayed but not immediate self-generated auditory stimuli.