No evidence for somatosensory attenuation during action observation of self-touch

Abstract

The discovery of mirror neurons in the macaque brain in the 1990s triggered investigations on putative human mirror neurons and their potential functionality. The leading proposed function has been action understanding: accordingly, we understand the actions of others by simulating them in our own motor system through a direct matching of the visual information to our own motor programs. Furthermore, it has been proposed that this simulation involves the prediction of the sensory consequences of the observed action, similar to the prediction of the sensory consequences of our executed actions. Here, we tested this proposal by quantifying somatosensory attenuation behaviorally during action observation. Somatosensory attenuation manifests during voluntary action and refers to the perception of self-generated touches as less intense than identical externally generated touches because the self-generated touches are predicted from the motor command. Therefore, we reasoned that if an observer simulates the observed action and, thus, he/she predicts its somatosensory consequences, then he/she should attenuate tactile stimuli simultaneously delivered to his/her corresponding body part. In three separate experiments, we found a systematic attenuation of touches during executed self-touch actions, but we found no evidence for attenuation when such actions were observed. Failure to observe somatosensory attenuation during observation of self-touch is not compatible with the hypothesis that the putative human mirror neuron system automatically simulates the observed action. In contrast, our findings emphasize a sharp distinction between the motor representations of self and others.

Predictive attenuation of touch and tactile gating are distinct perceptual phenomena

“…First, previous studies have shown that double touch is not sufficient to produce somatosensory attenuation. For example, when both index fingers are simultaneously tapped (bimanual stimulation) in the absence of any movement ( 2 ) or in the presence of a passive movement ( 11 ), somatosensory attenuation does not occur. Similarly, when participants perform the force-matching task or the force discrimination task (as in the present study) and thus receive bimanual tactile stimulation, but a distance or a spatial mismatch is introduced between their hands/fingers, the attenuation is substantially reduced ( 7, 14, 112 ) or not present ( 6, 113 ).…”

“…In all conditions, the comparison tap was delivered on the left index finger with a random delay of 800-1500 ms from the test tap. We opted to present the test tap before the comparison tap (fixed order design), consistent with previous studies ( 2, 4, 10, 11 ), to maintain the delay between the two taps constant across conditions and remove any effect of the comparison tap on the tap participants had to perform with their right index finger. For example, if the participants first received a 3 N comparison tap, they might press stronger to generate the subsequent test tap.…”

“…Several experimental studies in humans have shown that the brain attenuates somatosensory reafference (i.e., all somatosensory inputs generated by one’s own movement, including inputs originating directly from the moving body part and inputs from other passive body parts being touched) compared to exafference. In behavioral research, this process refers to participants perceiving self-generated strokes, forces, or taps as weaker than external equivalents of the same intensity ( 1, 2, 11, 3 – 10 ). This somatosensory attenuation is related to reduced activity in the secondary somatosensory cortex ( 12 – 14 ) and the cerebellum ( 12, 14, 15 ) and increased connectivity between the two areas ( 14, 16 ) during self-generated touches compared to externally generated touches.…”

The positive dimension of schizotypy is associated with a reduced attenuation and precision of self-generated touch

“…The psychophysical paradigm was a two-alternative forced choice force-discrimination task that has been extensively used to assess somatosensory attenuation (Bays et al, 2006(Bays et al, , 2005Kilteni et al, 2021Kilteni et al, , 2020Kilteni et al, , 2019Kilteni and Ehrsson, 2020b). Participants sat comfortably on a chair and rested their left hand, palm up, with the left index finger placed inside a molded support (Figure 1).…”

“…Moreover, the brain uses these predictions to attenuate the intensity of the self-generated signals, thereby amplifying the difference between self-generated and externally generated information (Bäß et al, 2008;Blakemore et al, 2000b;Gentsch and Schütz-Bosbach, 2011;Kilteni et al, 2020). In the tactile domain, this attenuation manifests in perceiving self-generated touch as being weaker than externally generated touch of the same intensity (Bays et al, 2005;Bays and Wolpert, 2008;Sarah Jayne Blakemore et al, 1999;Kilteni et al, 2021Kilteni et al, , 2020Kilteni et al, , 2018Kilteni and Ehrsson, 2020b, 2020a, 2017a, 2017bLalouni et al, 2020;Shergill et al, 2003) and in yielding weaker activity in the secondary somatosensory cortex and the cerebellum (Blakemore et al, 1998;Kilteni and Ehrsson, 2020a) and increased functional connectivity between the two areas (Kilteni and Ehrsson, 2020a). Somatosensory attenuation has been shown across a wide age range (18-88 years old) (Wolpe et al, 2016), and it is considered one of the reasons why we cannot tickle ourselves (Blakemore et al, 2000b;Leavens and Bard, 2016;Weiskrantz, L., Elliot, J.…”