Action does not enhance but attenuates predicted touch

Abstract

Dominant motor control theories propose that the brain uses efferent information to predict and attenuate the somatosensory consequences of actions, referred to as sensory attenuation. Support for this model comes from psychophysical and neuroimaging studies showing that touch applied on a passive hand elicits attenuated perceptual and neural responses if it is generated by actively tapping with one's other hand, compared to identical touch from an external origin. However, recent experimental findings have challenged this view by providing psychophysical evidence that the perceived intensity of touch on the passive hand is enhanced if the active hand does not receive simultaneous tactile stimulation with the passive hand (somatosensory enhancement) and by further attributing attenuation effects to the double tactile stimulation of the hands upon contact. Here, we directly contrasted the hypotheses of the attenuation and enhancement models regarding how action influences somatosensory perception by manipulating whether the active hand contacts the passive hand. In three preregistered experiments, we demonstrate that action does not enhance the perceived intensity of touch (Experiment 1), that the previously reported "enhancement" effects are driven by the baseline condition used (Experiment 2), and that self-generated touch is robustly attenuated regardless of whether the two hands make contact (Experiment 3). Our results provide conclusive evidence that action does not enhance but attenuates predicted touch. These findings prompt a reappraisal of recent experimental findings upon which theoretical frameworks proposing a perceptual enhancement by action prediction are based.

Dynamic changes in somatosensory and cerebellar activity mediate temporal recalibration of self-touch

“…Neither the percentages of the delayed or nondelayed trials per se can account for our results, as in both sessions, we modeled the less frequent touches that had an identical number of appearances ( i.e. , 12%) and differences between delayed and nondelayed self-generated touches have been previously observed in experimental contexts where predicted and unpredicted touches are equiprobable (50%-50%) 55,65 .…”

“…The 50 response trials enabled us to collect perceptual responses and included a two-alternative forced-choice force-discrimination task (Figure 3) that has previously been used to quantify somatosensory perception 46,51,[53][54][55]58,59,65,66,68 , including during delay adaptation 46 . Each response trial was preceded by five delayed (Figure 3a, top, purple) or nondelayed (Figure 3b, bottom, orange) self-generated touches depending on the session.…”

Aging exerts a limited influence on the perception of self-generated and externally generated touch

“…The psychophysical task was a two-alternative forced choice (2AFC) force-discrimination task that has been used by numerous studies investigating somatosensory attenuation ( 22 – 25 , 27 , 32 – 34 , 38 ).…”

“…These predictions allow the brain to estimate the expected sensory feedback without relying on the actual sensory feedback, which suffers from intrinsic delays ( 20 , 46 , 49 – 51 ), and to integrate it with the received sensory signals to improve the estimation of the state of the body ( 51 ). Action prediction signals also serve to attenuate the expected self-generated sensations ( 24 , 27 ), thereby increasing the salience and prioritizing the processing of unexpected externally generated sensations that might be more behaviorally relevant ( 20 , 21 , 36 , 48 ). Within a Bayesian integration framework, somatosensory attenuation relies on the integration of the forward model’s predictions and the somatosensory information, with both sources of information weighted based on their relative reliability ( 52 , 53 ).…”

“…In the present study, we chose not to include the force-matching task and instead used the force-discrimination task, a well-established psychophysical test that has been previously used to assess somatosensory attenuation ( 22 – 25 , 27 , 32 – 35 , 38 ). In the force-discrimination task, participants receive two forces on their finger and are asked to indicate which force felt stronger.…”