Neural dynamics of illusory tactile pulling sensations

Abstract

The sensation of directional forces and their associated sensorimotor commands are inextricably intertwined, complicating the identification of brain circuits responsible for tactile pulling sensations. One hypothesis is that, like tactile frequency discrimination, pulling sensations are generated by early sensory-frontal activity. Alternatively, they may be generated later in the somatosensory association cortex. To dissociate these accounts and uncouple the pulling sensation from unrelated but correlated sensory and motor processing, we combined high-density EEG with an oddball paradigm and asymmetric vibration, which creates an illusory sensation of the hand being directionally pulled. Oddballs that created a pulling sensation in the opposite direction to common stimuli were compared to the same oddballs in the context of neutral common stimuli (symmetric vibration) and to neutral oddballs. Brain responses to having directional pulling expectations violated by directional stimuli were therefore isolated. Contrary to the sensory-frontal account, frontal N140 brain activity was actually larger for neutral than pulling oddballs. Instead, pulling sensations were associated with amplitude and latency modulations of midline P200 and P3b potentials, and specifically, to contralateral parietal lobe activity 280ms post-stimulus. The timing of this activity suggested pulling sensations involve spatial processing, such as tactile remapping between coordinate frames. Source localization showed this activity to be centered on the postcentral sulcus, superior parietal lobule and intraparietal sulcus, suggesting that pulling sensations arise via the processing of body position, tactile orientation and peripersonal space. Our results demonstrate how tactile illusions can uniquely disambiguate parietal contributions to somatosensation by removing unrelated sensory processing. Significance statementThe neural mechanisms of tactile pulling sensations are poorly understood. Competing early sensory-frontal and later somatosensory association cortex accounts are hard to dissociate due to confounding sensory and motor signals present when forces are applied to the skin. Here, we used EEG and a novel asymmetric vibration approach to induce an illusory pulling sensation, which circumvents these issues. We found that pulling sensations were associated with parietal lobe activity 280ms post-stimulus and modulations of the P200. The timing and location of this activity suggested that pulling sensations necessitate spatial processing and supported a somatosensory association cortex account of the pulling sensation.