DOI: 10.1371/journal.pone.0358656 ISSN: 1932-6203

Distinct prior expectations shape tactile and proprioceptive localization

Hüseyin O. Elmas, W. Pieter Medendorp, Luke E. Miller

When a mosquito lands on your finger, swatting it away requires your brain to calculate its location in external space, which depends on the body’s 3D posture. Two competing hypotheses explain how the brain solves this challenge: the integration hypothesis , where tactile signals are transformed into spatial coordinates by integrating touch and posture information; and the cueing hypothesis , where touch merely cues a location on the body whose position is specified via proprioception. Adjudicating between these hypotheses is nearly impossible without modeling the latent factors underlying somatosensory spatial perception. We fill this gap in the present study. We first formalized each hypothesis from a Bayesian perspective: If touch merely triggers proprioceptive localization (cueing hypothesis), tactile and proprioceptive localization should rely on the same Bayesian computations, with identical prior expectations about the mosquito’s spatial location; If they involve distinct Bayesian computational processes (integration hypothesis), distinct prior expectations may shape tactile and proprioceptive localization. To test these predictions, we had nineteen participants localize either proprioceptive or tactile targets on their fingertips. We then fit their data with several Bayesian models of each hypothesis. Models allowing different prior distributions between modalities provided the best fit for most participants, with 15 out of 19 participants showing significantly different prior distributions across modalities. These provide strong computational evidence that tactile and proprioceptive localization rely on distinct computational mechanisms, a conclusion that has important implications for how we understand these everyday behaviors and their neural mechanisms.