Use-dependent plasticity of cortical proprioceptive representation in mice

Proprioception enables an organism to sense the position and motion of its limbs and body in space. Comparative evolutionary studies have proposed that the organization of the proprioceptive cortex does not emerge as a consequence of innervation density but rather as a result of the actual use of a limb. We tested this hypothesis by quantifying if and how the proprioceptive cortical representation reorganizes after skilled motor training in adult mice as well as enriched environmental exposure during development.We performed wide-filed calcium imaging of cortical activation in response to multi-joint proprioceptive stimulation of the mouse forelimb. Our results indicate that proprioceptive sensory maps in the mouse cortex are plastic and can be reorganized by extensive limb use. Adult mice trained in a forelimb reach-to-grasp task (30 sessions, ~400 reaches/session), as well as mice raised in an enriched environment from P20 showed broadened cortical proprioceptive activation relative to controls. We specifically observed a medial extension of the proprioceptive map from the somatosensory (fS1) towards the caudal motor forelimb area (CFA). Surprisingly, longitudinal tracking of single cell activity with two-photon microscopy showed very stable tuning of proprioceptive responses in both control and trained mice.Our findings provide direct experimental support for motor experience sculpting cortical proprioceptive representations. Plasticity seems to occur in the form of additional cortical neurons gaining proprioceptive responses rather than by shaping the tuning properties of existing ones.