Peripersonal encoding of forelimb proprioception in the mouse somatosensory cortex

Abstract

Conscious perception of limb movements depends on proprioceptive neural responses in the somatosensory cortex. In contrast to tactile sensations, proprioceptive cortical coding is barely studied in the mammalian brain and practically non-existent in rodent research. To understand the cortical representation of this important sensory modality we developed a passive forelimb displacement paradigm in behaving mice and also trained them to perceptually discriminate where their limb is moved in space. We delineated the rodent proprioceptive cortex with wide-field calcium imaging and optogenetic silencing experiments during behavior. Our results reveal that proprioception is represented in both sensory and motor cortical areas. In addition, behavioral measurements and responses of layer 2/3 neurons imaged with two-photon microscopy reveal that passive limb movements are both perceived and encoded in the mouse cortex as a spatial direction vector that interfaces the limb with the body’s peripersonal space.

An output-null signature of inertial load in motor cortex

“…Because muscle activity during load compensation was unchanged by cortical inactivation, we conclude this load-related signal is not a motor command underlying the compensation, but is instead a latent, output-null representation. Our finding that activity along the load dimension is minimally influenced by cerebellar perturbation further suggests it is not driven primarily by cerebellar projections through the ventrolateral thalamus, but may reflect sensory signals ascending from the dorsal column nuclei via somatosensory cortex 51 or a more abstract contextual signal from other cortical regions. This output-null representation of load may support the generation of appropriately-scaled commands when a voluntary, corticallydependent gait modification must be integrated with the spinally-generated locomotor program.…”

Exploration biases forelimb reaching strategies

“…We considered that the bias of showing direction and not endpoint responses during the probe test could have been confounded by insensitivity to the new start positions, as detected through proprioception. However, mice have been shown to reliably discriminate passive forelimb deviations of only 2 mm, 73 and our probe start positions were ~5.5 mm away from the original start. We are confident that animals rely on proprioception in our task because animals performed the task in the dark and performance was unchanged without whiskers.…”

“…Our task shares features with previous tasks for mice 51 , 52 , 56 , 58 – 61 , 63 , 72 that used SCARA joysticks 52 , 59 – 61 , 72 , 73 or spatial reward zones, 52 , 56 , 59 , 63 and expands on these studies in key aspects: (1) The perched posture in the cup allowed animals to increase workspace exploration. (2) Continuous movements with the joystick were not guided by motors or spring forces.…”