The contribution of cross-modal sensory input to reaching and grasping in blind and sighted short-tailed opossums

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Abstract

Reaching and grasping are essential goal-directed behaviors that require the integration of visual, olfactory, and somatosensory inputs. Although the loss of vision can profoundly disrupt sensory-guided behaviors, mammals often exhibit compensatory cross-modal plasticity allowing them to reach and grasp with ease. To examine how early sensory loss shapes reaching behavior, we performed bilateral enucleations in short-tailed opossums ( Monodelphis domestica ) at postnatal day 4, before retino-thalamic and thalamocortical connections have formed. We assessed performance in early blind (EB) and sighted control (SC) animals using a semi-naturalistic reach-to-grasp task requiring precise unilateral limb targeting to retrieve a dead cricket. To isolate the contributions of specific sensory modalities to this task, we selectively disrupted olfactory and mystacial vibrissae inputs and manipulated lighting conditions during task performance. EB opossums were capable of accurate reaching and grasping, although SC animals outperformed EB opossums under light conditions, but not in the absence of light. Both groups relied strongly on tactile input, as whisker trimming significantly increased targeting error. Removal of olfactory input also impaired performance, with a disproportionately greater effect in EB animals. These findings demonstrate that short-tailed opossums retain functional reach-to-grasp behavior after early vision loss and that accurate forelimb movements are generated by the enhancement of the spared sensory systems.

Significance Statement

Congenital sensory loss in humans alters the landscape used to navigate the world, making compensatory strategies mediated by the spared sensory systems essential for goal-directed behaviors such as reaching and grasping. Although these behaviors have been widely studied across species, the extent to which spared senses support their execution after congenital vision loss remains unclear. Here, we use the short-tailed opossum as a model of congenital blindness to quantify the contributions of whisker-mediated touch and olfaction to reaching performance. We show that both early blind and sighted opossums rely on whisker touch for reaching and grasping, but that olfaction plays a profound role in task performance in early blind opossums.

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