Developmental plasticity of texture discrimination following early vision loss in the marsupialMonodelphis domestica

Abstract

Behavioral strategies that depend on sensory information are not immutable; rather they can be shaped by the specific sensory context in which animals develop. This behavioral plasticity depends on the remarkable capacity for the brain to reorganize in response to alterations in the sensory environment, particularly when changes in sensory input occur at an early age. To study this phenomenon, we utilize the short-tailed opossum, a marsupial that has been a valuable animal model to study developmental plasticity due to the extremely immature state of its nervous system at birth. Previous studies in opossums have demonstrated that removal of retinal inputs early in development results in profound alterations to cortical connectivity and functional organization of visual and somatosensory cortex; however, behavioral consequences of this plasticity are not well understood. We trained early blind (EB) and sighted control (SC) opossums to perform a two-alternative forced choice texture discrimination task. Whisker trimming caused an acute deficit in discrimination accuracy for both EB and SC animals indicating that they primarily used a whisker-based strategy to guide choices based on tactile cues − though performance recovered in days, suggesting a shift to the use of other body parts when whiskers were absent. Mystacial whiskers were important for performance in both groups; however, genal whiskers only contributed to performance in EB animals. EB opossums significantly outperformed SC opossums in discrimination accuracy, being more sensitive to textural differences by ~75 μm smaller. Our results support behavioral compensation following early blindness using tactile inputs, especially the whisker system.

Available Sensory Input Determines Motor Performance and Strategy in Early Blind and Sighted Short-Tailed Opossums

“…Recent data from our laboratory indicate that EB animals are better at making fine tactile discriminations but show no differences in whisking behavior compared with SC opossums (Ramamurthy et al, Society for Neuroscience Abstracts, 2018; Ramamurthy and Krubitzer, 2018). In the current study, we found that EB opossums could detect rungs and place their limbs more accurately during ladder rung walking than SC opossums.…”

“…It may also be possible that EB animals are more efficient in their acquisition of sensory information through differences in whisker movement. Previous data from our laboratory indicate this is not the case, as EB and SC Monodelphis have similar whisker set-points and whisking frequencies (Ramamurthy and Krubitzer, 2018). Research in functionally blind rats with similar results adds support for EB animals having heightened sensory coding versus heightened sensory acquisition (Arkley et al, 2014).…”

“…However, it should be noted that differences in the kinematics of other body parts that we did not quantify, particularly in how the position of the whiskers relates to the position of the forelimbs, may also contribute to differences in performance. (Ramamurthy and Krubitzer, 2018). Thus, we examined the role of the whiskers during variable ladder rung walking.…”

“…The spared sensory systems are also affected. There are alterations in cortical and subcortical connections of primary somatosensory cortex (S1) (Figure 1C) (Dooley and Krubitzer, 2019;Karlen et al, 2006) and a spatial sharpening of receptive fields and improved population decoding for whisker-stimulus position for neurons in S1 (Figure 1D) (Ramamurthy and Krubitzer, 2018), indicating that individual neurons in S1 in EB opossums have better discriminability.…”

“…Abbreviations: S1, primary somatosensory cortex; S2, secondary somatosensory cortex; SC, caudal somatosensory area; SR, rostral somatosensory area; MM, multimodal cortex; V1, primary visual cortex; CT caudal temporal area; VL, ventral lateral; VA, ventral anterior nuclei of the thalamus. Figures adapted from Dooley and Krubitzer, 2019;Karlen et al, 2006, andRamamurthy and.…”