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

Deepa L Ramamurthy,Leah A Krubitzer,Heather K Dodson

doi:10.1242/jeb.236646

Deepa L Ramamurthy, Leah A Krubitzer + Show 1 more

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https://doi.org/10.1242/jeb.236646

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Abstract

ABSTRACTBehavioral 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 of 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 and sighted control opossums to perform a two-alternative forced choice texture discrimination task. Whisker trimming caused an acute deficit in discrimination accuracy for both groups, indicating the use of a primarily whisker-based strategy to guide choices based on tactile cues. Mystacial whiskers were important for performance in both groups; however, genal whiskers only contributed to behavioral performance in early blind animals. Early blind opossums significantly outperformed their sighted counterparts in discrimination accuracy, with discrimination thresholds that were lower by ∼75 μm. Our results support behavioral compensation following early blindness using tactile inputs, especially the whisker system.

Highlights

The behavioral strategies that animals use to orient themselves and navigate within complex environments are highly dependent on the sensory context in which they live
We trained sighted and early blind short-tailed opossums to perform a 2AFC texture discrimination task, in which choosing a rougher texture led to a food reward
By varying the difference in roughness between the textures presented for the choice, we generated psychometric functions for texture discrimination in short-tailed opossums and made comparisons of tactile perceptual sensitivity between sighted and early blind experimental groups

Summary

Introduction

The behavioral strategies that animals use to orient themselves and navigate within complex environments are highly dependent on the sensory context in which they live. Many subterranean mole rats that dwell in burrow systems, with little to no light, are naturally blind, with microphthalmic eyes and no functional vision (Cooper et al, 1993). Instead, they rely heavily on touch and. Even without the loss of a sensory receptor array, any given individual might rely more heavily on one sensory strategy over another in different settings, depending on the ongoing availability and behavioral relevance of sensory information (Montero, 1997; Lee et al, 2016); for example, touch and hearing may be prioritized over vision upon entering a dark room or at night, when visual information is not readily available

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