The normal environment delays the development of multisensory integration

Jinghong Xu,Benjamin A Rowland,Liping Yu,Barry E Stein

doi:10.1038/s41598-017-05118-1

Jinghong Xu, Benjamin A Rowland + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-05118-1

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Abstract

Multisensory neurons in animals whose cross-modal experiences are compromised during early life fail to develop the ability to integrate information across those senses. Consequently, they lack the ability to increase the physiological salience of the events that provide the convergent cross-modal inputs. The present study demonstrates that superior colliculus (SC) neurons in animals whose visual-auditory experience is compromised early in life by noise-rearing can develop visual-auditory multisensory integration capabilities rapidly when periodically exposed to a single set of visual-auditory stimuli in a controlled laboratory paradigm. However, they remain compromised if their experiences are limited to a normal housing environment. These observations seem counterintuitive given that multisensory integrative capabilities ordinarily develop during early life in normal environments, in which a wide variety of sensory stimuli facilitate the functional organization of complex neural circuits at multiple levels of the neuraxis. However, the very richness and inherent variability of sensory stimuli in normal environments will lead to a less regular coupling of any given set of cross-modal cues than does the otherwise “impoverished” laboratory exposure paradigm. That this poses no significant problem for the neonate, but does for the adult, indicates a maturational shift in the requirements for the development of multisensory integration capabilities.

Highlights

At least two interrelated factors appear to be necessary for superior colliculus (SC) neurons to develop their multisensory integration capabilities: functional inputs from ipsilateral association cortex, and experience with cross-modal events[1]
Pharmacological deactivation may have been so disruptive to the activity-dependent maturation of association cortex that it required years of rehabilitation before that cortex became capable of playing its normal role in this SC process
The present study examined these alternatives by using the same adult animals to compare the effects of the laboratory exposure paradigm and normal environments on the acquisition of SC multisensory integration capabilities

Summary

Introduction

At least two interrelated factors appear to be necessary for superior colliculus (SC) neurons to develop their multisensory integration capabilities: functional inputs from ipsilateral association cortex, and experience with cross-modal events[1]. Deactivating the tectopetal inputs from association cortex during early life disrupts this maturational process[2, 3], as does precluding relevant (e.g., visual-auditory) experience by rearing the animals in darkness or with continuous masking noise[4,5,6,7]. Normal + Training (VA Trained) 6 months cues derived from the same event in normal environments vary in their exact spatiotemporal relationships on different occurrences, can appear under very different background conditions, and are often interleaved with their unpaired counterparts This variability is avoided in the laboratory exposure paradigm. The present study examined these alternatives by using the same adult animals to compare the effects of the laboratory exposure paradigm and normal environments on the acquisition of SC multisensory integration capabilities

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