Experience Creates the Multisensory Transform in the Superior Colliculus

Wang, Zhengyang1; Yu, Liping2; Xu, Jinghong2; Stein, Barry E.3; Rowland, Benjamin A.3

2020-04-21

10.3389/fnint.2020.00018

Frontiers in Integrative Neuroscience   影响因子和分区

1662-5145

Although the ability to integrate information across the senses is compromised in some individuals for unknown reasons, similar defects have been observed when animals are reared without multisensory experience. The experience-dependent development of multisensory integration has been studied most extensively using the visual-auditory neuron of the cat superior colliculus (SC) as a neural model. In the normally-developed adult, SC neurons react to concordant visual-auditory stimuli by integrating their inputs in real-time to produce non-linearly amplified multisensory responses. However, when prevented from gathering visual-auditory experience, their multisensory responses are no more robust than their responses to the individual component stimuli. The mechanisms operating in this defective state are poorly understood. Here we examined the responses of SC neurons in "naive" (i.e., dark-reared) and "neurotypic" (i.e., normally-reared) animals on a millisecond-by-millisecond basis to determine whether multisensory experience changes the operation by which unisensory signals are converted into multisensory outputs (the "multisensory transform"), or whether it changes the dynamics of the unisensory inputs to that transform (e.g., their synchronization and/or alignment). The results reveal that the major impact of experience was on the multisensory transform itself. Whereas neurotypic multisensory responses exhibited non-linear amplification near their onset followed by linear amplification thereafter, the naive responses showed no integration in the initial phase of the response and a computation consistent with competition in its later phases. The results suggest that multisensory experience creates an entirely new computation by which convergent unisensory inputs are used cooperatively to enhance the physiological salience of cross-modal events and thereby facilitate normal perception and behavior.

cross-modal development timing coactivation enhancement dark-rearing

SCI

英语

第一

NIH[EY024458][EY026916] ; National Natural Science Foundation of China[31300910][31400944]

Behavioral Sciences ; Neurosciences & Neurology

Behavioral Sciences ; Neurosciences

WOS:000531607400001

FRONTIERS MEDIA SA

Web of Science

1.Southern Univ Sci & Technol, Dept Biomed Engn, Shenzhen, Peoples R China
2.East China Normal Univ, Sch Life Sci, Minist Educ & Shanghai, Key Lab Brain Funct Genom, Shanghai, Peoples R China
3.Wake Forest Sch Med, Dept Neurobiol & Anat, Winston Salem, NC 27101 USA

Wang, Zhengyang,Yu, Liping,Xu, Jinghong,et al. Experience Creates the Multisensory Transform in the Superior Colliculus[J]. Frontiers in Integrative Neuroscience,2020,14.

Wang, Zhengyang,Yu, Liping,Xu, Jinghong,Stein, Barry E.,&Rowland, Benjamin A..(2020).Experience Creates the Multisensory Transform in the Superior Colliculus.Frontiers in Integrative Neuroscience,14.

Wang, Zhengyang,et al."Experience Creates the Multisensory Transform in the Superior Colliculus".Frontiers in Integrative Neuroscience 14(2020).