Noise‐rearing disrupts the maturation of multisensory integration

Abstract

It is commonly believed that the ability to integrate information from different senses develops according to associative learning principles as neurons acquire experience with co-active cross-modal inputs. However, previous studies have not distinguished between requirements for co-activation versus co-variation. To determine whether cross-modal co-activation is sufficient for this purpose in visual–auditory superior colliculus (SC) neurons, animals were reared in constant omnidirectional noise. By masking most spatiotemporally discrete auditory experiences, the noise created a sensory landscape that decoupled stimulus co-activation and co-variance. Although a near-normal complement of visual–auditory SC neurons developed, the vast majority could not engage in multisensory integration, revealing that visual–auditory co-activation was insufficient for this purpose. That experience with co-varying stimuli is required for multisensory maturation is consistent with the role of the SC in detecting and locating biologically significant events, but it also seems likely that this is a general requirement for multisensory maturation throughout the brain.

Development of multisensory integration from the perspective of the individual neuron

“…4). Instead, they responded to cross-modal cues in the same way as do neurons in dark-reared and neonatal animals 133 . This result rules out the idea that a given sensory modality (for example, the visual modality) is uniquely critical and suggests instead that there is something specific about the nature of cross-modal exposure that determines whether multisensory integration capabilities mature.…”

Cross-Modal Plasticity in Higher-Order Auditory Cortex of Congenitally Deaf Cats Does Not Limit Auditory Responsiveness to Cochlear Implants

“…Although cross-modal reorganization is well documented (Rauschecker, 1995;Bavelier et al, 2006;Auer et al, 2007;Merabet and Pascual-Leone, 2010;Ding et al, 2015) and related to enhanced abilities in the remaining senses in deaf individuals (Neville and Lawson, 1987;Levänen et al, 1998;Bavelier et al, 2006;Bottari et al, 2014;Stein et al, 2014), the original function of the reorganized neural tissue has not been explored before at the level of neurons. The absence of adverse effects of crossmodal reorganization on auditory responsiveness has implications for visual communication before cochlear implantation in children born deaf.…”

“…In cats, visual deprivation interferes with development of multimodal integration (Wallace et al, 2004(Wallace et al, , 2006Carriere et al, 2007Carriere et al, , 2008. The absence of vision during development interferes with the development of multimodal interactions in the superior colliculus, but less with visual responsiveness (Yu et al, 2013;Stein et al, 2014). Even rearing under omnidirectional noise has a similar effect (Xu et al, 2014).…”

“…The absence of vision during development interferes with the development of multimodal interactions in the superior colliculus, but less with visual responsiveness (Yu et al, 2013;Stein et al, 2014). Even rearing under omnidirectional noise has a similar effect (Xu et al, 2014). Furthermore, early visual deprivation has detrimental effects on multimodal integration in association area 7 (adjoining the MLS areas; Carlson et al, 1987).…”

“…Congenital sensory loss triggers cross-modal plasticity in the deprived sensory cortex (Rauschecker, 1995;Bavelier et al, 2006;Stein and Stanford, 2008;Merabet and Pascual-Leone, 2010;Stein et al, 2014). Cross-modal reorganization is likely related to enhanced abilities in the remaining senses as best documented in deaf individuals (Neville and Lawson, 1987;Levänen et al, 1998;Bavelier and Neville, 2002;Bavelier et al, 2006;Auer et al, 2007;Bottari et al, 2010Bottari et al, , 2014.…”