Visual Experience Is Necessary for the Development of Multisensory Integration

Wallace, Mark T.; Perrault, Thomas J.; Hairston, W. David; Stein, Barry E.

doi:10.1523/jneurosci.2535-04.2004

Cited by 171 publications

(164 citation statements)

References 20 publications

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“…Thus, the AES appears to coordinate the maturation of multisensory capabilities in its intrinsic neurons, presumably involved in higherorder functions, with those of its target neurons in the SC through which it controls orientation behaviors (Wallace and Stein, 2000;Jiang et al, 2006). Furthermore, it appears to exercise this coordination late in the period during which cross-modal experiences critical for multisensory integration are acquired (Wallace et al, 2004b;Wallace and Stein, 2006).…”

Section: Discussionmentioning

confidence: 99%

The Development of Cortical Multisensory Integration

Wallace

Carriere²,

Perrault³

et al. 2006

J. Neurosci.

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120

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Although there are many perceptual theories that posit particular maturational profiles in higher-order (i.e., cortical) multisensory regions, our knowledge of multisensory development is primarily derived from studies of a midbrain structure, the superior colliculus. Therefore, the present study examined the maturation of multisensory processes in an area of cat association cortex [i.e., the anterior ectosylvian sulcus (AES)] and found that these processes are rudimentary during early postnatal life and develop only gradually thereafter. The AES comprises separate visual, auditory, and somatosensory regions, along with many multisensory neurons at the intervening borders between them. During early life, sensory responsiveness in AES appears in an orderly sequence. Somatosensory neurons are present at 4 weeks of age and are followed by auditory and multisensory (somatosensory-auditory) neurons. Visual neurons and visually responsive multisensory neurons are first seen at 12 weeks of age. The earliest multisensory neurons are strikingly immature, lacking the ability to synthesize the cross-modal information they receive. With postnatal development, multisensory integrative capacity matures. The delayed maturation of multisensory neurons and multisensory integration in AES suggests that the higher-order processes dependent on these circuits appear comparatively late in ontogeny.

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Section: Discussionmentioning

confidence: 99%

The Development of Cortical Multisensory Integration

Wallace

Carriere²,

Perrault³

et al. 2006

J. Neurosci.

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118

120

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“…In these studies, profound unimodal degradation, in the form of total deprivation, changes the functional properties of neurons in multisensory regions and unisensory regions of the intact modality (Heil et al 1991;Wallace et al 2004). As older adults lose their hearing, the unimodal acoustic input becomes increasingly less audible or more degraded over time.…”

Section: Discussionmentioning

confidence: 99%

“…Several lines of animal research show that multisensory mechanisms (such as the integration of sight and sound) depend on the integrity of each unimodal input. For instance, when subjects are deprived of one modality, the response to multisensory stimuli is often degraded relative to counterparts with normally functioning inputs (Heil et al 1991;Wallace et al 2004). HL can be considered a type of auditory deprivation because HL people receive less auditory input than NHs in normal listening conditions.…”

Section: Introductionmentioning

confidence: 99%

Audiovisual Deficits in Older Adults with Hearing Loss: Biological Evidence

Musacchia

Arum²,

Nicol³

et al. 2009

Ear &Amp; Hearing

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Objective:To examine the impact of hearing loss (HL) on audiovisual (AV) processing in the aging population. We hypothesized that agerelated HL would have a pervasive effect on sensory processing, extending beyond the auditory domain. Specifically, we predicted that decreased auditory input to the neural system, in the form of HL over time, would have deleterious effects on multisensory mechanisms. Design:This study compared AV processing between older adults with normal hearing (N ϭ 12) and older adults with mild to moderate sensorineural HL (N ϭ 12). To do this, we recorded cortical evoked potentials that were elicited by watching and listening to recordings of a speaker saying the syllable "bi." Stimuli were presented in three conditions: when hearing the syllable "bi" (auditory), when viewing a person say "bi" (visual), and when seeing and hearing the syllables simultaneously (AV). Presentation level of the auditory stimulus was set to ϩ30 dB SL for each listener to equalize auditory input across groups. Results:In the AV condition, the normal-hearing group showed a clear and consistent decrease in P1 and N1 latencies as well as a reduction in P1 amplitude compared with the sum of the unimodal components (auditory ϩ visual). These integration effects were absent or less consistent in HL participants.Conclusions: Despite controlling for auditory sensation level, visual influence on auditory processing was significantly less pronounced in HL individuals compared with controls, indicating diminished AV integration in this population. These results demonstrate that HL has a deleterious effect on how older adults combine what they see and hear. Although auditory amplification vastly improves the communication abilities in most HLs, the associated atrophy of multisensory mechanisms may contribute to a patient's difficulty in everyday settings. Our findings and related studies emphasize the potential value of multimodal tasks and stimuli in the assessment and rehabilitation of hearing impairments.

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“…This is exceedingly rare in both normal animals (see Stein et al 2004) and in animals reared in abnormal visual environments. In the latter cases, the nonvisual representations generally accommodate to the experience-induced changes in the visual topography in ways that maintain cross-modal map and receptive field alignment (see King et al 1988;Knudsen and Brainard 1991;Wallace et al 2004). These changes were also quite different from those noted during temporary cryogenic deactivation of AES and rLS, which had no effect on the overall register of a neuron's different receptive fields (e.g., see Jiang et al 2001).…”

Section: Neonatal Lesions Of Aes and Rlsmentioning

confidence: 99%

Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus

Jiang

Jiang²,

Stein³

2006

Journal of Neurophysiology

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ablation disrupts multisensory development in superior colliculus. J Neurophysiol 95: 1380 -1396, 2006. First published November 2, 2005 doi:10.1152/jn.00880.2005. The ability of cat superior colliculus (SC) neurons to synthesize information from different senses depends on influences from two areas of the cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Reversibly deactivating the inputs to the SC from either of these areas in normal adults severely compromises this ability and the SC-mediated behaviors that depend on it. In this study, we found that removal of these areas in neonatal animals precluded the normal development of multisensory SC processes. At maturity there was a substantial decrease in the incidence of multisensory neurons, and those multisensory neurons that did develop were highly abnormal. Their cross-modal receptive field register was severely compromised, as was their ability to integrate cross-modal stimuli. Apparently, despite the impressive plasticity of the neonatal brain, it cannot compensate for the early loss of these cortices. Surprisingly, however, neonatal removal of either AES or rLS had comparatively minor consequences on these properties. At maturity multisensory SC neurons were quite common: they developed the characteristic spatial register among their unisensory receptive fields and exhibited normal adult-like multisensory integration. These observations suggest that during early ontogeny, when the multisensory properties of SC neurons are being crafted, AES and rLS may have the ability to compensate for the loss of one another's cortico-collicular influences so that normal multisensory processes can develop in the SC.

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Visual Experience Is Necessary for the Development of Multisensory Integration

Cited by 171 publications

References 20 publications

The Development of Cortical Multisensory Integration

The Development of Cortical Multisensory Integration

Audiovisual Deficits in Older Adults with Hearing Loss: Biological Evidence

Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus

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