What is the function of auditory cortex when it develops in the absence of acoustic input?
Introduction
Hearing impairment is the most common sensory disability in adults and one of the most common birth defects in North America (Cossette & Duclos, 2002). For the latter group, it is well known that cochlear implants, which substitute for a non-functioning cochlea, are more effective in younger than older children (Harrison, Gordon, & Mount, 2005; Kral & Sharma, 2012; Lee et al., 2001; Papsin, Gysin, Picton, Nedzelski, & Harrison, 2000; Sharma, Dorman, & Kral, 2005). Even in adults, the longer the interval between hearing loss and cochlear implant, the poorer the prognosis for effective cochlear implant (Doucet et al., 2006; Lee et al., 2001). These studies suggest that the cochlear implant recipients that performed the poorest had their non-functioning central auditory pathways subsumed by the remaining sensory systems, rendering them ineffective to respond to the cochlear implants. In fact, while some imaging studies of early-deaf human adults report the presence of visual activity in deaf AI (Finney, Fine, & Dobkins, 2001; Karns, Dow, & Neville, 2012; Lambertz, Gizewski, Greiff, & Forsting, 2005), other imaging studies only find crossmodal visual activation in non-primary auditory areas (Hickok et al., 1997, Nishimura et al., 1999, Sadato et al., 2005, Weeks et al., 2000). Furthermore, the fact that deaf humans and animals show specific visual and tactile behavioural enhancements over intact, hearing subjects clearly establishes that deafness induces crossmodal plasticity (Bavelier et al., 2000; Levanen & Hamdof, 2001; Lomber, Meredith, & Kral, 2010). The loci underlying some of these crossmodal functional enhancements have been recently shown. The auditory field of the anterior ectosylvian sulcus (FAES) of the cat is replaced in early-deaf animals by visually responsive neurons. This physiological crossmodal plasticity is expressed at a behavioural level with FAES switching from mediating auditory to visual orienting behaviours (Meredith et al., 2011). It has also been identified that both early-deafness and late-deafness cause visual and tactile crossmodal plasticity in the anterior auditory field (AAF) of cats and ferrets (Allman, Keniston, & Meredith, 2009; Meredith & Lomber, 2011). These experiments show that crossmodal plasticity is produced by early- and late-onset deafness.
Similar to the visual system, auditory development passes through a sensitive period in which circuits and connections are established and then refined by experience (Knudsen, 2004; Kral, Hartmann, Tillein, Heid, & Klinke, 2000). During this period, the functional maturation of auditory processing and perception is critically dependent on adequate auditory experience. Cats appear to progress through a critical phase at 2–3 months old, and complete their auditory maturation by 6 months (Kral, Tillein, Heid, Hartmann, & Klinke, 2005). A similar, but more prolonged sensitive period seems to apply to humans (up to ∼13 years; Doucet et al., 2006), as evidenced by congenitally deaf subjects who receive cochlear implants in early childhood who develop complete language competence. In contrast, those who do not receive such treatment until later in life generally do not develop sophisticated spoken language skills, but may develop sophisticated signed language skills. The specific defects in the auditory system that underlie such persistent deficits remain to be identified. Some investigators using imaging or EEG techniques have asserted that such deficits are the result of crossmodal plasticity that subsumes the non-functional parts of the auditory system into other sensory modes (Doucet et al., 2006, Finney et al., 2001, Lee et al., 2001). In contrast, studies done in congenitally deaf animals with much higher correlational resolution have failed to show any crossmodal activation of AI (Kral, Schroder, Klinke, & Engel, 2003; Stewart & Starr, 1970) and revealed that auditory nerve stimulation maintained access to AI even in congenitally deaf adults (Kral et al., 2000, Kral et al., 2005). Ironically, despite the intense scrutiny that AI has received in these studies virtually none of the reorganized non-primary areas have been specifically named. This incorrectly seems to suggest that because non-primary areas are ‘expected’ to be reorganized, they all must be similarly affected (and to the same degree). Therefore, the crucial debate in this regard is not if deafness induces crossmodal plasticity, but where such plasticity occurs.
Section snippets
The congenitally deaf cat
The cat is an appealing model system to use for these types of investigations on cerebral networks in auditory cortex. It is a simplified and tractable version of the more complex networks present in monkeys and humans. Cats are ideal because: 1) they can quickly be trained to perform complex auditory tasks; 2) unlike the monkey, the majority of the auditory areas are easily approachable because they are exposed on the surfaces of gyri, rather than being buried in the depths of a sulcus; and 3)
Enhanced visual abilities of the congenitally deaf
Studies of deaf or blind subjects often report enhanced perceptual abilities in the remaining senses. Compared to hearing subjects, human psychophysical studies have revealed specific superior visual abilities in the early-deaf (Bavelier, Dye, & Hauser, 2006; Neville & Lawson, 1987; Shiell, Champoux, & Zatorre, 2014) as well as enhanced auditory functions in the early-blind (Lessard, Paré, Lepore, & Lassonde, 1998; Rauschecker, 1995; Röder et al., 1999). To more closely investigate this issue,
Reversible cooling deactivation of auditory cortex
The brain regions mediating superior sensory abilities have been proposed to reside in the deprived cerebral cortices that are thought to be utilized by the remaining sensory systems. Therefore, it has been hypothesized that auditory cortex of the deaf may be recruited to perform visual functions. To test this hypothesis, portions of auditory cortex (Fig. 2, yellow regions) were collectively and individually deactivated to determine if specific cortical areas mediated the enhanced visual
Visual localization in the peripheral field
For the visual localization task, the first step was to determine if auditory cortex could be mediating the enhanced performance of the deaf cats. Therefore, we simultaneously deactivated all four areas (PAF, DZ, A1, and AAF) bilaterally, which resulted in a significant reduction in visual localization performance restricted to the most peripheral positions (60°, 75°, and 90° positions; Fig. 3a,b). Although the animals often failed to accurately or precisely localize the stimulus in the far
Are unenhanced vision functions redistributed over deaf auditory cortex?
In addition to deaf auditory cortex serving as the neural substrate for enhanced visual functions, it is also possible that there was an overall redistribution of visual functions in the deaf brain. In light of this, it might be hypothesized that visual functions normally localized within visual cortex may become distributed into deaf auditory cortex. Therefore, we also sought to examine whether deaf auditory cortex undergoes wholesale cross-modal reorganization such that even unaffected visual
Deactivation of auditory cortex in hearing cats
As we have demonstrated that deaf auditory cortex is the neural substrate for the enhanced visual abilities of the deaf, it was essential to also demonstrate that the auditory cortex of hearing cats does not contribute to visual function. Therefore, for the group of hearing cats, we both simultaneously and individually deactivated the four auditory areas on each of the seven visual tasks. Overall, neither simultaneous nor individual deactivation of the four auditory regions altered the ability
Deaf auditory cortex as the neural substrate for enhanced visual functions
These studies demonstrate a causal link between crossmodal plasticity in auditory cortex and specific visual functional improvements in the congenitally deaf. Most importantly, cortical deactivation demonstrated that different perceptual improvements were dependent on specific and different subregions of auditory cortex. The improved localization of visual stimuli in deaf animals was eliminated by deactivating posterior auditory cortex, while the enhanced sensitivity to visual motion was
What is the anatomical basis for crossmodal reorganization following deafness?
How the structural or anatomical basis of the crossmodal reorganization described above might occur remains an issue of debate. Rauschecker (1995) described several possible cortical mechanisms, including unmasking of silent inputs, stabilization of normally transient connections, sprouting of new axons, or by some combination of these processes. Indeed, anatomical studies in non-rodent species have demonstrated that non-primary cortical sensory areas are connected both directly (Allman et al.,
The importance of understanding the deaf brain
Collectively, these results provide new and comprehensive insight into the specific brain changes induced by early deafness to a level that is essentially unobtainable through other experimental approaches. In addition, these observations form the basis for a robust and repeatable model of adaptive cortical plasticity that will be used to uncover the basic principles that characterize this phenomenon as well as better understand its relation to neuroplastic processes as a whole. By
Acknowledgements
The financial support of the Canadian Institutes of Health Research (CAN) and the Natural Sciences and Engineering Research Council of Canada are gratefully acknowledged.
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