Human brain plasticity: Evidence from sensory deprivation and altered language experience

Abstract

The results from the language studies taken as a whole point to different developmental time courses and developmental vulnerabilities of aspects of grammatical and semantic/lexical processing. They thus provide support for conceptions of language that distinguish these subprocesses within language. Similarly, following auditory deprivation, processes associated with the dorsal visual pathway were more altered than were functions associated with the ventral pathway, providing support for conceptions of visual system organization that distinguish functions along these lines. Could the effects observed in blind and deaf adults be accounted for, at least in part, by the redundant connectivity of the immature human brain? One way we tested this hypothesis was to study the differentiation of visual and auditory sensory responses in normal development (Neville, 1995). In normal adults, auditory stimuli elicit ERP responses that are large over temporal brain regions but small or absent over occipital regions. By contrast, in 6-month-old children we observed that auditory ERPs are equally large over temporal and visual brain regions, consistent with the idea that there is less specificity and more redundancy of connections between the auditory and visual cortex at this time. Between 6 and 36 months, however, we observed a gradual decrease in the amplitude of the auditory ERP over visual areas, while the amplitude over the temporal areas was unchanged. These results suggest that early in human development, there exists a redundancy of connections between auditory and visual areas and that this overlap gradually decreases after birth. This loss of redundancy may be a boundary condition that determines when sensory deprivation can result in alterations in the organization of remaining sensory systems. The considerable variability in timing of sensitive periods may also be in part due to temporal differences in the occurrence of redundancy within different systems. Ongoing studies of infants and children employing different types of stimuli will test for the specificity of these effects (Mitchell et al., 1999). Differences in the degree of plasticity may also be due to differences in the overall level of redundant connectivity within different systems. For example, it may be that aspects of sensory systems that are specialized for high spatial acuity (e.g., central vision and central audition) exhibit fewer developmental redundancies, decreased modifiability and more specificity than those displaying less acuity and precision (e.g., peripheral representations within vision and audition). There is some evidence for this hypothesis within the visual system (Chalupa and Dreher, 1991). In addition, there may be molecular differences between systems displaying different levels and patterns of experience-dependent plasticity. It is of interest that all levels of the dorsal pathway of the visual system, which in the studies reviewed here shows a high level of modifiability, displays strong immunoreactivity for the monoclonal antibody CAT 301 in macaque monkeys (DeYoe et al., 1990). By contrast there is very little labeling within the ventral visual pathway. Moreover, the expression of CAT 301 immunoreactivity shows marked experience-dependent plasticity, suggesting it may play a role in the guidance and/or stabilization of synaptic structure (Sur et al., 1988). Further research along these lines within the auditory system and in animal models of sensory deprivation and other developmental disorders may elucidate the role of specific molecular factors in the developmental plasticity of different neural systems. A related, more general hypothesis that may account for the different patterns of plasticity within both vision and language is that systems employing fundamentally different learning mechanisms (perhaps mediated by different anatomical and molecular substrates) display different patterns of developmental plasticity. It may be that systems that display experience-dependent change throughout life, including the topography of sensory maps (Merzenich et al., 1988; Gilbert, 1995; Kaas, 1995), lexical acquisition (i.e. object-word associations), and the establishment of form, face, and object representations (i.e., ventral pathway functions) rely upon very general, associative learning mechanisms that permit learning and adaptation throughout life. By contrast, systems that are important for computing dynamically shifting relations among locations, objects and events (including the dorsal visual pathway and the systems of the brain that mediate grammar) appear dependent on and modifiable by experience primarily during more limited periods in development. This could account for both the greater developmental deficits and enhancements of dorsal pathway function following various developmental anomalies and for the greater effects of altered language experience on grammatical functions. Further research is necessary to characterize systems that become constrained in this way and those that can be modified throughout life. This type of developmental evidence can contribute to fundamental descriptions of the architecture of different cognitive systems and can guide future studies of the cellular and molecular mechanisms important in neuroplasticity. Additionally, in the long run, they may contribute to the design of educational and habilitative programs for both normally and abnormally developing children.