ReviewCompensatory plasticity and cross-modal reorganization following early visual deprivation
Introduction
Traditionally, vision has always been considered as the most important sense for humans to interact with the environment. The relevance of sight is strongly embedded in common linguistic expressions. Consider everyday phrases, such as “I see what you mean” or “Do you see my point?” The importance that vision plays in everyday life is also reflected at the level of cortical organization. Indeed, about one third of the cortical surface in primates is involved in visual functions. This raises the question what happens to the visual cortex, both anatomically and functionally, when vision is lost at birth or later in life. There is now a wealth of animal studies showing that neonatal visual deprivation causes massive structural changes that take place not only in the visually deprived cortex but also in other brain areas (reviewed in Ptito and Desgent, 2006, Desgent and Ptito, 2012). In addition, these animal studies have shown that the visually deprived cortex becomes responsive to a variety of non-visual inputs. More recent studies have confirmed that similar plastic rearrangements also take place in the human brain. Whereas the initial studies focused largely on cross-modal responses in the tactile and auditory domain, more recent studies revealed a broader picture showing that the visually deprived occipital cortex is also involved in processing information from other sensory modalities (Kupers et al., 2011a), and even in various cognitive processes (Amedi et al., 2003, Amedi et al., 2004, Bonino et al., 2008, Burton et al., 2003, Cattaneo et al., 2008, Kupers et al., 2007, Kupers et al., 2010, Raz et al., 2005, Stevens et al., 2007).
The study of the congenitally blind brain also offers a unique model to gain better insights into the functioning of the normal sighted brain. To what extent is visual experience truly necessary for the brain to develop its functional architecture? For instance, is visual input necessary for the development of the dorsal and ventral visual streams? Another question is to which extent blindness causes a hyperacuity of the remaining senses, and if so, whether this hyperacuity is due to the recruitment of the occipital cortex. A final question that we will address in this review relates to the subjective character of activity in visually deprived cortex. In his monumental treatise “The principals of Psychology”, published in 1890, William James wondered whether we would “hear the lightning and see the thunder” if we could splice the nerves so that the excitation of the ear fed the brain centre concerned with seeing, and vice versa. We will review data from recent experimental studies that finally provide the first pieces of answer to this centennial question.
Section snippets
Compensatory plasticity
The term “compensatory plasticity” was originally coined to contrast common views that predicted a generalized degradation of sensory functions as a result of early blindness, because vision was viewed as the dominant sense that was needed to calibrate the auditory and tactile senses (Rauschecker, 1995). According to this view, even equal effectiveness of non-visual functions in the blind falls under the original meaning of the term. In current opinion, however, the term compensatory plasticity
Functional integrity of the two visual streams
In the sighted human and non-human primate brain, the retina sends ganglion cell axons to the lateral geniculate of the thalamus that make synapses either in the parvo- or magno-cellular layers and end in the primary visual cortex. The visual system is classically divided into a dorsal and ventral stream, involved in motion and object recognition, respectively (Ungerleider and Mishkin, 1982). One of the questions that come to mind is whether the functional segregation of the visual cortical
Subjective experience (qualia) associated with activation of the visual cortex
As shown above, the occipital cortex of congenitally blind individuals is activated by a wide range of sensory modalities and cognitive tasks. Under normal circumstances, stimulation of a particular cortical area produces a subjective sensation within the same domain. Thus, direct electrical stimulation of the somatosensory cortex (SI) induces somatotopically organized tactile sensations referred to a particular body area (Penfield and Boldrey, 1937). TMS is a non-invasive technique that allows
Functional role of the occipital cortex in blindness
As reviewed elsewhere (Kupers et al., 2011b, Pietrini et al., 2009), functional brain imaging studies have provided ample evidence that the occipital cortex of congenitally blind subjects is activated by a variety of non-visual tasks, such as auditory processing, tactile discrimination, Braille reading, semantic processing and verbal memory. However, these studies do not prove a causal link between the visual cortex activation and task performance. The first evidence for such a causal link came
Anatomical reorganization of the blind brain
The anatomo-functional organization of the normal mammalian brain has been well documented over the years (see Stein, 2012 for a recent review). These studies have underlined the presence of subcortical, heteromodal or cortico-cortical pathways that are unmasked or strengthened in visual deprivation (Kupers et al., 2006, Pascual-Leone et al., 2005). We will focus in this section on studies dealing with sensory deprivation in animal (Section 6.1) and in human (Section 6.2) models of blindness.
Concluding remarks
We have reviewed the literature on compensatory plasticity and cross-modal reorganization following early visual deprivation. In the first part of this paper, we have critically looked at the literature on compensatory plasticity in congenital blindness. Congenitally blind subjects compensate generally well for their loss of vision as testified by the numerous studies showing that they perform at least equally well as their sighted peers in a wide variety of non-visual sensory tasks. This
Acknowledgements
Supported by grants from the Lundbeck Foundation (R.K.), the Harland Sanders Foundation (M.P.), and the Danish Medical Research Foundation (Det Frie Forskningsråd (DFF) to R.K., M.P.).
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