Compensatory plasticity and cross-modal reorganization following early visual deprivation

Highlights

• Congenital blindness is associated with a hyperacuity for certain tactile and auditory tasks.

• The visual cortex of congenitally blind individuals is recruited by non-visual sensory modalities and by various cognitive tasks.

• The visual cortex of the congenitally blind is reduced in volume, is thicker and has a supranormal metabolic activity at rest.

• Visual experience is not necessary for the dorsal and ventral visual streams to develop.

• The subjective correlate of occipital activation in the blind brain can be tactile in nature.

Abstract

For human and non-human primates, vision is one of the most privileged sensory channels used to interact with the environment. The importance of vision is strongly embedded in the organization of the primate brain as about one third of its cortical surface is involved in visual functions. It is therefore not surprising that the absence of vision from birth, or the loss of vision later in life, has huge consequences, both anatomically and functionally. Studies in animals and humans, conducted over the past few decades, have demonstrated that the absence of vision causes massive structural changes that take place not only in the visually deprived cortex but also in other brain areas. These studies have further shown that the visually deprived cortex becomes responsive to a wide variety of non-visual sensory inputs. Recent studies even showed a role of the visually deprived cortex in cognitive processes. At the behavioral level, increases in acuity for auditory and tactile processes have been reported. The study of the congenitally blind brain also offers a unique model to gain better insights into the functioning of the normal sighted brain and to understand to what extent visual experience is necessary for the brain to develop its functional architecture. Finally, the study of the blind brain allows us to investigate how consciousness develops in the absence of vision. How does the brain of someone who has never had any visual perception form an image of the external world? In this paper, we discuss recent findings from animal studies as well as from behavioural and functional brain imaging studies in sighted and blind individuals that address these questions.

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.