4.1  Introduction

The question of what happens to the brain following the loss of sight is of seminal importance for any rehabilitative strategy for the blind. In order to interact effectively with their environment, blind individuals have to make striking adjustments to their loss of sight. Growing experimental evidence now suggests that these behavioral adaptations are reflected by dramatic neurophysiological changes at the level of the brain and specifically, with regions of the brain responsible for processing vision itself. These changes may represent the exploitation of spatial and temporal processing inherent within occipital visual cortex that allow a blind individual to adapt to the loss of sight and remain integrated in highly visually-dependent society.

Over the past 25 years, great strides have been made in understanding the neurophysiological mechanisms underlying visual perception. What is less known are the changes associated with how the brain adapts to the loss of sight. For example, what is the physiological and functional fate of cortical areas normally associated with the processing of visual information once vision is lost (e.g. from ocular disease or trauma)? Would this have an impact on the success of implementing a rehabilitative strategy such as a visual based neuroprosthesis in the hope of restoring functional vision? As research and development continues, we should be aware that some of the impediments to future progress in implementing a visual neuroprosthesis approach are not only technical, engineering and surgical issues, but are also related to the development and implementation of strategies designed to interface with the visually deprived brain.

In this chapter, we will review recent advances in the knowledge about brain plasticity and emphasize its importance in order to achieve optimal and desired behavioral outcomes with respect to neuroprosthesis development. Other important questions that will be reviewed relate to the time course of the plastic changes and whether cortical areas deprived of their normal sensory input can still process the lost sensory modality.

4.2  Current Concepts on Brain Plasticity and Implications for Visual Rehabilitation

Classical thought has held the view that the bulk of brain development occurred during childhood and that thereafter there was little opportunity for dramatic adaptive change. It was understood however, that adult brains must display some form of adaptation or “plasticity” since we are capable of sensory and motor learning

loss should be assumed to be beneficial or necessarily lead to functional recovery. In reality, neuroplasticity can be viewed as both a positive and negative response. On one hand, it can contribute to changes that are functionally adaptive when a sensory modality is lost. On the other, neuroplasticity can also constrain the degree of adaptation. Therefore, the consequences of neuroplastic change need to be considered not only as a consequence of sensory loss, but also with respect to an individual’s own experiences.

Plasticity is not only essential to allow the brain to adjust to its ever-changing sensory environment and experiences and improving perceptual skills, but also plays a crucial role in the recovery from damage and insult. This is also true with regard to the visual system, the adaptation to blindness and ultimately, the restoration of sight. In the case of restoring sight through neuroprosthetic means, it would be a great over-simplification to believe that re-introduction of the lost sensory input by itself will immediately restore the lost sense. Specific strategies have to be developed to modulate information processing by the brain and to extract relevant and functionally meaningful information from neuroprosthetic inputs.

4.3  Clinical Evidence for Reorganization of Cortical Networks in the Blind and Visually Impaired

It would seem reasonable to presume that in the setting of visual deprivation, the brain would reorganize itself to exploit the sensory inputs at its disposal [5, 17, 38, 40, 54, 61] and in fact, the loss of sight has been associated with superior non-visual perception in the blind, such as auditory and tactile abilities, and even in higher cognitive functions such as linguistic processing and verbal memory [4, 5, 12, 60, 79, 81, 92]. These adjustments not only implicate changes in the remaining sensory modalities (for example, touch and hearing) but also involve those parts of the brain once dedicated to the task of vision itself.

For example, the ability to read Braille is associated with an enlargement of the somatosensory cortical representation of the reading index finger (but not the corresponding non-reading finger) in association with the recruitment of the occipital visual cortex for the processing of tactile information. The functional significance of this cross-modal plasticity is supported by a variety of additional converging data. For example, Uhl et al. using event-related electroencephalography and single photon emission computerized tomography (SPECT) [90, 91] demonstrated that the primary visual areas are activated in early-blind subjects while performing a Braille reading task. Pascual-Leone and Hamilton had the opportunity of studying a congenitally blind woman who was an extremely proficient Braille reader (working as an editor for a Braille newsletter) who became suddenly Braille alexic while otherwise remaining neurologically intact, following a bilateral occipital stroke [40]. The interesting finding was contrary to expectations as the lesion did not affect the somatosensory cortex, but rather damaged the occipital pole bilaterally. Although she was well aware of the presence of the dot elements contained in the

Braille text, she was unable to extract enough information to determine the meaning contained in the dot patterns. Further support demonstrating the functional role of occipital cortex comes from the fact that reversible disruption of occipital cortex function, for example by transcranial magnetic stimulation (TMS), impairs Braille reading ability in the blind [24].

While initial work focused on the task of Braille reading [82, 83], increasing evidence has also demonstrated activation of occipital cortical areas in congenitally blind subjects during tasks of auditory localization [51, 93]. This issue was further addressed by assessing language-related brain activity implicated in speech processing and auditory verb-generation. It has been shown that speech comprehension activates not only parts of the brain associated with language (as with sighted adult controls) [80], but also striate and extra-striate regions of the visual cortex [5]. As with tactile processing, reversible functional disruption of the occipital cortex by TMS impairs verb-general performance only in blind subjects [4] providing further evidence that the recruitment of the occipital cortex in high-level cognitive processing is functionally relevant.

The work demonstrating the functional recruitment of occipital cortex for the processing of non-visual information may reveal only the “tip of the iceberg” in terms of the brain reorganization that follows visual deprivation. Nevertheless these neuroplastic changes define a specific time window for the success of any visual neuroprosthesis (before full cross-modal adaptation) that probably is influenced by factors such as the onset and duration of visual deprivation and the mechanisms and profile of the visual loss (Fig. 4.2).

Fig. 4.2  Adaptive and compensatory changes at the occipital cortex after visual deprivation. (a) Following visual deafferentation, inputs from other sensory processing areas reach the occipital cortex via connections through multisensory cortical areas (and possible through direct connections). These adaptive changes include the functional recruitment of visual cortical areas for the processing of non-visual information such as tactile information, auditory information and higher-order cognitive functions (e.g. verbal memory). (b) Over time, these neuroplastic changes may eventually lead to the establishment of new connections and functional roles with clear implications on the right time of implantation and the likelihood of success in recreating functional vision with a visual neuroprosthetic device