Visualizing the blind brain: brain imaging of visual field defects from early recovery to rehabilitation techniques

Marika Urbanski, Olivier A Coubard, Clémence Bourlon, Marika Urbanski, Olivier A Coubard, Clémence Bourlon

Abstract

Visual field defects (VFDs) are one of the most common consequences observed after brain injury, especially after a stroke in the posterior cerebral artery territory. Less frequently, tumors, traumatic brain injury, brain surgery or demyelination can also determine various visual disabilities, from a decrease in visual acuity to cerebral blindness. Visual field defects is a factor of bad functional prognosis as it compromises many daily life activities (e.g., obstacle avoidance, driving, and reading) and therefore the patient's quality of life. Spontaneous recovery seems to be limited and restricted to the first 6 months, with the best chance of improvement at 1 month. The possible mechanisms at work could be partly due to cortical reorganization in the visual areas (plasticity) and/or partly to the use of intact alternative visual routes, first identified in animal studies and possibly underlying the phenomenon of blindsight. Despite processes of early recovery, which is rarely complete, and learning of compensatory strategies, the patient's autonomy may still be compromised at more chronic stages. Therefore, various rehabilitation therapies based on neuroanatomical knowledge have been developed to improve VFDs. These use eye-movement training techniques (e.g., visual search, saccadic eye movements), reading training, visual field restitution (the Vision Restoration Therapy, VRT), or perceptual learning. In this review, we will focus on studies of human adults with acquired VFDs, which have used different imaging techniques (Positron Emission Tomography, PET; Diffusion Tensor Imaging, DTI; functional Magnetic Resonance Imaging, fMRI; Magneto Encephalography, MEG) or neurostimulation techniques (Transcranial Magnetic Stimulation, TMS; transcranial Direct Current Stimulation, tDCS) to show brain activations in the course of spontaneous recovery or after specific rehabilitation techniques.

Keywords: cortical reorganization; neuroimaging studies; plasticity; rehabilitation; restoration; visual field defect.

Figures

Figure 1
Figure 1
Schematic diagram of the human visual system. The main connections originating in the retina are represented in thick arrows. They synapse in the lateral geniculate nucleus (LGN) and project to the primary visual cortex (V1). V1 sent information to the extrastriate areas (V2, V3, V4 and MT+/V5). Most of the corticocortical (in blue) and subcortico-cortical (in orange) connections are reciprocal but are not represented for clarity of the schema. Alternative pathways are represented in thin arrows. The extrageniculostriate pathway belonging to the dorsal visual stream, originates in the retina and synapses in the superior colliculus (SC) and in the pulvinar and projects directly to extrastriate areas (in particular area MT+/V5) bypassing both V1 and the LGN. This pathway has been accounted to mediate action blindsight. Another colliculo-pulvinar pathway, associated with the ventral visual stream, synapses in the LGN and projects to extrastriate areas (in particular area V4) bypassing V1. This pathway has been accounted to mediate color and shape residual discrimination. Other collicular pathways are represented: the colliculo-pulvinar pathway (between SC and pulvinar), the pulvino-amygdalar pathway (between the pulvinar and amygdala) and the colliculo-pulvino-amygdalar pathway (between the SC, the pulvinar and the amygdala). These pathways have been accounted to mediate affective blindsight.
Figure 2
Figure 2
Schematic diagram of the subcortico-cortical connections, subcortical connections intra-and interhemispheric connections mediating blindsight in the human left and right hemispheres. For the clarity of the display, not all subcortical connections are represented. The colliculo-pulvinar pathway is represented in green. It extends to several subcortical and cortical areas and is highly symmetrical in the two hemispheres. Fibers passing through the superior colliculus (SC) and pulvinar continue to V1 and extrastriate areas, temporal pole, posterior parietal cortex (PPC), primary motor cortex (M1), frontal eye-field (FEF), dorsolateral prefrontal cortex (DLPFC) and orbitofrontal cortex. A part of the bundle passes through the amygdala, the caudate and brainstem (not represented). The pulvino-amygdalar pathway is represented in pink and is also symmetrical in the two hemispheres. Fibers passing through the pulvinar and the amygdala extend to temporal pole, dorsal prefrontal cortex, orbitofrontal cortex. It also extends to caudate and SC (not represented). The colliculo-pulvino-amygdalar pathway is represented in maroon and is symmetrical in the two hemispheres. It does not extend to other cortical or subcortical areas (see Tamietto et al., 2012).The geniculo-extrastriate pathway is represented in orange and is symmetrical in the two hemispheres. Only fibers connecting the LGN to area MT+/V5 are represented for clarity of the schema. The geniculostriate pathway is represented in blue and is symmetrical in the two hemispheres. Only fibers connecting the LGN to area V1 are represented. The complexity of cortico-cortical and subcortico-cortical routes is partially represented in Figure 1. The interhemispheric connections are represented in red. Both SC are connected via the intercollicular commissure (n°1), both pulvinar via the massa intermedia (n°2; see Catani and Thiebaut De Schotten, 2012), both amygdala are connected by the anterior commissure (n°3). Cortical areas in the occipital cortex are connected by the splenium of the corpus callosum (n°4). Intra-hemispheric connections are labeled by letters in light blue. They are displayed only for the right hemisphere but are also present in the left hemisphere. The pathway linking V4 to temporal pole is the inferior longitudinal fasciculus (ILF: a). The pathway linking the PPC to FEF is the superior longitudinal fascisculus (SLF: b). The pathway linking M1 to FEF and the DLPFC is the superior frontal longitudinal fasciculus (SFL: c). The pathway linking M1 to the orbitofrontal cortex is the inferior frontal longitudinal fasciculus (FIL: d).

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