Visual rehabilitation training alters attentional networks in hemianopia: An fMRI study
Introduction
Post-geniculate damage of the visual system leads to homonymous hemianopia which affects about 30% or more of all cases of stroke or brain trauma (Pambakian and Kennard, 1997). Hemianopia greatly reduces quality of life, affecting reading, driving and spatial navigating of patients (Das and Huxlin, 2010). Several strategies for visual field restoration have been introduced (for review see Sabel et al. (2011)). For example, Kasten et al. (1998) showed that patients trained with light detection tasks in areas of residual vision (ARV) had significantly enlarged visual fields. Meanwhile, Henriksson et al. (2007) trained patients with flickering letters to improve visual fields, and Huxlin et al. (2009) used randomly distributed, moving dots for training of visual movement perception problems. A recent functional magnetic resonance imaging (fMRI) study found that the changes of receptive field in primary visual cortex (V1) may result in the enlargements of visual field (Raemaekers et al., 2011). In another study, training was found to induce a stronger activation in the intact hemisphere which was interpreted as compensations by the intact hemisphere to achieve recovery (Henriksson et al., 2007); yet some suggested other neighboring areas of injured region could be recruited through cortico-cortical white matter connectivity (Sahraie et al., 2010) and through retino-colliculo-extrastriate pathway (Bertini et al., 2016). These results suggested that the deficit of hemianopia is not only a locally restricted event but also affects different regions of the visual and non-visual cortical regions which is supported by the prior findings of connectivity disorganization and reorganization after optic nerve damage (Bola et al., 2014). One possibility is that attentional mechanisms are involved in vision restoration. Indeed, behavioral studies of hemianopia showed that attention enhanced residual vision acuity (Poggel et al., 2006) and amplified the efficacy on long-term vision restoration training (Poggel et al., 2004).
Though neuroimaging evidence supports a possible role of attention in hemianopia, the knowledge in this field is still rather fragmentary. Single case based brain imaging analysis found that vision restoration activates different brain structures in the anterior cingulate (ACC), dorsolateral prefrontal cortex (DLPFC) and right temporo-parietal junction (rTPJ, Brodmann area 39/40) (Marshall et al., 2008), all of which are involved in the braińs attention network (Fan et al., 2005, Osaka et al., 2007). Case studies from Henriksson et al. (2007) also found that the right superior temporal cortex, whose caudate is part of the rTPJ, showed stronger activation after the training. However, this was only a single case study so that the level of confidence for a role of attention in vision restoration is still limited, unless this can be confirmed by neuroimaging in larger group study.
Therefore, we now measured the behavioral effects of the visual rehabilitation training and related vision recovery to brain activation changes. To this end, before and after five weeks of training hemianopia patients were assessed with MRI analysis of the salience attention network. We now show that vision restoration is associated with a modulation of the attention network.
Section snippets
Subjects and study design
We chose an open-label longitudinal study design to follow seven hemianopic patients recruited from the Chinese PLA General Hospital (Beijing, China) who gave informed, written consent. The study was approved by the local ethics committee and followed the tenets of the Declaration of Helsinki. Table 1 shows the clinical data of our 7 chronic hemianopia patients and Fig. 1 shows the patients’ MRI T1w images and lesion locations. Typically, spontaneous recovery of vision in hemianopia occurs only
Behavioral results
We asked hemianopic patients to carry out a five-week VRT. Here, training locations were individually positioned in one selected region at the visual field border or inside the damaged zone (Fig. 2) and visual performance was measured in these rehabilitation fields before vs. after training. In perimetric tests, hemianopic patients often show areas of residual vision (ARV), which can be considered as a functional representation of partially functioning neuronal structures (Poggel et al., 2006,
Discussion
Our study confirms a training-induced vision improvement of the damaged visual field of hemianopes and demonstrates that the training affects the attentional network as shown by enhancement of connectivity between ACC, left insula and rTPJ cortices. Most neurophysiological and brain imaging studies of hemianopic patients focused on alterations in brain activity while performing a visual-sensory task. Before treatment, all patients showed considerably reduced contrast sensitivity at the border
Conclusion
The visual cortex has long been considered to be the principal site of visual rehabilitation in hemianopia (Henschen, 1893, Nelles et al., 2002, Papanikolaou et al., 2014). Our data are compatible with the view that bottom-up visual information is projected to secondary visual association regions and frontal areas which have back-projections to the deep layer of V1 (Kok et al., 2016). This modulates neuronal activity in V1, a process which is important to achieve integration with contextual
Acknowledgement
This work was supported by the National Natural Science Foundation of China (31230032 and 81501942), the 12th Five-Year Plan“National Sci-Tech Support Plan, Clinical Study of Optic Neurotis (2012BAI08B06) and the China Postdoctoral Science Foundation (2013M541835)”. B. Sabel was supported by the ERA-net neuron network “Restoration of Vision after Stroke (REVIS)”, (BMBF grant nr: 01EW1210).
Declaration of conflicting interests
The author(s) declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
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These authors contributed equally to this work.