Sara Ajina

Human blindsight is mediated by an intact geniculo-extrastriate pathway.

Although damage to the primary visual cortex (V1) causes hemianopia, many patients retain some residual vision; known as blindsight. We show that blindsight may be facilitated by an intact white-matter pathway between the lateral geniculate nucleus and motion area hMT+. Visual psychophysics, diffusion-weighted magnetic resonance imaging and fibre tractography were applied in 17 patients with V1 damage acquired during adulthood and 9 age-matched controls. Individuals with V1 damage were subdivided into blindsight positive (preserved residual vision) and negative (no residual vision) according to psychophysical performance. All blindsight positive individuals showed intact geniculo-hMT+ pathways, while this pathway was significantly impaired or not measurable in blindsight negative individuals. Two white matter pathways previously implicated in blindsight: (i) superior colliculus to hMT+ and (ii) between hMT+ in each hemisphere were not consistently present in blindsight positive cases. Understanding the visual pathways crucial for residual vision may direct future rehabilitation strategies for hemianopia patients. DOI: http://dx.doi.org/10.7554/eLife.08935.001

Motion area V5/MT+ response to global motion in the absence of V1 resembles early visual cortex.

Little is known about how non-V1 inputs influence motion area V5/MT+. Ajina et al. reveal that after V1 damage, V5/MT+ activity resembles that of early visual cortex, perhaps driven by similar subcortical inputs. While these inputs are normally overshadowed by V1 connections, acknowledging their contribution may improve neuronal models.

Abnormal contrast responses in the extrastriate cortex of blindsight patients.

When the human primary visual cortex (V1) is damaged, the dominant geniculo-striate pathway can no longer convey visual information to the occipital cortex. However, many patients with such damage retain some residual visual function that must rely on an alternative pathway directly to extrastriate occipital regions. This residual vision is most robust for moving stimuli, suggesting a role for motion area hMT+. However, residual vision also requires high-contrast stimuli, which is inconsistent with hMT+ sensitivity to contrast in which even low-contrast levels elicit near-maximal neural activation. We sought to investigate this discrepancy by measuring behavioral and neural responses to increasing contrast in patients with V1 damage. Eight patients underwent behavioral testing and functional magnetic resonance imaging to record contrast sensitivity in hMT+ of their damaged hemisphere, using Gabor stimuli with a spatial frequency of 1 cycle/°. The responses from hMT+ of the blind hemisphere were compared with hMT+ and V1 responses in the sighted hemisphere of patients and a group of age-matched controls. Unlike hMT+, neural responses in V1 tend to increase linearly with increasing contrast, likely reflecting a dominant parvocellular channel input. Across all patients, the responses in hMT+ of the blind hemisphere no longer showed early saturation but increased linearly with contrast. Given the spatiotemporal parameters used in this study and the known direct subcortical projections from the koniocellular layers of the lateral geniculate nucleus to hMT+, we propose that this altered contrast sensitivity in hMT+ could be consistent with input from the koniocellular pathway.

Blindsight and Unconscious Vision: What They Teach Us about the Human Visual System.

Damage to the primary visual cortex removes the major input from the eyes to the brain, causing significant visual loss as patients are unable to perceive the side of the world contralateral to the damage. Some patients, however, retain the ability to detect visual information within this blind region; this is known as blindsight. By studying the visual pathways that underlie this residual vision in patients, we can uncover additional aspects of the human visual system that likely contribute to normal visual function but cannot be revealed under physiological conditions. In this review, we discuss the residual abilities and neural activity that have been described in blindsight and the implications of these findings for understanding the intact system.

Rehabilitation of damage to the visual brain

Homonymous visual field loss is a common consequence of stroke and traumatic brain injury. It is associated with an adverse functional prognosis and has implications on day-to-day activities such as driving, reading, and safe navigation. Early recovery is expected in around half of cases, and may be associated with a return in V1 activity. In stable disease, recovery is unlikely beyond 3 and certainly 6 months. Rehabilitative approaches generally target three main areas, encompassing a range of techniques with variable success: visual aids aim to expand or relocate the affected visual field; eye movement training builds upon compensatory strategies to improve explorative saccades; visual field restitution aims to improve visual processing within the damaged field itself. All these approaches seem to offer modest improvements with repeated practice, with none clearly superior to the rest. However, a number of areas are demonstrating particular promise currently, including simple web-based training initiatives, and work on neuroimaging and learning. The research interest in this area is encouraging, and it is to be hoped that future trials can better untangle and control for the number of complicated confounds, so that we will be in a much better position to evaluate and select the most appropriate therapy for patients.

Novel brain imaging approaches to understand acquired and congenital neuro-ophthalmological conditions.

PURPOSE OF REVIEW The arrival of large datasets and the on-going refinement of neuroimaging technology have led to a number of recent advances in our understanding of visual pathway disorders. This work can broadly be classified into two areas, both of which are important when considering the optimal management strategies. The first looks at the delineation of damage, teasing out subtle changes to (specific components of) the visual pathway, which may help evaluate the severity and extent of disease. The second uses neuroimaging to investigate neuroplasticity, via changes in connectivity, cortical thickness, and retinotopic maps within the visual cortex. RECENT FINDINGS Here, we give consideration to both acquired and congenital patients with damage to the visual pathway, and how they differ. Congenital disorders of the peripheral visual system can provide insight into the large-scale reorganization of the visual cortex: these are investigated with reference to disorders of the optic chiasm and anophthalmia (absence of the eyes). In acquired conditions, we consider the recent work describing patterns of degeneration, both following single insult and in neurodegenerative conditions. We also discuss the developments in functional neuroimaging, with particular reference to work on hemianopia and the controversial suggestion of cortical reorganization following acquired retinal injury. SUMMARY Techniques for comparing neuro-ophthalmological conditions with healthy visual systems provide sensitive metrics to uncover subtle differences in grey and white matter structure of the brain. It is now possible to compare the massive reorganization present in congenital conditions with the apparent lack of plasticity following acquired damage.

Subcortical pathways to extrastriate visual cortex underlie residual vision following bilateral damage to V1

Residual vision, or blindsight, following damage to the primary visual cortex (V1) has been investigated for almost half a century. While there have been many studies of patients with unilateral damage to V1, far fewer have examined bilateral damage, mainly due to the rarity of such patients. Here we re-examine the residual visual function and underlying pathways of previously studied patient SBR who, as a young adult, suffered bilateral damage restricted to V1 which rendered him cortically blind. While earlier work compared his visual cortex to healthy, sighted participants, here we consider how his visual responses and connections compare to patients with unilateral damage to V1 in addition to sighted participants. Detection of drifting Gabor patches of different contrasts (1%, 5%, 10%, 50% and 100%) was tested in SBR and a group of eight patients with unilateral damage to V1. Performance was compared to the neural activation in motion area hMT+ measured using functional magnetic resonance imaging. Diffusion tractography was also used to determine the white matter microstructure of the visual pathways in all participants. Like the patients with unilateral damage, patient SBR showed increased % BOLD signal change to the high contrast stimuli that he could detect compared to the lower contrast stimuli that were not detectable. Diffusion tractography suggests this information is conveyed by a direct pathway between the lateral geniculate nucleus (LGN) and hMT+ since this pathway had microstructure that was comparable to the healthy control group. In contrast, the pathway between LGN and V1 had reduced integrity compared to controls. A further finding of note was that, unlike control participants, SBR showed similar patterns of contralateral and ipsilateral activity in hMT+, in addition to healthy white matter microstructure in the tract connecting hMT+ between the two hemispheres. This raises the possibility of increased connectivity between the two hemispheres in the absence of V1 input. In conclusion, the pattern of visual function and anatomy in bilateral cortical damage is comparable to that seen in a group of patients with unilateral damage. Thus, while the intact hemisphere may play a role in residual vision in patients with unilateral damage, its influence is not evident with the methodology employed here.

Blindsight relies on a functional connection between hMT+ and the lateral geniculate nucleus, not the pulvinar

When the primary visual cortex (V1) is damaged, the principal visual pathway is lost, causing a loss of vision in the opposite visual field. While conscious vision is impaired, patients can still respond to certain images; this is known as ‘blindsight’. Recently, a direct anatomical connection between the lateral geniculate nucleus (LGN) and human motion area hMT+ has been implicated in blindsight. However, a functional connection between these structures has not been demonstrated. We quantified functional MRI responses to motion in 14 patients with unilateral V1 damage (with and without blindsight). Patients with blindsight showed significant activity and a preserved sensitivity to speed in motion area hMT+, which was absent in patients without blindsight. We then compared functional connectivity between motion area hMT+ and a number of structures implicated in blindsight, including the ventral pulvinar. Only patients with blindsight showed an intact functional connection with the LGN but not the other structures, supporting a specific functional role for the LGN in blindsight.

Visual training in hemianopia alters neural activity in the absence of behavioural improvement: a pilot study

Damage to the primary visual cortex (V1) due to stroke often results in permanent loss of sight affecting one side of the visual field (homonymous hemianopia). Some rehabilitation approaches have shown improvement in visual performance in the blind region, but require a significant time investment.

Motion perception within the blind hemifield

Abstract Background Homonymous visual field deficit is a common clinical problem, most frequently caused by stroke or traumatic brain injury. After 3 months, the visual field loss is generally considered to be permanent. In certain cases, however, information within the blind hemifield can influence behaviour despite the individual often having no conscious awareness of the stimulus. The mechanism and extent of this function remains poorly understood, especially in cases of adult-onset injury. We aimed to investigate the ability of patients with primary visual cortex damage sustained in adulthood to detect and discriminate direction of low-luminance moving targets within the blind visual field. Our hypothesis was that individuals will retain some ability beyond chance, optimally for speeds between 8°/s and 30°/s. Methods Participants were recruited from ophthalmological or stroke services in three UK centres. Testing was done at the John Radcliffe Hospital, Oxford. Of 14 participants recruited, two were excluded after structural imaging showed almost complete damage to the occipital lobe, extending to parietal and temporal lobes including subcortical nuclei. Cases with additional non-correctable visual impairment, or previous neurological disease, were also excluded. All patients had sustained unilateral damage to the primary visual cortex (V1), causing homonymous visual field loss recorded by Humphrey perimetry. Pathological changes had been caused by posterior circulation stroke in 11 patients, or by benign tumour resection in three patients, at least 6 months previously. Psychophysical testing was conducted with a 60Hz monitor at a distance of 68 cm. Visual stimuli consisted of moving black dots (8 dots per deg 2 ) in an aperture of 5° or 8° diameter. Stimulus location was restricted to the scotoma, on a grey background. Each stimulus appeared for 500 ms with jittered onset while the participant fixated on a central black cross. In experiment 1, participants indicated whether a stimulus appeared in the first or second time-interval. If they saw nothing, they were instructed to guess. In experiment 2, participants reported horizontal or vertical direction of motion. In both experiments, stimulus speed was altered parametrically: 4°/s, 8°/s, 20°/s, 32°/s, with 20 trials per condition. Fixation was recorded with an eye tracker, and any trials containing eye movements were removed from analysis. All patients underwent high-resolution structural MRI on the day of testing. Primary outcome was whether patients could demonstrate significant detection or discrimination of visual stimuli above chance. Secondary analysis considered how accuracy altered as a function of stimulus speed. Statistical testing was modelled with a binomial distribution. Written and verbal consent was given by all participants. Ethics approval was provided by the Oxford Research Ethics Committee (ref B 08/H0605/156). Findings Eight patients showed significant detection above chance (patient [P] 1 94%, p Interpretation This study is one of the few to assess visual performance in patients with homonymous visual field deficit due to primary visual cortex damage in adulthood. We have shown that even low-contrast complex motion can elicit blindsight in most patients, with optimum detection and discrimination at speeds of 20°/s. In some cases, particularly for direction discrimination, differences in performance can be subtle. Such trends become more apparent at a group level, or perhaps if patients were to undertake a greater number of trials. Performance as a function of speed echoes research into motion processing in area MT+/V5, where an optimum response is seen for intermediate speeds. It provides further evidence for a direct, perhaps subcortical route to this region when V1 is damaged, which may be present in most patients with these areas intact. That slow motion (postulated to depend upon V1 processing) was discriminated above chance, though small, warrants further investigation. Funding Royal Society, Wellcome Trust, NIHR Oxford Biomedical Research Centre.