More than blindsight: Case report of a child with extraordinary visual capacity following perinatal bilateral occipital lobe injury
Introduction
In primates, including humans, the perception of visual information is mediated by a pathway from the retina to the primary visual cortex (V1, striate cortex) via the lateral geniculate nucleus (LGN) (Felleman and Van Essen, 1991). From V1, the visual information is distributed to extrastriate cortical areas following two parallel pathways: the dorsal visual stream, which progresses to the parietal cortex via the middle temporal area (MT) and mediates visually guided behaviors; and, the ventral visual stream, which reaches the temporal cortex via areas V2, V3 and V4, and mediates object perception (Goodale and Milner, 1992).
Damage to V1, therefore, results in disconnection of the flow of visual information resulting in a blind spot or ‘scotoma’ in the visual field. However, early work pioneered by Larry Weiskrantz and colleagues in the 1970's demonstrated that a patient with a V1 injury was able to detect an object in the scotoma well above chance (Weiskrantz, 1986). Weiskrantz called this phenomenon, whereby a patient's behaviour was reliably controlled by a visual stimulus the patient could not see, ‘blindsight’. Subsequent studies in humans (Barbur et al., 1980, Fendrich et al., 1992, Goebel et al., 2001, Innocenti et al., 1999) and monkeys (Cowey and Stoerig, 1997, Innocenti et al., 1999, Schmid et al., 2010a, Schmid et al., 2010b) have revealed much information on the visual capacity associated with blindsight, demonstrating a remarkable range of residual visual abilities. Much work continues today exploring these spared visual capacities in both monkeys and man (Bridge et al., 2008, Yu et al., 2013).
Identifying the neural substrate responsible for the phenomenon has been slightly more contentious but most studies in humans (Ajina et al., 2015a, Ajina et al., 2015b, Bridge et al., 2010) and monkeys (Rosa et al., 2000, Schmid et al., 2010a, Schmid et al., 2010b) report that neurons in MT of the extrastriate cortex, involved in motion processing, respond to a certain degree in the absence of V1. Furthermore, area MT has been demonstrated to respond to global motion differently in patients following a lesion of V1 in adulthood, where coherence-related activity was more representative of V1 (Tamietto and Morrone, 2016), suggesting that it can take up specific functions of V1 in its absence. This has led researchers to develop hypotheses around alternative visual pathways that bypass V1, including a disynaptic pathway through the K layers of the lateral geniculate nucleus (LGN) (Sincich et al., 2004) and via the medial subdivision of the inferior pulvinar (PIm) (Bridge et al., 2016, Warner et al., 2010). The majority of evidence points towards the LGN being the neural substrate following an adult lesion of V1 (Bridge et al., 2016, Schmid et al., 2010a, Schmid et al., 2010b) but a role for the retinorecipient pulvinar cannot be discounted (Gross, 1991, Rodman et al., 1990).
A consideration that has received little attention and needs further exploration is the age-associated visual capacity following a lesion to V1. Few studies to date have focussed on perinatal V1 injury. Instead, most comprehensive studies have examined the residual visual abilities of adult humans and monkeys that received a V1 injury. This likely emerged as a consequence of the early work by Lambert and colleagues (Lambert et al., 1987) who studied 30 infants with cortical blindness and concluded that they had poor visual outcomes, which they attributed to premature birth. Evidence does exist from patient M.S., however, who received a bilateral lesion to V1 in early life and shows a superior visual capacity to individuals with a similar injury received later in life (Innocenti et al., 1999). Indeed, in some tasks, M.S.’s performance matched that of children of her age. Other patients are also examples of early-life unilateral and bilateral occipital lobe injury who have near normal visual ability (Werth, 2006). One of the most studied cases is patient G.Y., who sustained unilateral V1 damage at the age of 8 years old. G.Y showed remarkable residual visual capacities and has become a representative case of blindsight (Barbur et al., 1980, Bridge et al., 2008, Weiskrantz, 1996). Seminal studies of experimental V1 lesions in macaque monkeys at 5–6 weeks of age determined that monkeys were able to detect stimuli within their scotoma (Moore et al., 1996). As with blindsight, the cortical areas postulated to be responsible for the preserved vision in these cases are the extrastriate areas, including MT which is a visual area known to mature early in humans and monkeys (Bourne and Morrone, 2017, Bourne and Rosa, 2006, Mundinano et al., 2015, Watson et al., 1993), but the pathway/s responsible still remain undetermined.
Here we present the case of a child (B.I.) who received extensive bilateral damage to the occipital cortex within the first two postnatal weeks, but who has an exceptional visual ability. To demonstrate this, we performed an ophthalmological assessment and examined different visual behaviour tasks such as contrast sensitivity, orientation and shape discrimination, color recognition, 2D and 3D object recognition, face discrimination and grasping. Finally, to interrogate which neural pathways might be underpinning his residual visual abilities, we performed structural and diffusion MRI, comparing results with 4 healthy young male controls.
Section snippets
History
Patient B.I., male, at the age of 9 days old suffered from seizures and neonatal hypoglycemia caused by a medium-chain acyl-Co-A dehydrogenase deficiency (MCAD). MRI studies immediately after the incident revealed normal brain characteristics (gyral pattern consistent with gestational age, the ventricular system was normal, no intracranial haemorrhage, normal parenchymal echogenicity and extra-axial spaces, and normal posterior fossa). A second MRI study 20 days later revealed severe acute
Discussion
Patient B.I., despite his extensive bilateral visual cortical damage, has astonishing residual visual abilities. In short, despite the apparent bilateral absence of V1, V2 and other association cortices extending into the parietal lobe, he is not blind, as confirmed through ophthalmic and neuropsychological examination but instead has a remarkably preserved visual ability.
Although we don’t have information between the MRI 20 days after the neonatal hypoglycaemia/ seizures and the one acquired
Conclusion
Considering above described limitations with care, this study suggests that the disynaptic retinal relay through the pulvinar (PI) to area MT is the likely neural substrate for the extensive sparing of visual abilities, including conscious perception, following an early-life lesion of V1 that go well beyond that observed in patients with adult lesions. We cannot exclude the contribution of the LGN-MT pathway to the retained visual abilities and future studies of B.I., including functional MRI,
Acknowledgements
We thank Richard McIntyre of Monash Biomedical Imaging (MBI) for his assistance with MRI acquisition, and MBI for providing gratis scanning. We also thank Alexandra Coros and James Kryklywy for their assistance with some of the behavioural testing. The Australian Regenerative Medicine Institute is supported by grants from the State Government of Victoria and the Australian Government. This work was supported by an NHMRC Project Grant (APP1042893) and an NSERC Discovery Grant to M.A.G. J.A.B. is
References (69)
- et al.
Visual activation of extra-striate cortex in the absence of V1 activation
Neuropsychologia
(2010) - et al.
Adaptive pulvinar circuitry supports visual cognition
Trends Cogn. Sci.
(2016) - et al.
Visual detection in monkeys with blindsight
Neuropsychologia
(1997) - et al.
Conscious, preconscious, and subliminal processing: a testable taxonomy
Trends Cogn. Sci.
(2006) - et al.
Influence of intensity on children's sensitivity to happy, sad, and fearful facial expressions
J. Exp. Child Psychol.
(2009) - et al.
Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients
Vision. Res.
(2001) - et al.
Separate visual pathways for perception and action
Trends Neurosci.
(1992) Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and the inferior temporal cortex
Neuropsychologia
(1991)- et al.
Pulvinar contributions to the dorsal and ventral streams of visual processing in primates
Brain Res Rev.
(2007) Towards a true neural stance on consciousness
Trends Cogn. Sci.
(2006)
SIFT: spherical-deconvolution informed filtering of tractograms
NeuroImage
Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information
NeuroImage
Visual Plasticity: Blindsight Bridges Anatomy andFunction in the Visual System
Curr Biol.
Blindsight in children with congenital and acquired cerebral lesions
Cortex
Preservation of vision by the pulvinar following early-life primary visual cortex lesions
Curr. Biol.
Blindsight revisited
Curr. Opin. Neurobiol.
Misbinding of color and motion in human visual cortex
Curr. Biol.
Motion area V5/MT+ response to global motion in the absence of V1 resembles early visual cortex
Brain
Human blindsight is mediated by an intact geniculo-extrastriate pathway
Elife
New insights in the optic radiations connectivity in the human brain
Invest. Ophthalmol. Vis. Sci.
Human visual responses in the absence of the geniculo-calcarine projection
Brain
Residual vision in patients with retrogeniculate lesions of the visual pathways
Brain
Plasticity of visual pathways and function in the developing brain: is the pulvinar a crucial player?
Front Syst. Neurosci.
Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT)
Cereb. Cortex
Unconscious processing of orientation and color without primary visual cortex
Proc. Natl. Acad. Sci. USA
Residual colour vision in a human hemianope: spectral responses and colour discrimination
Proc. Biol. Sci.
Changes in connectivity after visual cortical brain damage underlie altered visual function
Brain
Parallel colour-opponent pathways to primary visual cortex
Nature
The blindsight saga
Exp. Brain Res.
Transneuronal retrograde degeneration of retinal ganglion cells and optic tract in hemianopic monkeys and humans
Brain
Revision of visual impairment definitions in the International Statistical Classification of Diseases
BMC Med.
Age correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys
Invest Ophthalmol. Vis. Sci.
A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning
Cereb. Cortex
What is perception?
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