Adapting our understanding of cerebral visual impairment

Investigators explored whether visuospatial deficits in CVI are explained solely based on dorsal stream dysfunction. Image credit: ©Katynn – stock.adobe.com

Cerebral (or cortical) visual impairment (CVI), the most common cause of visual impairment in paediatric patients in developed countries,¹ is a broad term that covers brain-based visual disorders that damage and/or cause maldevelopment of the retrochiasmal visual processing areas in patients who do not have a major ocular disease.

Lotfi Merabet, OD, PhD, MPH, director of the Laboratory for Visual Neuroplasticity, Department of Ophthalmology, Massachusetts Eye and Ear, Harvard Medical School, Boston, has dedicated his career to the dual goal of unraveling the complexities of CVI and developing assistive devices that aid patients living with visual impairment.

In a recent publication,² he and his team investigated visuospatial processing impairments in CVI and unexpectedly uncovered a previously unrecognised response in the ventral visual processing stream in these patients. This recognition led to speculation that the impaired visuospatial processing in CVI is associated with differential recruitment of the dorsal and ventral visual streams, two key pathways implicated with the processing of visual information.

Stepping stones

Based on previous studies dating back to the mid-1990s,^3-11 CVI was reported to make performing visuospatial tasks especially difficult, even in the presence of normal or near-normal visual acuity and visual field function.

From this research, the terms “dorsal stream dysfunction”^12,13 and “dorsal stream vulnerability”^14,15 emerged, which proposed to describe the common prevalence of visuospatial impairments in CVI, i.e., impaired visual search, deficits in complex motion processing and spatial awareness of surroundings, and their purported association with impaired processing along the dorsal visual stream, Dr Merabet recounted.

Pivotal studies^16,17 provided objective evidence for impaired dorsal stream function but spared ventral stream function in individuals with neurodevelopmental disorders, including CVI.

Investigating other cortical regions

Even with the previously cited studies suggesting that the visuospatial deficits in CVI may be specific to dorsal stream dysfunction, no study before his latest research,² Dr Merabet noted, has collectively examined the multiple cortical regions beyond the dorsal stream, including the early visual cortex (EVC), the ventral visual stream, and the frontal cortex that may or may not be implicated in the visuospatial impairments in the CVI population. The obvious question that arose was: are the visuospatial deficits in CVI explained solely based on dorsal stream dysfunction?

Focus on the ventral stream

In this new research,² Dr Merabet and colleagues designed visual search tasks and used functional magnetic resonance imaging (fMRI) to investigate the activity in the EVC, frontal cortex and the ventral visual stream that previously had not been investigated. They compared visual search performance using eye tracking in 14 individuals with CVI (8 males, 6 females; mean age, 19.57) and to 16 neurotypical participants (5 males, 11 females; mean age, 22.63 years). The participants were instructed to perform a virtual reality–based visual search task during which participants searched for, located, and pursued a human target walking in a moving crowd. They also studied the effect of task difficulty (load) on overall performance by manipulating the size of the surrounding crowd, i.e., distractors.

All study participants had visual acuities, intact visual field function within the area corresponding to the visual stimulus presentation, and fixation and binocular ocular motor function sufficient for completing the task requirements and eye-tracking calibration.

“We found that the visual search performance was impaired in CVI participants compared to neurotypicals. Further, fMRI revealed significantly reduced activation in regions along the dorsal stream in CVI compared with neurotypicals, consistent [with] the dorsal stream dysfunction in CVI hypothesis,” Dr Merabet said.

However, a highly interesting result was that regions along the ventral stream showed the opposite response profile with greater activation compared with neurotypicals, with task difficulty disproportionately affecting the CVI participants. Finally, activation within the EVC and frontal cortex did not differ significantly between the two groups, he reported.

The investigators concluded, “These results suggested that the impaired visuospatial processing abilities in CVI are associated with differential recruitment of the dorsal and ventral visual streams, likely resulting from impaired selective attention. Specifically, it appears that this observed increase in activation in the ventral stream actually reflects a maladaptive mechanism. Thus, impaired processing and interactions between both the dorsal and ventral streams appear to contribute to the known visuospatial impairment in individuals with CVI, suggesting a more complex clinical profile characterising this condition. A greater understanding of the nature of higher order visual processing deficits (particularly in the context of naturalistic viewing conditions) is crucial to better characterise the nature of this condition, as well as potentially help devise appropriate habilitative strategies for individuals with CVI.”

Dr Merabet was joined in the study under discussion by Dr Zahide Pamir (lead author) from the Department of Psychology and Department of Neuroscience, Bilkent University, Üniversiteler, Çankaya/Ankara, Turkey, and Aysel Sabuncu Brain Research Center, Bilkent University, Üniversiteler, Çankaya/Ankara; Claire E. Manley from the Laboratory for Visual Neuroplasticity, Department of Ophthalmology, Massachusetts Eye and Ear, Harvard Medical School, Boston; Dr Corinna M. Bauer from the Lab for Neuroimaging and Vision Science, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston; Dr Peter J. Bex from the Translational Vision Laboratory, Department of Psychology, Northeastern University, Boston; and Dr Daniel D. Dilks from the Department of Psychology, Emory University, Atlanta.

References

1. Solebo AL, Teoh L, Rahi J. Epidemiology of blindness in children. Arch Dis Child. 2017;102(9):853-857. doi:10.1136/archdischild-2016-310532

2. Pamir Z, Manley CE, Bauer CM, Bex PJ, Dilks DD, Merabet LB. Visuospatial processing in early brain-based visual impairment is associated with differential recruitment of dorsal and ventral visual streams. Cereb Cortex. 2024;34(5):bhae203. doi:10.1093/cercor/bhae203

3. Boot FH, Pel JJ, van der Steen J, Evenhuis HM. Cerebral visual impairment: which perceptive visual dysfunctions can be expected in children with brain damage? A systematic review. Res Dev Disabil. 2010;31(6):1149-1159. doi:10.1016/j.ridd.2010.08.001

4. Dutton GN. The spectrum of cerebral visual impairment as a sequel to premature birth: an overview. Doc Ophthalmol. 2013;127(1):69-78. doi:10.1007/s10633-013-9382-1

5. Dutton GN, McKillop EC, Saidkasimova S. Visual problems as a result of brain damage in children. Br J Ophthalmol. 2006:90(8):932-933.

6. Dutton GN, Saaed A, Fahad B, et al. Association of binocular lower visual field impairment, impaired simultaneous perception, disordered visually guided motion and inaccurate saccades in children with cerebral visual dysfunction-a retrospective observational study. Eye (Lond). 2004;18(1):27-34. doi:10.1038/sj.eye.6700541

7. Jacobson L, Ek U, Fernell E, Flodmark O, Broberger U. Visual impairment in preterm children with periventricular leukomalacia–visual, cognitive and neuropaediatric characteristics related to cerebral imaging. Dev Med Child Neurol. 1996;38(8):724-735. doi:10.1111/j.1469-8749.1996.tb12142.x

8. Lam FC, Lovett F, Dutton GN. Cerebral visual impairment in children: a longitudinal case study of functional outcomes beyond the visual acuities. J Visual Impair Blin. 2010:104(10):625-635.

9. Manley CE, Bennett CR, Merabet LB. Assessing Higher-order visual processing in cerebral visual impairment using naturalistic virtual-reality-based visual search tasks. Children (Basel). 2022;9(8):1114. doi:10.3390/children9081114

10. Manley CE, Bauer CM, Bex PJ, Merabet LB. Impaired visuospatial processing in cerebral visual impairment revealed by performance on a conjunction visual search task. Br J Vis Impair. 2023:42(3):02646196231187550./10.1177/ 02646196231187550.

11. McDowell N, Dutton GN. Hemianopia and features of Bálint syndrome following occipital lobe hemorrhage: identification and patient understanding have aided functional improvement years after onset. Case Rep Ophthalmol Med. 2019;2019:3864572. doi:10.1155/2019/3864572

12. Dutton GN. 'Dorsal stream dysfunction' and 'dorsal stream dysfunction plus': a potential classification for perceptual visual impairment in the context of cerebral visual impairment?. Dev Med Child Neurol. 2009;51(3):170-172. doi:10.1111/j.1469-8749.2008.03257.x

13. Macintyre-Beon C, Ibrahim H, Hay I, et al. Dorsal stream dysfunction in children: a review and an approach to diagnosis and management. Curr Pediatr Rev. 2010:6(3):166-182. doi:10.2174/157339610793743 895

14. Braddick O, Atkinson J, Wattam-Bell J. Normal and anomalous development of visual motion processing: motion coherence and 'dorsal-stream vulnerability'. Neuropsychologia. 2003;41(13):1769-1784. doi:10.1016/s0028-3932(03)00178-7

15. Pamir Z, Bauer CM, Bailin ES, Bex PJ, Somers DC, Merabet LB. Neural correlates associated with impaired global motion perception in cerebral visual impairment (CVI). Neuroimage Clin. 2021;32:102821. doi:10.1016/j.nicl.2021.102821

16. Atkinson J. The Davida Teller Award Lecture, 2016: Visual brain development: a review of "Dorsal Stream Vulnerability"-motion, mathematics, amblyopia, actions, and attention. J Vis. 2017;17(3):26. doi:10.1167/17.3.26

17. Merabet LB, Manley CE, Pamir Z, Bauer CM, Skerswetat J, Bex PJ. Motion and form coherence processing in individuals with cerebral visual impairment. Dev Med Child Neurol. 2023;65(10):1379-1386. doi:10.1111/dmcn.15591.

Lotfi B. Merabet, OD, PhD, MPH | E: lotfi_merabet@meei.harvard.edu

Merabet is an associate professor of ophthalmology at Massachusetts Eye and Ear, Harvard Medical School, in Boston. He has no financial interest in this subject matter.

This work was supported by grants from the National Institutes of Health/National Eye Institute (NIH/NEI R01 EY030973).