Altered neural oscillations underlying visuospatial processing in cerebral visual impairment

Author:

Federici Alessandra1,Bennett Christopher R2,Bauer Corinna M2,Manley Claire E2,Ricciardi Emiliano1,Bottari Davide1,Merabet Lotfi B2ORCID

Affiliation:

1. IMT School for Advanced Studies , 55100 Lucca , Italy

2. The Laboratory for Visual Neuroplasticity, Department of Ophthalmology, Massachusetts Eye and Ear, Harvard Medical School , Boston, MA 02114 , USA

Abstract

Abstract Visuospatial processing deficits are commonly observed in individuals with cerebral visual impairment, even in cases where visual acuity and visual field functions are intact. Cerebral visual impairment is a brain-based visual disorder associated with the maldevelopment of central visual pathways and structures. However, the neurophysiological basis underlying higher-order perceptual impairments in this condition has not been clearly identified, which in turn poses limits on developing rehabilitative interventions. Using combined eye tracking and EEG recordings, we assessed the profile and performance of visual search on a naturalistic virtual reality-based task. Participants with cerebral visual impairment and controls with neurotypical development were instructed to search, locate and fixate on a specific target placed among surrounding distractors at two levels of task difficulty. We analysed evoked (phase-locked) and induced (non-phase-locked) components of broadband (4–55 Hz) neural oscillations to uncover the neurophysiological basis of visuospatial processing. We found that visual search performance in cerebral visual impairment was impaired compared to controls (as indexed by outcomes of success rate, reaction time and gaze error). Analysis of neural oscillations revealed markedly reduced early-onset evoked theta [4–6 Hz] activity (within 0.5 s) regardless of task difficulty. Moreover, while induced alpha activity increased with task difficulty in controls, this modulation was absent in the cerebral visual impairment group identifying a potential neural correlate related to deficits with visual search and distractor suppression. Finally, cerebral visual impairment participants also showed a sustained induced gamma response [30–45 Hz]. We conclude that impaired visual search performance in cerebral visual impairment is associated with substantial alterations across a wide range of neural oscillation frequencies. This includes both evoked and induced components suggesting the involvement of feedforward and feedback processing as well as local and distributed levels of neural processing.

Funder

National Institutes of Health

National Eye Institute

Publisher

Oxford University Press (OUP)

Subject

Neurology,Cellular and Molecular Neuroscience,Biological Psychiatry,Psychiatry and Mental health

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