Preserved extrastriate visual network in a monkey with substantial, naturally occurring damage to primary visual cortex

Author:

Bridge Holly12ORCID,Bell Andrew H134ORCID,Ainsworth Matthew34ORCID,Sallet Jerome13ORCID,Premereur Elsie5ORCID,Ahmed Bashir6ORCID,Mitchell Anna S3ORCID,Schüffelgen Urs13ORCID,Buckley Mark3ORCID,Tendler Benjamin C12ORCID,Miller Karla L12ORCID,Mars Rogier B127ORCID,Parker Andrew J6ORCID,Krug Kristine6ORCID

Affiliation:

1. Wellcome Centre for Integrative Neuroimaging, FMRIB, Oxford University, Oxford, United Kingdom

2. Nuffield Department of Clinical Neurosciences, Oxford University, Oxford, United Kingdom

3. Department of Experimental Psychology, Oxford University, Oxford, United Kingdom

4. MRC Cognition and Brain Sciences Unit, Cambridge, United Kingdom

5. Laboratory for Neuro- and Psychophysiology, KU Leuven, Leuven, Belgium

6. Department of Physiology, Anatomy and Genetics, Oxford University, Oxford, United Kingdom

7. Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands

Abstract

Lesions of primary visual cortex (V1) lead to loss of conscious visual perception with significant impact on human patients. Understanding the neural consequences of such damage may aid the development of rehabilitation methods. In this rare case of a Rhesus macaque (monkey S), likely born without V1, the animal’s in-group behaviour was unremarkable, but visual task training was impaired. With multi-modal magnetic resonance imaging, visual structures outside of the lesion appeared normal. Visual stimulation under anaesthesia with checkerboards activated lateral geniculate nucleus of monkey S, while full-field moving dots activated pulvinar. Visual cortical activation was sparse but included face patches. Consistently across lesion and control monkeys, functional connectivity analysis revealed an intact network of bilateral dorsal visual areas temporally correlated with V5/MT activation, even without V1. Despite robust subcortical responses to visual stimulation, we found little evidence for strengthened subcortical input to V5/MT supporting residual visual function or blindsight-like phenomena.

Funder

Wellcome

Biotechnology and Biological Sciences Research Council

Medical Research Council

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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