Bypassing V1: Orientation selectivity in hMT+ of cortically-blinded patients

Abstract

Orientation selectivity is a core property of primary visual cortex (V1) in mammals, yet patients with V1 damage can relearn orientation discrimination at trained, blind-field locations. What neural machinery underlies such recovery? Here, we explore 2 possible mechanisms involving plastic changes in 1) perilesional V1, and/or 2) visual pathways that bypass V1 and transfer information directly to extrastriate cortex, which uses it to construct orientation-selective signals. We conducted two fMRI experiments at 3T and 7T, in which 4 V1-stroke patients (age: 17–63 years, 2 females, 3 right V1 strokes) viewed oriented gratings while performing a demanding task at fixation. In Expt 1, stimuli were large (10° radius), sinusoidal gratings centered on fixation, whose orientation progressed through 16 evenly-spaced angles (0-180°) over a 24s period (Freeman et al. 2011). In Expt 2, stimuli were small (2.5° radius), oriented (45° or 135°), sinusoidal gratings, presented peripherally (7.1-8.6° eccentricity), deep within the blind or intact visual hemifield. In Expt 1, we observed reliable, orientation-selective responses in ipsilesional hMT+, which is well-known to retain activity after V1 damage (Ffytche et al., 1996; Baseler et al., 1999; Morland et al., 2004; Ajina et al., 2015; Papanikolaou et al., 2019). However, because the large grating stimulated the intact field, the blind field, and the spared visual field simultaneously, we could not rule out a contribution from peri-lesional V1. In Expt 2, we also observed reliable responses in ipsilesional hMT+ for oriented stimuli entirely inside the blind field. Ongoing analyses aim to assess the strength and selectivity of these hMT+ responses, but the fact remains that they may have been elicited in the absence of orientation-selective input from V1. This would suggest a remarkable level of plasticity for this fundamental, low-level visual feature and poses questions regarding how it arises in the residual visual circuitry.