Degraded attentional modulation of cortical neural populations in strabismic amblyopia

Abstract

Behavioral studies have reported reduced spatial attention in amblyopia, a developmental disorder of spatial vision. However, the neural populations in the visual cortex linked with these behavioral spatial attention deficits have not been identified. Here, we use functional MRI–informed electroencephalography source imaging to measure the effect of attention on neural population activity in the visual cortex of human adult strabismic amblyopes who were stereoblind. We show that compared with controls, the modulatory effects of selective visual attention on the input from the amblyopic eye are substantially reduced in the primary visual cortex (V1) as well as in extrastriate visual areas hV4 and hMT+. Degraded attentional modulation is also found in the normal-acuity fellow eye in areas hV4 and hMT+ but not in V1. These results provide electrophysiological evidence that abnormal binocular input during a developmental critical period may impact cortical connections between the visual cortex and higher level cortices beyond the known amblyopic losses in V1 and V2, suggesting that a deficit of attentional modulation in the visual cortex is an important component of the functional impairment in amblyopia. Furthermore, we find that degraded attentional modulation in V1 is correlated with the magnitude of interocular suppression and the depth of amblyopia. These results support the view that the visual suppression often seen in strabismic amblyopia might be a form of attentional neglect of the visual input to the amblyopic eye.

Covert spatial attention is functionally intact in amblyopic human adults

“…Future research will establish if the reduced attentional modulation found for contrast detection (Hou et al, 2016) is also present for the discrimination task we employed here. We encourage future studies investigating these and other aspects of attention with neurotypical and special populations to take advantage of precise terminology and well-established experimental protocols, such as those employed in this study, which allow experimenters to reliably isolate, manipulate, and measure particular types of attention.…”

“…They found that amblyopes significantly underestimated the number of targets when using their amblyopic eye compared to the nonamblyopic eye and controls across all cueing conditions, which they argue to be evidence for a “high-level deficit.” Note that even though their amblyopes do exhibit a robust and reliable endogenous attention effect (valid vs. invalid cueing) of the same magnitude as that shown by visually intact observers, this study is often cited as one of the primary studies providing evidence for a visual attention deficit in amblyopia (Farzin & Norcia, 2011; Ho et al, 2006; Hou et al, 2016; Levi, 2013; Levi & Tripathy, 2006; McKee, Levi, Schor, & Movshon, 2016; Secen et al, 2011; Tripathy & Levi, 2008). …”

“…These deficits include enhanced crowding as well as problems with stimulus localization, contour integration, texture and second-order pattern perception, shape discrimination, motion sensitivity, stereopsis, eye movements, and oculomotor coordination. Although typically characterized as a foveal visual disorder, amblyopia-related deficits and their neural markers are present across the visual field, including the perifovea (Bankó, Körtvélyes, Németh, & Vidnyánszky, 2014; Ho et al, 2006; Hou, Kim, Lai, & Verghese, 2016; Katz, Levi, & Bedell, 1984). …”

“…However, the authors attributed their results to a deficit of visual attention in amblyopia, inferring its contribution to their tasks without directly manipulating it. Indeed, only two studies have used attentional cues to investigate voluntary attention in human strabismic amblyopes: Sharma et al (2000) assessed its behavioral effects on numerosity estimation, and Hou et al (2016) explored the underlying neural correlates in a contrast detection task.…”

“…In the first study to directly investigate the underlying neural correlates of voluntary visual attention in strabismic amblyopia, Hou et al (2016) used fMRI-informed EEG source imaging to measure the amplitudes of steady-state visual evoked potentials (SSVEPs) as observers were cued (100% validity) to voluntarily attend to one hemifield at a time during a contrast change detection task. Overall, SSVEP amplitudes corresponding to visual inputs from both eyes of the amblyopes were significantly reduced relative to visually intact controls.…”