Population representation of visual information in areas V1 and V2 of amblyopic macaques

Abstract

Amblyopia is a developmental disorder resulting in poor vision in one eye. The mechanism by which input to the affected eye is prevented from reaching the level of awareness remains poorly understood. We recorded simultaneously from large populations of neurons in the supragranular layers of areas V1 and V2 in 6 macaques that were made amblyopic by rearing with artificial strabismus or anisometropia, and 1 normally reared control. In agreement with previous reports, we found that cortical neuronal signals driven through the amblyopic eyes were reduced, and that cortical neurons were on average more strongly driven by the non-amblyopic than by the amblyopic eyes. We analyzed multiunit recordings using standard population decoding methods, and found that visual signals from the amblyopic eye, while weakened, were not degraded enough to explain the behavioral deficits. Thus additional losses must arise in downstream processing. We tested the idea that under monocular viewing conditions, only signals from neurons dominated by – rather than driven by – the open eye might be used. This reduces the proportion of neuronal signals available from the amblyopic eye, and amplifies the interocular difference observed at the level of single neurons. We conclude that amblyopia might arise in part from degradation in the neuronal signals from the amblyopic eye, and in part from a reduction in the number of signals processed by downstream areas.

Linking V1 Activity to Behavior

“…Several recent studies have looked at the performance of various decoders based on multiple simultaneously recorded, well-isolated single neurons or multi-unit sites (nonisolated neural signals) in V1 of anesthetized or awake, fixating macaques (Graf et al 2011, Berens et al 2012, Shooner et al 2015, Arandia-Romero et al 2016). Two common findings emerge from these studies.…”

Covert spatial attention is functionally intact in amblyopic human adults

“…Interestingly, quantitative analyses show that the extent of neural abnormalities in V1 cannot explain the full range of visual deficits in amblyopia (Bi et al, 2011; Kiorpes, Kiper, O'Keefe, Cavanaugh, & Movshon, 1998; Kiorpes & McKee, 1999; Kiorpes & Movshon, 2004; Shooner et al, 2015). This may be due, at least in part, to a reduced strength of amblyopic eye input to higher level areas (Anderson, Holliday, & Harding, 1999; Anderson & Swettenham, 2006).…”

“…This may be due, at least in part, to a reduced strength of amblyopic eye input to higher level areas (Anderson, Holliday, & Harding, 1999; Anderson & Swettenham, 2006). Thus, whereas V1 anomalies may be at the root of amblyopic impairments, they are likely to be amplified by the progressive degradation of feed-forward neural signals in the dorsal and ventral pathways (Barnes, Hess, Dumoulin, Achtman, & Pike, 2001; Choi et al, 2001; Conner, Odom, Schwartz, & Mendola, 2007; El-Shamayleh, Kiorpes, Kohn, & Movshon, 2010; Goodyear, Nicolle, Humphrey, & Menon, 2000; Ho & Giaschi, 2009; Imamura et al, 1997; Kiorpes, 2006; Kiorpes et al, 1998; Kiorpes & Movshon, 1996; Levi, 2006; X. Li, Dumoulin, Mansouri, & Hess, 2007; Muckli et al, 2006; Secen, Culham, Ho, & Giaschi, 2011; Shooner et al, 2015; Sincich, Jocson, & Horton, 2012). Indeed, several studies have shown reduced levels of activation for amblyopes than neurotypical observers as far downstream as parietal and ventral temporal cortex (Ho & Giaschi, 2009; Hyvarinen, Hyvarinen, & Linnankoski, 1981; Lerner et al, 2006; Secen et al, 2011; review by Anderson & Swettenham, 2006).…”

A window into visual cortex development and recovery of vision: Introduction to the Vision Research special issue on Amblyopia

“…Using multi-electrode recordings from V1 and V2 in macaques with experimentally induced amblyopia, Shooner et al (2015) demonstrated that more information from the amblyopic eye is available at an early stage of cortical processing than would be expected based on behavioral contrast sensitivity losses. This implies deficits in downstream processing.…”

“…This implies deficits in downstream processing. Shooner et al (2015) identified a reduction in the relative proportion of signals passing to extrastriate areas due to sub-optimal pooling of neural information from the …”