Asymmetric Dichoptic Masking in Visual Cortex of Amblyopic Macaque Monkeys

Abstract

In amblyopia, abnormal visual experience leads to an extreme form of eye dominance, in which vision through the nondominant eye is degraded. A key aspect of this disorder is perceptual suppression: the image seen by the stronger eye often dominates during binocular viewing, blocking the image of the weaker eye from reaching awareness. Interocular suppression is the focus of ongoing work aimed at understanding and treating amblyopia, yet its physiological basis remains unknown. We measured binocular interactions in visual cortex of anesthetized amblyopic monkeys (female ), using 96-channel "Utah" arrays to record from populations of neurons in V1 and V2. In an experiment reported recently (Hallum et al., 2017), we found that reduced excitatory input from the amblyopic eye (AE) revealed a form of balanced binocular suppression that is unaltered in amblyopia. Here, we report on the modulation of the gain of excitatory signals from the AE by signals from its dominant fellow eye (FE). Using a dichoptic masking technique, we found that AE responses to grating stimuli were attenuated by the presentation of a noise mask to the FE, as in a normal control animal. Responses to FE stimuli, by contrast, could not be masked from the AE. We conclude that a weakened ability of the amblyopic eye to modulate cortical response gain creates an imbalance of suppression that favors the dominant eye. In amblyopia, vision in one eye is impaired as a result of abnormal early visual experience. Behavioral observations in humans with amblyopia suggest that much of their visual loss is due to active suppression of their amblyopic eye. Here we describe experiments in which we studied binocular interactions in macaques with experimentally induced amblyopia. In normal monkeys, the gain of neuronal response to stimulation of one eye is modulated by contrast in the other eye, but in monkeys with amblyopia the balance of gain modulation is altered so that the weaker, amblyopic eye has little effect while the stronger fellow eye has a strong effect. This asymmetric suppression may be a key component of the perceptual losses in amblyopia.

Amblyopic Suppression: Passive Attenuation, Enhanced Dichoptic Masking by the Fellow Eye or Reduced Dichoptic Masking by the Amblyopic Eye?

“…Under conditions of normal binocular viewing (same stimuli in both eyes), this increased masking would result in a suppression of low spatial-frequency information seen through the amblyopic eye. This conclusion in humans with amblyopia gains support from a recent nonhuman primate model of amblyopia in which it has also been shown that there is reduced dichoptic masking by cells driven by the amblyopic eye 25 ; this, in principle, could be due to attenuation (a threshold offset) or reduced contrast gain per se. Shooner et al 25 didn't present their stimuli at a constant suprathreshold contrast as we were able to do psychophysically.…”

“…This conclusion in humans with amblyopia gains support from a recent nonhuman primate model of amblyopia in which it has also been shown that there is reduced dichoptic masking by cells driven by the amblyopic eye 25 ; this, in principle, could be due to attenuation (a threshold offset) or reduced contrast gain per se. Shooner et al 25 didn't present their stimuli at a constant suprathreshold contrast as we were able to do psychophysically. Therefore, their result supports the reduced amblyopic-to-fellow eye inhibition but is not definitive about its cause.…”

Plasticity and Adaptation in Adult Binocular Vision

“…Specifically, measurements from the primary visual cortex of non-human primates reared to model amblyopia suggest only a weak shift in neuronal ocular dominance preferences in primary visual cortex -more notable effects include an overall reduction in binocularly responsive neurons, as well as abnormal monocular receptive fields for the weaker eye [38]. Consistent with this observation, physiological measurements in primates suggest that the visual cortex of adult amblyopes is characterized not only by reduced excitatory drive from the weaker eye, but also by active, ongoing interocular suppression of the weaker eye, perhaps reflecting asymmetric gain control [39]. Primate amblyopia models have also revealed changes in tuning and interocular suppression beyond V1 [40].…”

Abnormal Monocular and Dichoptic Temporal Synchrony in Adults with Amblyopia

“…11 Huang and colleagues 12 also reported that the amblyopic eye's temporal synchrony sensitivity, which is defined as the minimum degree of temporal phase difference that enables participants to discriminate that the target is flickering asynchronously in time, was considerably higher than that of the fellow eye. These visual deficits in spatial and temporal processes are considered to be from some abnormalities in the developed visual system in the brain [13][14][15][16][17][18] rather than those in the eye. Since the problems reside in the neural circuitry rather than anatomy of the eye, they cannot be directly corrected optically.…”