Adaptation of Ocular Opponency Neurons Mediates Attention-Induced Ocular Dominance Plasticity

Abstract

Previous research has shown that ocular dominance can be biased by prolonged attention to one eye. The ocular-opponency-neuron model of binocular rivalry has been proposed as a candidate account for this phenomenon. Yet direct neural evidence is still lacking. By manipulating the contrast of dichoptic testing gratings, here we measured the steady-state visually evoked potentials (SSVEPs) at the intermodulation frequencies to selectively track the activities of ocular-opponency-neurons before and after the "dichoptic-backward-movie" adaptation. One hour of adaptation caused a shift of perceptual and neural ocular dominance towards the unattended eye. More importantly, we found a decrease in the intermodulation SSVEP response after adaptation, which was significantly greater when high-contrast gratings were presented to the attended eye than when they were presented to the unattended eye. These results strongly support the view that the adaptation of ocular-opponency-neurons contributes to the ocular dominance plasticity induced by prolonged eye-based attention.

Keywords: Adaptation; Attention; Ocular dominance; Opponency neuron; Steady-state visually evoked potential.

Fig. 1

A Schematic of the ocular-opponency-neuron model [14]. The opponency neurons compute the difference of monocular input signals for a particular orientation preference and retinotopic location, and are activated only when the excitatory signals outweigh the inhibitory signals (solid blue lines for excitatory signals, solid red lines for inhibitory signals). When activated, the opponency neurons also suppress the monocular activity for the opposite eye (dashed red lines). To maintain brevity, the figure does not depict the excitatory and inhibitory inputs received by the left eye-right eye (LE-RE) opponency neuron. Abbreviations: LE, left eye; RE, right eye. B Simplified schematic of the mechanism of adaptation in ocular-opponency-neurons. The horizontal-colored lines depict the firing levels of ocular opponency neurons in the pre- and post-tests, with green/orange/magenta denoting relatively high/moderate/low intensity. Due to a greater extent of adaptation, the firing intensity of AE-UAE neurons decreases more than UAE-AE neurons, resulting in less inhibition of the signals from the unattended eye. Consequently, the ocular dominance shifts towards the unattended eye (green arrow). The black arrows indicate the transmission of visual signals. The solid blue or red arrows indicate the signal inputs from monocular neurons to the ocular opponency neurons. The dotted red or blue arrows indicate the modulation by the ocular opponency neurons or attention. The thickness of the arrow denotes the signal intensity. For simplicity, the orientation tuning information at the monocular processing stage has been omitted in this illustration. Abbreviations: AE, attended eye; UAE, unattended eye.

Fig. 2

Schematic of the experimental paradigm and blob target stimulus in the adaptation phase. A The experimental paradigm known as the “dichoptic-backward-movie”. The red texts are the Chinese subtitles for the movie images. The figure is for demonstration purposes only. The actual movie images are not shown here because of copyright issues. B The blob target (see the gray region around the mouth in this example). This figure displays identifiable images of human faces solely for demonstration purposes. These images were captured from three students in our laboratory who have granted permission for their images to be published.

Fig. 3

Illustration of (A) the process in the formal experiment and (B) the three test conditions. Abbreviations: AE, attended eye; UAE, unattended eye.

Fig. 4

Average topography for SNR at the fundamental frequencies (2f₁ = 6 Hz and 2f₂ = 7.5 Hz) and the intermodulation frequency (f₁+f₂ = 6.75 Hz). Despite the lower SNR of intermodulation responses compared to the fundamental responses, the topography consistently revealed activity in the occipital region.

Fig. 5

The results for (A) the perceptual ocular dominance shift, (B) the blob detection, and (C) the neural ocular dominance shift (n = 33). The bars in A show the grand average perceptual ODI and in C show the grand average neural ODI. The bars in B show the grand average detection percentages of the two eyes in the formal experiment. The individual data are represented by gray lines. Error bars indicate the SEM. **P <0.01; ***P <0.001, paired-sample t-test. Abbreviations: AE, attended eye; UAE, unattended eye.

Fig. 6

A The SSVEP amplitudes at the intermodulation frequency (n = 33). The bars show the grand average SSVEP amplitudes for each condition. AE-UAE means “attended eye-unattended eye” condition, and UAE-AE means “unattended eye-attended eye” condition. The individual data are represented by gray lines. Error bars indicate the SEM. *P <0.05; **P <0.01; n.s., P >0.05, repeated measures ANOVA followed by the post hoc of the paired-sample t-test; the resulting P-value was corrected for multiple comparisons using the FDR method. B The amplitudes differences between the pre- and post-test under the AE-UAE and the UAE-AE conditions. After adaptation, the attenuation of the amplitude in the AE-UAE condition was significantly greater than those in the UAE-AE condition.