Neural Dynamics during Binocular Rivalry: Indications from Human Lateral Geniculate Nucleus

Abstract

When two sufficiently different stimuli are presented to each eye, perception alternates between them. This binocular rivalry is conceived as a competition for representation in the single stream of visual consciousness. The magnocellular (M) and parvocellular (P) pathways, originating in the retina, encode disparate information, but their potentially different contributions to binocular rivalry have not been determined. Here, we used functional magnetic resonance imaging to measure the human lateral geniculate nucleus (LGN), where the M and P neurons are segregated into layers receiving input from a single eye. We had three participants (one male, two females) and used achromatic stimuli to avoid contributions from color opponent neurons that may have confounded previous studies. We observed activity in the eye-specific regions of LGN correlated with perception, with similar magnitudes during rivalry or physical stimuli alternations, also similar in the M and P regions. These results suggest that LGN activity reflects our perceptions during binocular rivalry and is not simply an artifact of color opponency. Further, perception appears to be a global phenomenon in the LGN, not just limited to a single information channel.

Keywords: binocular rivalry; fMRI; lateral geniculate nucleus; magnocellular; parvocellular.

Figure 1.

The structure of lateral geniculate nucleus. a, the magnocellular-parvocellular structure; b, the eye-specific structure. C, Contralateral eye; I, ipsilateral eye; M, magnocellular; P, parvocellular. Tracings were generated based on the study by Andrews et al. (1997).

Figure 2.

The stimulus presentation for the experimental conditions. Rivalry was the conventional binocular rivalry paradigm in which each eye was presented with a different stimulus, and rotations were counterbalanced across the eyes in the actual experiment. Replay was the physical alternations of the stimuli matching with the perceptual reports of the observer during a previous rivalry block. IOS Rivalry was the interocular switch paradigm in which the rivalry stimuli swapped between the eyes in every few seconds, randomly chosen between 2.5 and 3.5 s.

Figure 3.

Histograms for durations of exclusive perceptions during rivalry. Riv, Rivalry; CW, clockwise rotation; –CW, counterclockwise rotation. In the third column are the histograms collapsed across the two rotations for exclusive perceptions. Black lines reflect the median duration. Bin interval is 1 s.

Figure 4.

GLM results for rivalry and replay in the M and P regions of LGNs. a, Coronal slices of each LGN showing the z scores for the rivalry−replay contrast. The red line delimits the boundary between the M and P regions according to their T1 relaxation time (Yildirim et al., 2022). *p < 0.05, uncorrected for multiple comparisons for voxels. b, Scatterplots of the M and P voxels, indicated by their T1 relaxation time in seconds on the x-axis, showing similar suppression for rivalry and replay. The suppression index on the y-axis was calculated by the B weights. For illustration purposes, the voxels with indices beyond 10 and −10 were plotted at 10 and −10, respectively. Black lines indicate the mean suppression indices for the M and P voxels. Error bars are the SEM. **p = 0.02, Bonferroni corrected for six LGNs.

Figure 5.

fMRI activity around the exclusive eye perceptions during rivalry and replay. The x-axis shows the time around when the stable perception started (time 0), indicated by the participant’s perceptual reports. The y-axis shows the difference in the percentage fMRI signal for the CL eye perceptions versus IL eye perceptions. Error shades are 95% CIs. *p < 0.05.