Interocular suppression in the primary visual cortex: a possible neural basis of binocular rivalry

Abstract

In an attempt to demonstrate a physiological basis for the alternating suppression of perception when the two eyes view very different contours (binocular rivalry), we studied the responses of neurons in the lateral geniculate nucleus (LGN) and area 17 of cats for drifting gratings of different orientation, spatial frequency and contrast in the two eyes. Almost half of the LGN neurons studied exhibited modest inhibitory interocular interaction, but independent of interocular differences in orientation. Monocularly driven units in layer 4 of area 17 behaved similarly. However, for the majority of binocular cortical cells, the response to a grating of optimal orientation in one eye was suppressed by a grating of very different orientation shown to the other eye, over a wide range of spatial frequency and independent of relative spatial phase. This interocular suppression exhibits a remarkable non-linearity: a grating of non-preferred orientation in one eye causes significant interocular suppression only if the neuron is already responding to an appropriate stimulus in the other eye [Sengpiel and Blakemore (1994) Nature, 368, 847-850]. We propose that the switches in perceptual dominance during binocular rivalry depend on interocular interactions at the level of binocular neurons of the primary visual cortex, which might involve intracortical inhibition between adjacent ocular dominance columns. The spontaneous alternations in perceptual suppression that occur during prolonged viewing of rivalrous patterns remain to be explained, although significant variation in the strength of neuronal suppression in such conditions was occasionally seen.

Does direction of walking impact binocular rivalry between competing patterns of optic flow?

“…Decades ago, binocular rivalry was considered by many to be a bottom-up driven visual phenomenon whose dynamics were determined primarily by the interplay of adaptation and inhibition within early visual cortex (Levelt, 1965;Matsuoka, 1984;Mueller, 1990;Lehky & Blake, 1991;Sengpiel et al, 1995). But that view began to change as evidence mounted for the involvement influences originating beyond early visual cortex, influences including attentional modulation of dominance at the onset of rivalry (Mitchell et al, 2004) and interocular grouping in the formation of global, coherent dominance during rivalry (e.g., Kovács et al, 1996).…”

Psychophysical evidence for two routes to suppression before binocular summation of signals in human vision

“…One view is that rivalry is image-based rather than eye-based (Kovacs et al, 1996;Logothetis et al, 1996), though recent work has found that whatever the drive, the consequences can be observed as early as the LGN (Haynes et al, 2005;Wunderlich et al, 2005). Notwithstanding the involvement of higher-order interactions Logothetis et al, 1996;Logothetis, 1998;Macknik and Martinez-Conde, 2004;Tse et al, 2005), it now seems likely that a substantial contribution to binocular rivalry arises from interocular suppression (Sengpiel et al, 1995;Harrad, 1996;Wilson, 2003;Lee and Blake, 2004;Freeman et al, 2005). Nevertheless, it has been difficult to determine the origins of the effects observed in various brain areas within either functional or anatomical maps (Polonsky et al, 2000;Haynes et al, 2005;Lee et al, 2005;Tse et al, 2005;Wunderlich et al, 2005).…”

“…The stimuli used in studies of XOS are similar to those frequently used in studies of another, presumably related form of suppression (Sengpiel et al, 1995;Harrad, 1996;Brown et al, 1999) known as binocular rivalry. In a typical experiment, very different images (e.g.…”

“…The last two accounts are applicable only when the mask and test are presented to the same eye (monoptic presentation) and overlap in space and time. However, in cat at least, XOS is not a purely ipsiocular process because when an oriented grating and crossoriented mask are presented to different eyes (dichoptic presentation), suppression is evident in striate cells (Sengpiel et al, 1995;Walker et al, 1998;Li et al, 2005;Sengpiel and Vorobyov, 2005). Although interocular suppression has been found in the LGN (e.g.…”

Alteration of Interocular Suppression Following Monocular Homogeneous Stimulus

“…Contralateral dominance might thus be based on suppression properties at early neural sites in the visual pathway (Sengpiel & Blakemore, 1994;Sengpiel, Blakemore, & Harrad, 1995). The dominance of ipsilateral view, on the other hand, may indicate the influence of sustained attention to a stimulus in the primed eye through the binocular correspondence stage (Ooi & He, 1999).…”