Intracortical Origins of Interocular Suppression in the Visual Cortex

Abstract

The response of neurons in the primary visual cortex to an optimally oriented grating is usually suppressed quite dramatically when a second grating of, for example, orthogonal orientation is superimposed. Such "cross-orientation suppression" has been implicated in the generation of cortical orientation selectivity and local response normalization. Until recently, little experimental evidence was available concerning the neurophysiological substrate of this phenomenon, although an involvement of intracortical inhibition was commonly assumed. However, Freeman et al. (2002) proposed that cortical cross-orientation suppression is caused by suppression in the thalamus and depression at geniculocortical synapses. Here, we examine a dichoptic form of cross-orientation suppression, termed interocular suppression and thought to be involved in binocular rivalry (Sengpiel et al., 1995a). We show that its dependency on the drift rate of the suppressing stimulus is consistent with a cortical origin; unlike monocular cross-orientation suppression, it cannot be evoked by very fast-moving stimuli. Moreover, we find that previous adaptation to the orthogonal stimulus essentially eliminates interocular suppression. Because adaptation is a cortical phenomenon, this result also argues in favor of a cortical locus of suppression, again unlike monocular cross-orientation suppression, which is not affected by adaptation to the suppressor (Freeman et al., 2002). Finally, interocular suppression is greatly reduced in the presence of the GABA antagonist bicuculline. Together, our study demonstrates that interocular suppression is substantially different from monocular cross-orientation suppression and is mediated by inhibitory circuitry within the visual cortex.

A common contrast pooling rule for suppression within and between the eyes

“…Stage 1 can also accommodate masking from within and between the eyes across a range of orientations and spatial frequencies (Baker et al, 2007b;Baker & Meese, 2007). Elsewhere (Baker et al, 2007b), we have suggested that the two routes to suppression might exert their influence at distinct sequential stages (''stage 1a'' and ''stage 1b'') and speculated (Meese & Holmes 2002;Baker et al, 2007b) that the first of these stages is in the LGN (or retina, or layer 4 of visual cortex), for which there is physiological evidence (Freeman et al, 2002;Bonin et al, 2005;Li et al, 2005;Sengpiel & Vorobyov, 2005;Nolt et al, 2007) and for which the excitatory exponent is low (Derrington & Lennie, 1984;Sclar et al, 1990;Felisberti & Derrington, 1999) [though higher exponents (~2) are also found; Sclar et al, 1990;Felisberti & Derrington, 2001].…”

“…Models of suppressive contrast gain control have prompted a resurgence of interest in ocular interactions in psychophysics (Meese & Hess, 2004;Maehara & Goryo, 2005;Ding & Sperling, 2006;Meese et al, 2006;Tsuchiya et al, 2006;Medina et al, 2007;Baker et al, 2007aBaker et al, , 2007bWeiler et al, 2007), electrophysiology (Walker et al 1998;Truchard et al, 2000;Li et al, 2005;Sengpiel & Vorobyov, 2005), and functional imaging (Büchert et al, 2002). These studies have driven the development of binocular models of masking, where interocular suppression forms part of the divisive contrast gain control (Walker et al, 1998;Meese & Hess, 2004;Maehara & Goryo, 2005;Meese et al, 2006;Baker et al, 2007a).…”

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

“…Early work supposed that XOS is caused by intra-cortical inhibition (Morrone et al, 1987;Heeger, 1992), but recent studies of cat physiology have challenged this view. For example, mask stimuli that drift or flicker too quickly to excite most cortical cells will nevertheless produce XOS, implying precortical involvement (Freeman et al, 2002;Sengpiel and Vorobyov, 2005). Possible origins include suppressive interactions in the lateral geniculate nucleus (LGN) (Levick et al, 1972;Bonin et al, 2005), saturation in the retina or LGN (Li et al, 2006;Priebe and Ferster, 2006;Smith et al, 2006) and depression at the thalamo-cortical synapse (Freeman et al, 2002).…”

“…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.…”

A dichoptic projection system for visual psychophysics in fMRI scanners

“…The way in which the human visual system behaves when stimuli are presented independently to each eye (dichoptic presentation) is of interest to researchers investigating the mechanisms underlying visual perception (Baker et al, 2007;Harrad and Hess, 1992;Levi et al, 1979;Li et al, 2005;Macknik and Martinez-Conde, 2004;Meese et al, 2006;Sengpiel, 1997;Sengpiel and Vorobyov, 2005). Functional magnetic resonance imaging (fMRI) can be combined with dichoptic stimulation procedures to explore the neural responses of the human brain under different perceptual states (Tong et al, 2006).…”