Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area

Abstract

A possible neurobiological basis for the ''oblique effect'' is linked to the finding that more neural machinery is devoted to processing cardinal vs. oblique orientations in primary visual cortex (V1). We used optical imaging to determine whether more territory is devoted to processing horizontal and vertical orientations than oblique orientations in owl monkey middle temporal visual area (MT), a visual area highly sensitive to moving stimuli. We found that more of MT was devoted to representing cardinal than oblique orientations, and that the anisotropy was more prominent in parts of MT representing central vision (<10°). Neural responses to orientations of 0°and 90°were also greater than those to 45°and 135°. In comparison, an overrepresentation of cardinal orientations in the representation of central vision in owl monkey V1 was relatively small and inconsistent. Our data could explain the greater sensitivity to motion discrimination when stimuli are moved along cardinal meridians and suggest that the neural machinery necessary to explain the motion oblique effect either originates in MT or is enhanced at this level.oblique effect ͉ optical imaging ͉ orientation preference ͉ owl monkey ͉ visuotopic maps P rimary visual cortex (V1) of primates and a number of other mammals contains a retinotopic map of visual space with a map of stimulus orientations superimposed. Neurons selective for similar orientations are clustered together in regions devoted to a portion of visual space. One of the unexpected observations is that more cortical machinery is devoted to representing vertical and horizontal (cardinal) than oblique orientations, because more neurons are selective for cardinal orientations, and cardinal orientations produce a greater neuronal response (1-5). Although the functional consequences of greater representation of cardinal orientations are uncertain, a popular proposal is that such an anisotropy in human visual cortex underlies the ability of humans to better discriminate gratings and other visual stimuli with horizontal and vertical rather than oblique orientations (6-8). This psychophysical observation is known as the ''oblique effect,'' and the effect can be eccentricity-dependent (9, 10). Another proposal suggests that the greater representation promotes the stability of orientation tuning for neurons most sensitive to cardinal orientations, because stimulus adaptation can alter the tuning properties of cortical neurons (11). In either case, differences in the representation of stimulus features in V1 are expected to have significant perceptual consequences.Surprisingly, there have been no reports about anisotropies in the representation of orientation in primate visual areas outside V1, although few studies have ever investigated this issue beyond V1 (3,12,13). Yet there are reasons for believing that orientation anisotropies might be found in other visual cortical areas, especially the middle temporal visual area (MT; also known as V5), because MT receives direct and indirect inputs from V1, and...

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“…The oblique effect was greater in the older groups, producing a larger difference between oblique and both horizontal and vertical trajectories in the older than in the younger groups. As we pointed out in the introduction, the oblique effect is usually attributed to a larger cardinal versus oblique neural representation in the primary visual cortex, and to the fact that horizontal and vertical orientations have a greater neuronal response (Li, Peterson, & Freeman, 2003;Xu, Collins, Khaytin, Kaas, & Casagrande, 2006). Older participants, whether or not they practiced a sport, exhibited a larger oblique effect than did the young adults, suggesting that the neural areas involved in the processing of oblique orientations decline with aging.…”

“…Moreover, performance is better in horizontal than in diagonal trajectories (the so-called oblique effect; Appelle, 1972;Gros, Blake, & Hiris, 1998;Loffler & Orbach, 2001;Meng & Qian, 2005). This effect might be due to the larger cardinal (northsouth/east-west) versus oblique representation in the primary visual cortex, with the horizontal and vertical orientations producing greater neuronal responses (Li, Peterson, & Freeman, 2003;Xu, Collins, Khaytin, Kaas, & Casagrande, 2006).…”

Differential human brain activation by vertical and horizontal global visual textures

“…Previous observations (Furmanski and Engel 2000;Li et al 2003;Wang et al 2003;Xu et al 2006) have revealed that there is more 'neural machinery' devoted to processing the cardinal (horizontal and vertical) orientations than the oblique orientations; these results have been related to the greater psychophysical sensitivity to cardinal than oblique orientations ('the oblique eVect'; Appelle 1972).The higher activation to vertical than horizontal patterns might be taken to similarly reXect an imbalance in the number of neurons that prefer each orientation. However, a single unit study in cat V1 (Li et al 2003) found a greater abundance of neurons tuned to horizontal than to vertical orientations and studies in ferret V1 have shown that larger cortical areas are devoted to horizontal than to vertical orientations (Chapman and BonhoeVer 1998;Coppola et al 1998).…”

Grid Cells and Spatial Maps in Entorhinal Cortex and Hippocampus

“…Stimuli oriented along the cardinal axes yield better psychophysical performance compared to obliquely oriented stimuli. In the visual cortices, both single-neuron responses and population responses reflect this psychophysical anisotropy by increased representational density along the cardinal axes (Furmanski and Engel 2000;Wang et al 2003;Xu et al 2006). Several studies suggest that the oblique effect originates in higher order cortices (Nasr and Tootell 2012;Liang et al 2007;Shen et al 2008), as the effect is stronger here compared to early sensory cortex (Shen et al 2008;Müller et al 2000), and the effect in early cortex is selectively abolished by temporal inactivation of higher order cortex (Shen et al 2008).…”

“…1). Further, using optical imaging in area MT (which shows movement and orientation selectivity for stimuli) in the visual system, Xu et al (2006) showed frequency plots of activation over the range of possible stimulus orientations. In these plots, there are quite distinct peaks with bimodal offsets from the cardinal axes (Fig.…”