Elsevier

NeuroImage

Volume 24, Issue 2, 15 January 2005, Pages 306-314
NeuroImage

Predominantly extra-retinotopic cortical response to pattern symmetry

https://doi.org/10.1016/j.neuroimage.2004.09.018Get rights and content

Abstract

Symmetry along one or more axes is a key property of objects and biological organisms. We report on a bilateral visual region of occipital cortex that responds strongly to the presence of multiple symmetries in the viewed image. The stimuli consisted of random dots organized in fourfold and onefold mirror-symmetric patterns, against random control stimuli. The contrast between symmetric and random patterns produced negligible or inconsistent activation of the primary visual projection area V1 or of other medial occipital projection areas. However, there was strong symmetry-specific activation in extra-retinotopic lateral occipital cortex. The high level of activation in this region of cortex may represent part of a general class of computations that require integration of information across a large span of the visual field.

Introduction

Visual perception involves a series of synaptic transformations through which visually responsive neurons in the brain process image information projected onto the retina. The spatial integration across the visual scene by cortical neurons can be more than a thousand times greater than for the individual photoreceptors. What analysis do the large receptive fields of these cortical neurons perform?

Several fundamental types of visual computation employ information that is distributed across large portions of the visual field. These computations may be useful for a variety of visual functions, including perceptual rescaling (color constancy), estimating object properties (connectivity, perceptual grouping), and the processing of specific cues that are important for pattern recognition and object classification. Symmetry is an example of an object property that requires long-range integration of scene features. In many cases, symmetry information is not present in the local features and can be found only by comparing information distributed across long distances in the visual field. (Tyler and Hardage, 1996). The reason for the perceptual salience of symmetry is unclear, but it has been argued that symmetry is a useful cue for discriminating living organisms (friend or foe) from inanimate objects. Symmetry has been shown to be a significant determinant of mate selection (Johnstone, 1994, Moller, 1992).

In relation to the evolutionary theme, there is a well-established relationship between symmetry and perceived attractiveness (or beauty) of potential mates in humans, both in their faces (Grammer and Thornhill, 1994, Jacobsen and Hofel, 2002, Mealey et al., 1999, Rhodes et al., 2001, Rhodes et al., 2002) and in their bodies (Booth et al., 2002, Tovee et al, 2000). Possible confounds of symmetry correlating with masculinity or with familiarity have been ruled out (Little and Jones, 2003, Penton-Voak et al., 2001). Some studies find the opposite effect of a preference for natural asymmetries (Swaddle and Cuthill, 1995) but there is a consensus that the dimension of preference for asymmetry is aligned with emotional expressiveness of the face rather than structural variables, for which symmetry is preferred (Kowner, 1996, Zaidel et al, 1995). Curiously, although symmetry preference in infants is demonstrable for abstract patterns (Fisher et al., 1981, Humphrey and Humphrey, 1989, Humphrey et al., 1986, Pornstein and Krinsky, 1985), any preference for symmetry in faces has been difficult to establish (Rhodes et al., 2002, Samuels et al., 1994).

Taken as a whole, such studies show a strong association between the perception of symmetry and its biological relevance in mate selection for humans, although it is evident that there are competing factors such as emotional expressiveness that also come into play. The importance of symmetry as a visual cue to humans is evident from the widespread occurrence of symmetric patterns and designs in the constructed environment of architecture and art throughout human history (Tyler, 1996). It is a striking fact of our constructed environment that symmetry is built extensively into furniture, buildings, ornaments, and vehicles. Some of this fabricated symmetry is a reflection of the bilateral symmetry of its users, but much of it has a purely esthetic role. Common examples are oriental rugs and inlaid cabinetry. It is unclear from an evolutionary perspective whether there is an adaptive value for humans to enhance the symmetry around them, but it is clearly a ubiquitous urge whose neural basis is of considerable interest.

There is some neuropsychological evidence of a cortical specialization for large-scale visual computations. Patients suffering from certain visual agnosias, for example simultanagnosia, identify local elements of the visual field but have difficulty discerning the relations among elements in the image. The patients act as though they can see only one object at a time. Brain injury in these patients is often associated with localized lesions in the occipito-parietal portions of the brain (Farah, 1990). More specifically, certain patients with posterior cerebral artery infarcts of the lateral occipital cortex show a specific deficit in detecting bilateral symmetry in random-dot patterns presented to the contralesional visual field, while pattern and motion discrimination in the deficient regions of the field are relatively normal (L. Vaina, personal communication). There is one (and remarkably, only one) study that has reported single-cell responses specific to the presence of symmetric configurations of visual stimuli (Lee et al., 1998). Using shapes specified by the second-order borders between different orientation-defined textures, they found local activations at the point where the shapes lay symmetrically over the receptive fields of neurons in monkey area V1, that is, where the symmetry axis of the figure coincided with the receptive field position defined by the texture-edge response. Although they recorded in V1, these authors concluded from an analysis of the delayed dynamics of the symmetry response that it did not originate in V1 but by feedback from a higher cortical area. Thus, although this lone study identified symmetry as a relevant variable for neural processing in visual cortex, it did not identify the locus at which the property of symmetry is extracted and identified in terms of a neural signal distinct from that for the local pattern elements in the stimulus. The technique of functional Magnetic Resonance Imaging (fMRI) offers the opportunity to track down the cortical region(s) where symmetry-specific processing occurs.

We used fMRI to measure activity in the cortical visual pathways while observers viewed patterns containing large-scale symmetry. The object of the study was to determine whether the property of symmetry would elicit specialized responses or activate known retinotopic regions of human cortex. Four hypotheses were evaluated:

  • (i)

    that symmetry-specific activation would occur in area V1, where Lee et al. (1998) found symmetry-axis responses in monkey,

  • (ii)

    that symmetry-specific activation would occur in adjacent retinotopic areas, well-positioned to be the source of the feedback signal of Lee et al. (1998),

  • (iii)

    that symmetry-specific activation would occur in higher retinotopic areas known to process pattern structure (such as V3A or V4), and

  • (iv)

    that symmetry-specific activation would occur in further region of occipital cortex whose specialization remains to be determined.

The results showed an increase in fMRI signal in a bilateral region of occipital cortex when the observers viewed fields of random versus symmetric patches in comparison control stimuli of purely random dots. The activity caused by the pattern symmetries was mainly present outside the early visual projection areas V1–V4 (which can be identified by retinotopic mapping with traveling-wave stimuli; DeYoe et al., 1996, Engel et al., 1994, Engel et al., 1997, Sereno et al., 1995).

Section snippets

Experiment 1

The stimuli for the primary experiments consisted of 16° fields of white dots, each 15′ in diameter, at 25% density on a dark background. The primary symmetry probe consisted of fields of random dots organized with symmetry structure alternated in a block design with null sequences of non-symmetric random patterns. Examples are shown in Fig. 1, with a four-axis reflection symmetry pattern in Fig. 1a, and a non-symmetric random pattern in Fig. 1b. Note that very little of the symmetry can be

Experiment 1

The local hemodynamic response to the symmetry/random alternation was extracted throughout the human occipital lobe and compared with the locations of the retinotopic visual areas obtained by standard fMRI techniques (as described in Materials and methods). In Fig. 2a, a single axial brain slice from passing through the pons, cerebellum, occipital, and temporal lobes is shown for each of three observers scanned at 1.5 T. The slice was chosen to pass through regions of symmetry activation and

Discussion

The data are consistent with the idea that regions in the DLO are particularly involved in the processing of long-range stimulus structure. Because there is little symmetry-related activity in the early retinotopic organized visual areas, the responses cannot be explained by the long-range connections present in area V1 (see Callaway, 1998, for a review), area V2 (Merigan et al., 1993, von der Heydt and Peterhans, 1989), or other retinotopic areas (Reppas et al., 1997) (with the individual

Acknowledgments

Supported by NEI R01 13025 and the Radiology Department, Stanford University.

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