Two retinotopic visual areas in human lateral occipital cortex

Abstract

We describe two visual field maps, lateral occipital areas 1 (LO1) and 2 (LO2), in the human lateral occipital cortex between the dorsal part of visual area V3 and visual area V5/MT+. Each map contained a topographic representation of the contralateral visual hemifield. The eccentricity representations were shared with V1/V2/V3. The polar angle representation in LO1 extended from the lower vertical meridian (at the boundary with dorsal V3) through the horizontal to the upper vertical meridian (at the boundary with LO2). The polar angle representation in LO2 was the mirror-reversal of that in LO1. LO1 and LO2 overlapped with the posterior part of the object-selective lateral occipital complex and the kinetic occipital region (KO). The retinotopy and functional properties of LO1 and LO2 suggest that they correspond to two new human visual areas, which lack exact homologues in macaque visual cortex. The topography, stimulus selectivity, and anatomical location of LO1 and LO2 indicate that they integrate shape information from multiple visual submodalities in retinotopic coordinates.

Figure 1.

Right hemisphere retinotopic maps. Cortical representation of visual polar angle and eccentricity displayed on computationally unfolded and flattened patches (“flat maps”) of the occipital cortex of the right hemispheres for two individual subjects (S8 and S4) and averaged across 15 hemispheres (for details of intersubject averaging, see Materials and Methods). Solid white lines, left horizontal meridian (LHM) and right horizontal meridian (RHM); dotted white lines, upper vertical meridian (UVM); dashed white lines, lower vertical meridian (LVM); white circles, approximate locations of foveal representations of V1/V2/V3. Individual subject data only shown for voxels with response coherence >0.25 (see Materials and Methods). In the left column, color indicates polar angle (inset legend). In the right column, color indicates eccentricity between 0 and 6° (inset legend). Flat maps of polar angle in the remaining 13 right hemispheres are available as online supplemental information (supplemental Figs. 1, 2, available at www.jneurosci.org as supplemental material).

Figure 2.

Left hemisphere retinotopic maps of subjects S5 and S9, and averaged across 15 hemispheres. Conventions, abbreviations, and legend are as in Figure 1. Flat maps of polar angle in the remaining 13 right hemispheres are available as online supplemental information (supplemental Figs. 3, 4, available at www.jneurosci.org as supplemental material).

Figure 3.

Schematic summary of visual field topography. A, Human visual cortex. Topography and location of LO1 and LO2 relative to other retinotopic visual areas (shown in flattened format for the right hemisphere) averaged across all 30 hemispheres (for details of intersubject averaging, see Materials and Methods). B, The organization of the corresponding region of macaque visual cortex is shown for comparison (not to scale). Adapted from Gattass et al. (1988), Brewer et al. (2002), and Fize et al. (2003). UVF, Upper visual field; LVF, lower visual field.

Figure 4.

Anatomical locations of LO1 and LO2. A, Locations of LO1 and LO2 and neighboring visual areas displayed on a partially inflated brain of a representative subject. los, lateral occipital sulcus; log, lateral occipital gyrus; tos, transverse occipital sulcus; ios, inferior occipital sulcus; its, inferior temporal sulcus; sts, superior temporal sulcus; ips, intraparietal sulcus. B, Variability in the locations of LO1 and LO2 across subjects relative to local anatomical landmarks. For subject S1, LO1 and LO2 are located mostly on the crest of the lateral occipital gyrus/gyri; for subject S6, LO1 and LO2 are located mostly on the fundus of the lateral and transverse occipital sulcus/sulci.

Figure 5.

Cortical magnification functions for V1, V2, V3, LO1, LO2, and hV4. Plot symbols, eccentricity, and cortical distance measurements from nine subjects (different plot symbols indicate different subjects) are shown. Solid curves and equations show parametric fits to the data pooled across subjects, where E is eccentricity in degrees, D is cortical distance in millimeters, and a and b are constants. Cortical distances have been aligned to an origin corresponding to the 3° isoeccentricity representation (see Materials and Methods). Because of the reduced stimulus duty cycle close to the edge of the stimulus aperture (beyond 5° from the center of gaze), there was a systematic underestimation of eccentricity at more peripheral locations (evidenced by an apparent change in the slope of eccentricity versus distance beyond ∼5° or 10 mm from the origin). Data from these peripheral locations were not included in the fits (solid lines).

Figure 6.

LO1 and LO2 have large voxel response fields. A, Voxel response field size along radial (eccentricity) dimension (σ_R, SD of Gaussian fits to expanding/contracting ring data) as a function of eccentricity in areas V1, V2, LO1, and LO2. Response field sizes were estimated for individual voxels in 28 hemispheres with response fields centered between 0.5 and 3.5° eccentricity, and with response coherence >0.25 (see Materials and Methods). Lines are least squares fits. B, Slopes of best-fit lines for each visual area. The light bars show the radial component of response field size σ_R, based on least squares fits such as those shown in A. The dark bars show the polar angle component of response field size σ_P. Error bars indicate SEM across subjects and hemispheres. Response field sizes increase more rapidly with eccentricity (steeper slopes) in higher-tier visual areas.

Figure 7.

Visual field coverage in LO1 and LO2 compared with visual areas V3d, V3v, hV4, and V1. Each contour indicates the visual field coverage between 0.5 and 3.5° eccentricity for an individual subject, estimated from the summed response fields of voxels with coherence >0.25. Red and green indicate left and right hemisphere, respectively. Areas V3d and V3v, in each hemisphere, represent the lower and upper contralateral quadrants of the visual field, respectively. In contrast, the entire contralateral hemifield, including both upper and lower quadrants, is represented in each of LO1, LO2, and V1.

Figure 8.

Visual field coverage of retinotopic maps in V1, V2, V3, hV4, LO1, and LO2. A, Visual field eccentricity (color scale at right) averaged across 30 hemispheres (15 subjects, collapsed across left and right hemispheres) plotted in canonical atlas coordinate system (see Materials and Methods). Abscissa represents a cortical distance axis parallel to isoeccentricity contours and the ordinate represents the orthogonal distance axis, parallel to isoangle contours. Note that units of the axes in this coordinate system [distance from the anterior, or lower vertical meridian (LVM), boundary of hV4 for the abscissa and distance from 1° isoeccentricity contour for the ordinate] are arbitrary and do not reflect true physical distances, but merely provide a canonical coordinate system for aligning data across subjects. Data for LO1 and LO2 restricted to atlas eccentricities 1–4.5° (see Materials and Methods). B, Visual polar angle (color scale at right) averaged across 30 hemispheres (15 subjects). Positive phase angles (red) correspond to upper hemifield, negative phase angles (blue) to lower hemifield. UVM, upper vertical meridian; HM, horizontal meridian; vertical black lines, visual area boundaries at phase reversals in polar angle. C, Profile of visual polar angle, collapsed across eccentricity, as a function of atlas distance from anterior (lower vertical meridian) boundary of hV4. Red solid curve, average profile across all 30 hemispheres; dark green dots, right hemisphere data for individual subjects; dark red dots, left hemisphere data for individual subjects; blue solid curve, predicted polar angle profile assuming full hemifield representations in LO1 and LO2; orange solid curve, predicted polar angle profile assuming only upper quadrant representations in LO1 and LO2. Note that predictions of the quadrant and hemifield models only differ in LO1 and LO2.

Figure 9.

fMRI responses to motion, motion boundaries, and objects. A–C, Responses from typical individual subject (S4, right hemisphere). Superimposed visual area regions of interest are color-coded as follows: blue outlines, early visual areas (V1–V3); red outlines, ventral visual areas (hV4, VO1); green outlines, dorsal visual areas (V3A/B, V7, V5); white, LO1; black, LO2. A, fMRI responses to moving random dot patterns alternating with static random dot patterns. Color scale, correlation between fMRI response and a sinusoid with the same (24 s) period as the stimulus alternations, for voxels showing strong (|correlation| > 0.25) response modulation. Positive correlation indicates stronger fMRI responses to moving dots (test stimulus) than to static dots (control stimulus); negative correlation indicates the opposite response pattern. B, fMRI responses to random dot patterns containing motion boundaries alternating with transparently moving random dot patterns. The correlation threshold and color scale are as in A. Positive correlation indicates stronger fMRI responses to motion boundary stimuli (test) than to transparent motion (control). C, fMRI responses to images of objects and faces alternating with scrambled versions of the same images. Threshold and color scale are as in A. Positive correlation indicates stronger fMRI responses to object and face images (test) than to scrambled images (control). D, Amplitudes of mean fMRI responses to localizer stimuli in each visual area, averaged across seven subjects. Positive amplitudes correspond to stronger fMRI responses to test stimuli (A–C, red and yellow); negative amplitudes correspond to stronger responses to control stimuli (A–C, blue). Error bars indicate SEM across subjects.