A channel for 3D environmental shape in anterior inferotemporal cortex

Abstract

Inferotemporal cortex (IT) has long been studied as a single pathway dedicated to object vision, but connectivity analysis reveals anatomically distinct channels, through ventral superior temporal sulcus (STSv) and dorsal/ventral inferotemporal gyrus (TEd, TEv). Here, we report a major functional distinction between channels. We studied individual IT neurons in monkeys viewing stereoscopic 3D images projected on a large screen. We used adaptive stimuli to explore neural tuning for 3D abstract shapes ranging in scale and topology from small, closed, bounded objects to large, open, unbounded environments (landscape-like surfaces and cave-like interiors). In STSv, most neurons were more responsive to objects, as expected. In TEd, surprisingly, most neurons were more responsive to 3D environmental shape. Previous studies have localized environmental information to posterior cortical modules. Our results show it is also channeled through anterior IT, where extensive cross-connections between STSv and TEd could integrate object and environmental shape information.

Figure 1

Stimuli and example results. (A) Example stimulus shape presented at six scales. Inset values specify the maximum visual angle subtended by the stimulus. The fixation point (red dot) remains at the same point on the stimulus surface. As scale increases, the stimulus extends beyond the screen borders, and the visible portion becomes landscape-like. (B) Example morphing transformations. From left to right: surface distortion removal, x-axis rotation, translation/rotation of latitudinal ring, change in surface distortion height function, y-axis rotation. (C) High-response stimuli for example TEd neurons. The coronal MRI image shows the approximate extent of TEd (cyan tint) and recording location of example neurons (colored dots). For each neuron, high-response stimuli from independent lineages (left and right columns) are indicated by arrows of the corresponding color. The border color around each stimulus indicates response rate (averaged across the 750 ms presentation period and 5 repetitions) based on the scale bars at right, which index the minimum-to-maximum response range of each neuron in sp/s. As in our previous studies of IT shape coding (Yamane et al., 2008; Hung et al. 2012), we observed that high-response stimuli differed in global shape but shared partial structure, consistent with fragment-based ensemble coding of shape. In these previous studies, we used multidimensional parameterization of surface and medial axis shape to construct linear/nonlinear models of 3D shape fragment tuning validated by correspondence across lineages. Similar analyses can be applied to these data, but will require extensive presentation in a separate report. Precise characterization of shape tuning is not critical for our purpose here, which is to analyze overall selectivity for stimulus scale. The essential cross-validation here is between scale-tuning functions in separate lineages. (D) Scale-tuning functions for example TEd neurons. Average response (+/− SEM) across all stimuli as a function of stimulus scale is plotted for each example (indexed by color) in each lineage (left vs. right). The correlations between scale-tuning functions across lineages are given by the r values in (C). These correlations were each highly significant (p < 0.001). Baseline activity +/− SEM for each example neuron (colored points next to vertical axis) was averaged across randomly scheduled null stimulus presentation periods during the fixation task. (E) High-response stimuli for example STSv neurons. Details as in (C). (F) Scale-tuning functions for example STSv neurons. Details as in (D). See also Fig. S1.

Figure 2

Population results. (A) The scale-tuning function of each neuron (n = 141) is plotted as a vertical strip. Color represents scale, as in Fig. 1D,F, ranging from small objects (red) to large environments (green). Brightness at each point along the vertical strip is proportional to the average normalized response strength across all stimuli at the corresponding scale in the upper half of the neuron’s response range. Neurons are arranged along the horizontal axis based on their positions in the coronal plane along the STSv and TEd channels (see MRI images and arrows). (B) For each neuron, we plot the result of a Wilcoxon rank-sum test based on the 10 highest response environmental stimuli (subtending > 80°) as compared to the 10 highest response objects (subtending < 22°). The rank-sum value can vary from 55 (if the environmental stimuli occupy all the lower ranks, 1–10) to 155 (if the environmental stimuli occupy all the higher ranks, 11–20). Dashed lines indicate significance thresholds (p < 0.05, two-tailed). Significant neurons are plotted in red (object) or green (environment). Neurons are ordered along the horizontal axis as in (A). (C) Distributions of Pearson correlations between scale-tuning functions in the two independent lineages for each neuron. Filled bars represent significant correlations (p < 0.01). (D) Average normalized response levels in STSv (red) and TEd (green) as a function of stimulus diameter. The shaded regions represented the 95% confidence interval of average response values. See also Fig. S2.

Figure 3

Control tests on TEd neurons with significant selectivity for environmental stimuli. Example results are presented for a single TEd neuron (cyan dot in population plots). (A) Sensitivity to 3D shape-in-depth vs. 2D shape. One high-response and one low-response environmental stimulus were selected from the adaptation experiment. Modulation strength is the response difference divided by the maximum. 3D modulation strength (x-axis) is based on the original stimuli with all depth cues. 2D modulation strength (y-axis) was based on stimuli with no disparity cues, no shading, and either fronto-parallel hexagonal texture, random line texture, or no texture (silhouettes), whichever produced the highest modulation value. Stimuli for the example neuron are shown next to the corresponding axes, with borders indicating response rate (see scale bar). Removing cues for shape-in-depth largely abolished differential responses. The average 3D modulation strength of 0.86 was significantly greater than the average 2D modulation strength of −0.041 (paired t-test, p < 0.0001). (B) Responses do not depend on texture density. Responses to the original texture density (medium) are plotted against the vertical scale. Responses remained consistent when texture density decreased (low) or increased (high). (C) Scale-tuning test. The high-response environmental stimulus for the example neuron was presented at 6 scales, ranging from object to environmental. (The original stimulus from the adaptive experiment was the largest scale, at right.) Preference for environmental-scale stimuli was maintained even for this optimal shape. Similar consistency of scale tuning for optimal shapes was observed for other neurons in TEd (Fig. S3C) and STSv (Fig. S3D). (D) Consistency of response across lighting directions. Responses to the original lighting direction (from the direction of the viewer, at infinite distance) are plotted against the vertical scale. Responses remained consistent for spotlights positioned to the right, left, bottom, or top, which produced substantially different image contrast patterns. See also Fig. S3.