fMR-Adaptation Reveals Invariant Coding of Biological Motion on the Human STS

Abstract

Neuroimaging studies of biological motion perception have found a network of coordinated brain areas, the hub of which appears to be the human posterior superior temporal sulcus (STSp). Understanding the functional role of the STSp requires characterizing the response tuning of neuronal populations underlying the BOLD response. Thus far our understanding of these response properties comes from single-unit studies of the monkey anterior STS, which has individual neurons tuned to body actions, with a small population invariant to changes in viewpoint, position and size of the action being viewed. To measure for homologous functional properties on the human STS, we used fMR-adaptation to investigate action, position and size invariance. Observers viewed pairs of point-light animations depicting human actions that were either identical, differed in the action depicted, locally scrambled, or differed in the viewing perspective, the position or the size. While extrastriate hMT+ had neural signals indicative of viewpoint specificity, the human STS adapted for all of these changes, as compared to viewing two different actions. Similar findings were observed in more posterior brain areas also implicated in action recognition. Our findings are evidence for viewpoint invariance in the human STS and related brain areas, with the implication that actions are abstracted into object-centered representations during visual analysis.

Keywords: biological motion; fMRI; superior temporal sulcus; vision; visual recognition.

Figure 1

(A) Schematic of stimuli. Subjects viewed 750 ms point-light animations, separated by a short interstimulus interval (250 ms in Experiments 1 and 2, 50 ms in Experiments 3 and 4). (B) Adaptation indices were computed from the three timepoints at the peak of the hemodynamic response, as the average increase in BOLD response relative to the Repeated condition.

Figure 2

Statistical maps and ROIs identified with the biological motion localizer. (A) Biological motion selective regions as computed from a group average of all subjects (Experiments 1–4) on Talairach standardized data, shown on an individual subject's anatomy. This analysis is shown only to demonstrate those regions that are consistently selective for biological motion, across our group of subjects. To account for individual differences in anatomical features (i.e., sulcal and gyral patterns), the primary experimental analyses for these experiments were computed in native (unwarped) brain space. (B) The biological motion selective areas in two individual subjects, shown in native brain space. These two representative subjects demonstrate the range of variability we observed across the subject population for this localizer. All statistical maps (biological motion – scrambled motion) are corrected with a false discovery rate of q < 0.01. STSp, posterior superior temporal sulcus; ITS, inferior temporal sulcus; IOG, inferior occipital gyrus; Fus, posterior fusiform; PMC, premotor cortex; PT, posterior planum temporale.

Figure 3

Average deconvolved hemodynamic response functions and the corresponding adaptation indices for each hemisphere of the STSp (left) and hMT+ (right) for Experiment 1. *Indicates statistically significant different peak response relative to the Repeated baseline, as computed from the deconvolved BOLD responses using planned statistical contrasts (see Section “Materials and Methods”). More detailed statistical analyses are shown in (Table 2).

Figure 4

The predicted and measured BOLD responses for the cross-adaptation between biological and scrambled motion (Experiment 2). Top Panel: The predicted BOLD response from a brain area with only “low-level” neurons that are velocity tuned (left), and a mixture of low- and high-level neurons (right). This model predicts the same BOLD response for the single biological and single scrambled trials (orange and green), and an identical BOLD response for the biological + scrambled as the scrambled + biological trials (blue and purple, respectively). The adaptation effect was estimated from Experiment 1 (Repeated trials reduced the neural response by ≈84% in the STSp, as compared to Different trials), and the relative proportion of low- and high-level neurons estimated from the trials with single presentations of biological and scrambled motion in the STSp (≈74% as many low-level neurons as compared to high-level neurons). Bottom panel: Deconvolved hemodynamic response functions measured across our subjects from the hMT+ (left) and the STSp (right).

Figure 5

Average deconvolved hemodynamic response functions and the corresponding adaptation indices for each hemisphere of the STSp and hMT+ for (A) position changes and (B) size changes. *Indicates statistically significant peak response from the Repeated (foveal or medium) condition, as computed from the deconvolved hemodynamic response functions.

Figure 6

Average deconvolved hemodynamic response functions and the corresponding adaptation indices for each of the remaining ROIs. (A) Experiment 1, action specificity and invariance across mirror reversals, (B) position invariance, and (C) size invariance. *Indicates statistically different peak BOLD response from the Repeated condition, as computed in the ROI-based planned statistical contrasts. Abbreviations are the same as in Figure 2.

Figure 7

Group GLM results for statistical contrasts testing for fMR-adaptation in the deconvolved BOLD response, overlaid on a single subject anatomy. (A) Group contrast testing for adaptation for the repeated action trials (Different actions – Repeated actions). (B) Group contrast testing for adaptation in trials depicting the same action from two viewpoints (Different – Mirror Reversed). All contrasts are thresholded at a false discovery rate of q < 0.01.