Neural encoding of temporal and spatial plausibility in naturalistic motion: an awake monkey fMRI study

Time flows in one direction, a physical constraint humans recognize, as reflected in proverbs such as “there is no crying over spilt milk.” Recent work from our laboratory has demonstrated that human participants rely on specific cues to discriminate the direction of time's arrow, with functional magnetic resonance imaging (fMRI) identifying neural networks selective for temporal directionality. These neural bases are likely shared across species, as the physical constraint of time is universal, even if other species may not “recognize” it as a law. In this study, we investigated whether and how the non-human primate brain encodes the naturalistic dynamics (plausibility) of biological and non-biological motion in temporal and spatial domains by presenting monkeys with video clips of biological and non-biological motion under three conditions: (1) normal (forward and upright), (2) temporally reversed, and (3) spatially inverted. Whole-brain analyses revealed that the superior temporal sulcus (STS) preferentially responded to forward, upright biological motion, reflecting sensitivity to naturalistic dynamics (plausibility) in both temporal and spatial domains. Within the STS, a consistent posterior-to-anterior gradient was observed in both monkeys: temporal plausibility was encoded posteriorly, spatial plausibility anteriorly, and both in the intermediate region. These results suggest that the primate STS is selectively tuned to the naturalistic dynamics of biological motion, with its posterior subregion contributing to the evaluation of temporal plausibility, which may underlie time-direction judgments in specific perceptual contexts.