A common neural substrate for processing scenes and egomotion-compatible visual motion

Abstract

Neuroimaging studies have revealed two separate classes of category-selective regions specialized in optic flow (egomotioncompatible) processing and in scene/place perception. Despite the importance of both optic flow and scene/place recognition to estimate changes in position and orientation within the environment during self-motion, the possible functional link between egomotion-and scene-selective regions has not yet been established. Here we reanalyzed functional magnetic resonance images from a large sample of participants performing two well-known "localizer" fMRI experiments, consisting in passive viewing of navigationally relevant stimuli such as buildings and places (scene/place stimulus) and coherently moving fields of dots simulating the visual stimulation during self-motion (flow fields). After interrogating the egomotionselective areas with respect to the scene/place stimulus and the scene-selective areas with respect to flow fields, we found that the egomotion-selective areas V6+ and pIPS/V3A responded bilaterally more to scenes/places compared to faces, and all the scene-selective areas (parahippocampal place area or PPA, retrosplenial complex or RSC, and occipital place area or OPA) responded more to egomotion-compatible optic flow compared to random motion. The conjunction analysis between scene/place and flow field stimuli revealed that the most important focus of common activation was found in the dorsolateral parieto-occipital cortex, spanning the scene-selective OPA and the egomotion-selective pIPS/V3A. Individual inspection of the relative locations of these two regions revealed a partial overlap and a similar response profile to an independent low-level visual motion stimulus, suggesting that OPA and pIPS/V3A may be part of a unique motion-selective complex specialized in encoding both egomotion-and scene-relevant information, likely for the control of navigation in a structured environment.

Optic flow selectivity in the macaque parieto-occipital sulcus

“…Indeed, MT neurons respond equally well to a bar as to random dot patterns in translation (Tanaka et al, 1986), and MT neurons respond as well to optic flow fields as to translating random dots (Lagae et al 1994;Nelissen et al 2006). The functional profile observed here in mSTs also mirrors that observed in the human counterpart, where MT+ (identified by Radial Rings) was found to respond, although at different extent, also to Flow Fields besides to Radial Rings (Sulpizio et al, 2020).…”

“…Here we found a robust and consistent fMRI activations in V6+ for the contrast between Flow Fields and random motion (Figures 3-4). This region did not show any significant activation to Radial Rings stimulus, like the human counterpart (Pitzalis et al, 2010;Sulpizio et al, 2020). In addition, the average sensitivity ratio of POs (Figure 8A) indicates that V6+ was one of the motion areas with the greatest preference for the Flow Field with respect to the radial rings.…”

“…We first tested the responsiveness of macaque brain to low contrast radial motion (Radial Rings, Figure 1A), the stimulus used initially in humans to functionally map the motion middle temporal area MT/V5 (Tootell et al 1995a,b) and later on routinely used also in our lab as MT+ localizer (e.g., Pitzalis et al, 2010Pitzalis et al, , 2012Pitzalis et al, , 2013aSulpizio et al, 2020).…”

“…We then tested the responsiveness of the macaque brain to another type of motion stimulus, Flow Fields, which contrasts coherent optical flow stimulation with scrambled control (see Figure 1B). This stimulus was originally used in humans to functionally map the medial motion area V6 (Pitzalis et al 2010) and later on routinely used in our lab as V6 localizer (e.g., Pitzalis et al, 2012Pitzalis et al, , 2013aSerra et al, 2019;Sulpizio et al, 2020).…”

“…The motion sensitivity observed here in the anterior bank of the Lunate sulcus, likely corresponding to macaque V3A, deserves a comment. Since its discovery in humans (Tootell et al, 1997), a growing number of fMRI studies have reported that human V3A is significantly activated by coherent motion and by complex motion patterns as the Flow Field stimulus (e.g., Sunaert et al, 1999;Sereno et al, 2001;Pitzalis et al, 2010Pitzalis et al, , 2013cFischer et al, 2012b;Serra et al, 2019;Sulpizio et al, 2020). In contrast, the motion sensitivity of macaque V3A is still a debated question.…”