Adaptation to heading direction dissociates the roles of human MST and V6 in the processing of optic flow

Abstract

The extraction of optic flow cues is fundamental for successful locomotion. During forward motion, the focus of expansion (FoE), in conjunction with knowledge of eye position, indicates the direction in which the individual is heading. Therefore, it is expected that cortical brain regions that are involved in the estimation of heading will be sensitive to this feature. To characterize cortical sensitivity to the location of the FoE or, more generally, the center of flow (CoF) during visually simulated self-motion, we carried out a functional MRI (fMRI) adaptation experiment in several human visual cortical areas that are thought to be sensitive to optic flow parameters, namely, V3A, V6, MT/V5, and MST. In each trial, two optic flow patterns were sequentially presented, with the CoF located in either the same or different positions. With an adaptation design, an area sensitive to heading direction should respond more strongly to a pair of stimuli with different CoFs than to stimuli with the same CoF. Our results show such release from adaptation in areas MT/V5 and MST, and to a lesser extent V3A, suggesting the involvement of these areas in the processing of heading direction. The effect could not be explained either by differences in local motion or by attention capture. It was not observed to a significant extent in area V6 or in control area V1. The different patterns of responses observed in MST and V6, areas that are both involved in the processing of egomotion in macaques and humans, suggest distinct roles in the processing of visual cues for self-motion.

Fig. 1.

Stimuli, experimental design, and anatomical location of regions of interest (ROIs). A: schematic representation of a single trial sequence. The experiment was designed to test for adaptation effects in several motion areas. For that purpose, in every trial a pair of stimuli were presented sequentially. The first stimulus (S1), referred to as the adapter, was shown for 3 s, followed by a 1-s presentation of a black background displaying only a fixation square. After this, the second stimulus (S2), the probe, was presented for 1 s. Trials were separated by 8-s periods of background presentation. B: stimuli. There were 4 conditions: Same (S1 = S2), Different CoF [center of flow (CoF) of S2 located in the opposite left-right location to S1], Attention Control (S2 had the same CoF but a different luminance), and No Probe (no S2). In all trials, the adapter consisted of dots expanding, contracting, and rotating from a CoF located toward the right or left of fixation, as indicated by the red arrows. The arrows and the white circle surrounding the dots were not present in the stimuli and are shown only for diagrammatic purposes. The red arrows indicate only that spiral global motion occurred and do not represent dot trajectories. C: cortical ROIs. The locations of areas V6, V3A, MST, and MT/V5 on sagittal slices of the brain of 1 participant are shown. Slice coordinates are in Talairach space.

Fig. 2.

Sensitivity to CoF in visual motion areas MT/V5 and MST. Top: time courses of the indicated ROIs in response to the 4 experimental conditions. Time courses represent averages across hemispheres (n = 14), and error bars show ±SE. Bottom: response to S2 isolated (i.e., “No Probe” time course subtracted from that of the relevant condition). Time windows indicated in gray represent the periods of stimulus presentation. Diff CoF, Different CoF; Att Control, Attention Control. Black asterisks indicate significant differences between “Same” and “Different CoF” based on the data from single time points. Gray asterisks indicate significant differences between “Different CoF” and “Attention Control” (*P < 0.05, **P < 0.01, ***P < 0.001).

Fig. 3.

Sensitivity to CoF in areas V1, V3A, and V6. All details as in Fig. 2, apart from n = 12 in V3A and V6. *P < 0.05.

Fig. 4.

Adaptation indexes. Adaptation indexes for conditions “Different CoF” and “Attention Control” are shown separately for each ROI. Bars indicate the mean ± SE index across hemispheres. Asterisks indicate significant differences between conditions “Different CoF” and “Attention Control” (*P < 0.05, **P = 0.01).