Processing of Egomotion-Consistent Optic Flow in the Rhesus Macaque Cortex

Abstract

The cortical network that processes visual cues to self-motion was characterized with functional magnetic resonance imaging in 3 awake behaving macaques. The experimental protocol was similar to previous human studies in which the responses to a single large optic flow patch were contrasted with responses to an array of 9 similar flow patches. This distinguishes cortical regions where neurons respond to flow in their receptive fields regardless of surrounding motion from those that are sensitive to whether the overall image arises from self-motion. In all 3 animals, significant selectivity for egomotion-consistent flow was found in several areas previously associated with optic flow processing, and notably dorsal middle superior temporal area, ventral intra-parietal area, and VPS. It was also seen in areas 7a (Opt), STPm, FEFsem, FEFsac and in a region of the cingulate sulcus that may be homologous with human area CSv. Selectivity for egomotion-compatible flow was never total but was particularly strong in VPS and putative macaque CSv. Direct comparison of results with the equivalent human studies reveals several commonalities but also some differences.

Keywords: egomotion; heading; monkey fMRI; optic flow; vision.

Figure 1.

(A) Schematic representation of the monkey fMRI set-up. The animal sits in a sphinx position within the primate chair, in the bore of the scanner, head restrained by the head-post, with the 8 channel, phase array coil located on top of the head. The animal is involved in a passive fixation task, i.e., maintaining the gaze on a green fixation target back-projected on a stimulation screen by a video-projector. Eye position is monitored by an infrared video-based eye-tracker. Correct fixation triggers the delivery of fluid rewards during the runs. (B) Illustration of the stimuli and experimental design. The EC stimulus consisted of a square field of dots moving in a coherent optic flow pattern containing expansion/contraction and rotation components that varied over time, consistent with self-motion on a varying spiral trajectory. The EI stimulus consisted of a 3 × 3 array of 9 identical panels, each containing a smaller version of the EC stimulus. Recordings were performed using a block-design, with the alternation of EC and EI flow stimuli, separated by blank periods. Each run contained 7 repetitions of such blocks (112 TR in total). EC conditions were shown first in half of the runs and EI conditions appeared first in the other half of the runs.

Figure 2.

(A) Statistical parametric maps for the EC versus EI contrast in monkeys M01, M02, and M03. Results are projected on dorsal, lateral, and medial views of the left and right hemispheres of the individual cortices. The color code reflects the contrast t-values and indicates statistically significant differences between BOLD responses evoked by the EC and EI conditions (P < 10⁻³ uncorrected). Hot (orange to yellow) and cold (dark to pale blue) colors indicate stronger responses to EC and EI, respectively. (B) Map of overlap between significant activations in the EC versus EI contrast across the 3 monkeys. Only activation sites found in at least 2 individuals are shown. Results are projected on the flattened representations of the left and right hemispheres of the F99 template. Orange and yellow indicate cortical sites significantly more activated by EC than by EI in 2/3 and 3/3 of the subjects, respectively. Dark and pale blue show regions more activated by EI than by EC in 2/3 and 3/3 of the subjects, respectively. Seven cortical were significantly activated in our 3 macaques: MSTd, 7a, STPm, VIP, VPS, FEFsem, and FEFsac. Black stars indicate a region of the cingulate sulcus (pmCSv) that was found in the 3 animals in the left hemisphere and in one animal on the right hemisphere. White stars indicate a region of the parieto-occipital sulcus were significant activations were found in 2 animals. Borders of the primary visual area (V1) are shown as white dotted lines (as, arcuate sulcus; cs, cingulate sulcus; ips, intraparietal sulcus; ls, lateral sulcus; sts, superior temporal sulcus).

Figure 3.

Activity profiles in areas MSTd, VPS, VIP, pmCSv, and FEFsem. (A) Statistical results of the EC > EI contrast shown on axial sections for monkeys M01, M02, and M03 (neurological convention). Areas are indicated by arrows on the 3 monkeys. (B) PSC in these 5 areas for the EC and EI conditions with respect to baseline (blank condition) in both hemispheres of the 3 macaques. The first half of the data was used to define ROIs around the local maxima of these areas and the second half was used to compute PSC (see details in the text). The error bars provide the standard errors across runs (n = 18). Stars indicate areas whose PSCs during the EC condition were significantly stronger than during the EI condition (t-tests, P < 0.05). P-values of the t-tests are provided for areas that did not pass significance.

Figure 4.

Activity profiles in areas 7a, FEFsac, and STPm. (A) Statistical results of the EC > EI contrast shown on axial sections for the 3 monkeys. Areas 7a (in all monkeys) and LIPd (in M02 and M03) are indicated by arrows. (B) PSC in area 7a for the EC and EI conditions with respect to baseline. (C) Statistical results of the EC > EI contrast shown on axial sections for the 3 monkeys. Areas STPm and FEFsac are indicated by arrows. (D) PSC in areas FEFsac and STPm for the EC and EI conditions with respect to baseline. Other details as in Fig. 3.

Figure 5.

(A) Average sensitivity ratio (%) between the responses to the EC and EI conditions. The ratio (defined in the text) may be thought of as the reduction in response that occurs when an EC stimulus is replaced with EI. As for the PSC, ratios were computed on the second half of the data (see details in the text). Only areas with significant responses in the 3 animals are shown. Areas were sorted according to their mean sensitivity ratio. Markers provide the individual data corresponding to M01 (circles), M02 (diamonds), and M03 (squares). (B) Schematic localization of the 8 areas on the F99 template.