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.

Antero-posterior versus lateral vestibular input processing in human visual cortex

“…Bremmer et al (2001), a multisensory area that integrates visual and vestibular inputs Schlack et al, 2002;Chen et al, 2011). In particular, VIP in macaque strongly responds to optic flow (Cottereau et al, 2017) and is supposed to play an important role for navigation in space (Bremmer, 2005). Altogether, these results are in line with our findings and suggest that area VIP is important for locomotion in both human and macaque.…”

“…Its responses are strongly influenced by optic flow signals but are not modulated by inertial motion (Fan et al, 2015). If areas V6 in human and macaque share similar visual properties, like their retinotopic organization (Pitzalis et al, 2006; or their selectivity to optic flow (Cardin and Smith, 2010;Fan et al, 2015, but see Cottereau et al, 2017), our results suggest that human V6 has a specific role for processing locomotion consistent vestibular inputs. It is, therefore, possible that the homology between human and macaque V6 is not as pronounced as currently believed (Pitzalis et al, 2013;2015).…”

Retinal stabilization reveals limited influence of extraretinal signals on heading tuning in the medial superior temporal area

“…If, however, biases remain as large as they are under simulated pursuit, that finding would suggest that downstream areas integrate efference-copy cues. Relatively few physiological studies have investigated pursuit compensation in frontal (Yang and Gu, 2017), premotor (Cottereau et al, 2017), or high-level parietal (Siegel and Read, 1997) cortical areas that receive projections from high-level visual-motion cortex. Additional investigations into the roles of efference copy in these areas would therefore benefit the field.…”

Stereomotion processing in the non-human primate brain

“…Prior to our statistical analyses, we used independent datasets to characterise the BOLD haemodynamic impulse response functions (HRF) separately for each animal. These datasets respectively contained 16 (M01) and 12 (M02) 204s long runs that consisted of 6 cycles of 4s full field counter phasing (10Hz) checkerboards separated by a 30s blank interval (see more details about this procedure in Cottereau et al, 2017). Data were pre-processed using the pipeline described above and projected onto individual surfaces generated with the CARET software (Van Essen et al, 2001).…”

“…Finally, it is worth noting that in monkey M02, significant BOLD activations were also found in more anterior parts of the IPS (p<10 -3 , uncorrected, see figures 2, 3 and 4), notably within the ventral and anterior intraparietal areas (VIP and AIP, respectively). VIP has been shown to be involved in egomotion-compatible optic flow processing in both monkey (Cottereau et al, 2017) and human (Wall & Smith, 2008), whereas AIP has been suggested to play a role in 3D object processing and visually guided hand movements in both species as well (Sakata et al, 1997;Durand et al, 2007;Shikata et al, 2007). Unfortunately, we were not able to find those activations in the other macaque, potentially because of a slightly smaller SNR.…”