Heading Tuning in Macaque Area V6

Abstract

Cortical areas, such as the dorsal subdivision of the medial superior temporal area (MSTd) and the ventral intraparietal area (VIP), have been shown to integrate visual and vestibular self-motion signals. Area V6 is interconnected with areas MSTd and VIP, allowing for the possibility that V6 also integrates visual and vestibular self-motion cues. An alternative hypothesis in the literature is that V6 does not use these sensory signals to compute heading but instead discounts self-motion signals to represent object motion. However, the responses of V6 neurons to visual and vestibular self-motion cues have never been studied, thus leaving the functional roles of V6 unclear. We used a virtual reality system to examine the 3D heading tuning of macaque V6 neurons in response to optic flow and inertial motion stimuli. We found that the majority of V6 neurons are selective for heading defined by optic flow. However, unlike areas MSTd and VIP, V6 neurons are almost universally unresponsive to inertial motion in the absence of optic flow. We also explored the spatial reference frames of heading signals in V6 by measuring heading tuning for different eye positions, and we found that the visual heading tuning of most V6 cells was eye-centered. Similar to areas MSTd and VIP, the population of V6 neurons was best able to discriminate small variations in heading around forward and backward headings. Our findings support the idea that V6 is involved primarily in processing visual motion signals and does not appear to play a role in visual-vestibular integration for self-motion perception.

Two Visual Pathways in Primates Based on Sampling of Space: Exploitation and Exploration of Visual Information

“…Radial optic flow patterns are generated as a result of these self-motion trajectories and their importance is indicated by the overall greater responsiveness of the set of cortical areas in the IPS to radial, as compared to planar or circular, flow fields (Silver and Kastner, 2009). Several areas in the dorsal stream of the macaque, i.e., V6 (Fan et al, 2015), VIP (Chen et al, 2013), and MSTd (Lee et al, 2011) have been found to process information related to self-motion and heading. Radial optic flow patterns have a curious property—as Figure 4 shows, there is zero motion at the center of gaze in a radial optic flow field (termed the focus of expansion, or FOE), while strong motion input is present away from the center of gaze, namely in the visual periphery.…”

Flexible egocentric and allocentric representations of heading signals in parietal cortex

“…ventral intraparietal area | reference frame | vestibular | body/world-centered | egocentric/allocentric S patial navigation is a complex problem requiring information from both visual and vestibular systems. Heading, the instantaneous direction of translation of the observer, represents one of the key variables needed for effective navigation and is represented in a number of cortical and subcortical regions (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12). Although visual heading information is generally represented in an eye-centered reference frame by neurons in various brain areas (13)(14)(15)(16)(17)(18), the vestibular representation of heading appears to be more diverse (8,15,19).…”

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

“…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).…”

“…A tracer study showed that anatomically, it is mostly connected to other visual regions, including areas MST and VIP (Galletti, et al, 2001). 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.…”