Sixty years of visual cortex single-cell studies to explain the perceptual deficits of Davida.

An elongated shape, such as an arrow, provides two cues from which its in-plane orientation can be derived: the inclination (first spatial derivative of position) of the overall shape and the position of its endpoints. In the extensive investigation of the perceptual capacities of Davida (Vannuscorps et al., 2022, this journal), those two cues are used interchangeably (experiments 1.1, 1.7, 3.2 and 3.3). Yet at the neuronal level, endpoints require a more complex receptive field (RF) endowed with end-stopping (Heitger et al., 1992; Hubel & Wiesel, 1965; Orban et al., 1979; Schiller et al., 1976; Yazdanbakhsh & Livingstone, 2006), while the inclination of the shape can be analysed by a simple oriented RF (Hubel & Wiesel, 1959). Given the widespread use of gratings to investigate the early visual regions of the non-human primate (nhp) visual system, relatively little is known about processing of endpoints up to area V4 (Pasupathy & Connor, 1999; Ponce et al., 2017). The authors claim that tilt discrimination is spared in Davida (experiments 2.5 and 3.5), but the methods do not state that the position of the lines was randomised to disable the position-of-endpoint cue, allowing the subject to use this alternative cue. It also opens the door to more complex explanations of the deficit, such as conflicts between cues because the position-of-endpoint cue provides erroneous information. In addition, the test involved a comparison between lines, which is more complex than identifying the orientation of a single line (Orban et al., 1984). For example, the temporal comparison in successive orientation discrimination requires the rostral infero-temporal (IT) cortex, where the orientation of the first stimulus is stored in a short-lived buffer (Orban & Vogels, 1998). The use of a single line would have simplified the interpretation, and enabled comparison with nhp lesion studies (De Weerd et al., 1999; Vogels et al., 1997) showing that orientation identification requires only the initial parts of the ventral stream up to V4. The report states (experiment 6.10) that the processing of orientation of kinetic edges has been investigated extensively in human and non-human primates and seems intact. In humans, the so-called kinetic occipital (KO) region (Van Oostende et al., 1997) is in fact part of the lateral occipital (LO) complex (Larsson & Heeger, 2006), which corresponds to dorsal V4 of the monkey (Kolster et al., 2010). Single-cell studies have shown that the extraction of kinetic edges is achieved in IT cortex (Sary et al., 1993), and even in V4 (Mysore et al., 2006), but not in MT (Marcar et al., 1995), nor V1, and only weakly in V2 (Marcar et al., 2000). Even if there is some grouping of neurons according to the cue used in V4, its retinotopic organisation (Gattass et al., 1988) imposes that this segregation is limited to a distance well below the size of a hypothetical focal disruption (e.g. grating patches in V4 are about 1 mm in size, Vanduffel et al., 2002). The kinetic edge data thus suggests that the disruption in processing occurs neither in area V4 nor downstream from it, but rather concerns the white matter (WM) including the connections between areas V2/3 and V4. Not all visual afferents to V4 should be disrupted, as the kinetic edge data suggests that the magnocellular input to V4 is intact. The observation (experiment 2.8) that the processing of tactile orientation is spared, coupled with the single-cell study of Maunsell et al. (1991), reporting a convergence of visual and tactile signals of orientation in 25% of the V4