Blobs versus bars: Psychophysical evidence supports two types of orientation response in human color vision

Abstract

The classic hypothesis of Livingstone and Hubel (1984, 1987) proposed two types of color pathways in primate visual cortex based on recordings from single cells: a segregated, modular pathway that signals color but provides little information about shape or form and a second pathway that signals color differences and so defines forms without the need to specify their colors. A major problem has been to reconcile this neurophysiological hypothesis with the behavioral data. A wealth of psychophysical studies has demonstrated that color vision has orientation-tuned responses and little impairment on form related tasks, but these have not revealed any direct evidence for nonoriented mechanisms. Here we use a psychophysical method of subthreshold summation across orthogonal orientations for isoluminant red-green gratings in monocular and dichoptic viewing conditions to differentiate between nonoriented and orientation-tuned responses to color contrast. We reveal nonoriented color responses at low spatial frequencies (0.25-0.375 c/deg) under monocular conditions changing to orientation-tuned responses at higher spatial frequencies (1.5 c/deg) and under binocular conditions. We suggest that two distinct pathways coexist in color vision at the behavioral level, revealed at different spatial scales: one is isotropic, monocular, and best equipped for the representation of surface color, and the other is orientation-tuned, binocular, and selective for shape and form. This advances our understanding of the organization of the neural pathways involved in human color vision and provides a strong link between neurophysiological and behavioral data.

Interactions between luminance and color signals: Effects on shape

“…We note that an additional level of complexity has been suggested; there is a possibility of multiplexing of color (red-green) and luminance information in the parvocellular pathway (e.g., see Billock, 1995;Billock & Tsou, 2004). In turn the cortical simple cells will exploit this multiplexing, and it has been suggested that there might be two distinct pathways processing chromatic (red-green) information, one non-oriented and monocular and the other one orientation selective and binocular (Gheiratmand, Meese, & Mullen, 2013). The multiplexing hypothesis is however still controversial (for example, see Lee, Sun, and Valberg, 2011).…”

Cross-orientation masking in human color vision: Application of a two-stage model to assess dichoptic and monocular sources of suppression

“…Hence, the greater strength of contrast normalization in color vision might be explained by differences in this normalizing gain pool for color versus achromatic contrast. Psychophysical evidence suggests that the underlying orientation tuning of color detectors is somewhat broader than in achromatic vision (Beaudot & Mullen, 2005;Gheiratmand, Meese, & Mullen, 2013). Grating stimuli will cause greater activation of a gain pool if the individual modulatory neurons are broadly rather than narrowly tuned for orientation.…”

“…Crossorientation suppression (XOS) is observed in most neurons in mammalian cortex (Morrone, Burr, & Maffei, 1982;Bonds, 1989;DeAngelis, Robson, Ohzawa, & Freeman, 1992;Heeger, 1992;Carandini, Heeger, & Movshon, 1997;Walker, Ohzawa, & Freeman, 1998;Li, Peterson, Thompson, Duong, & Freeman, 2005;Sengpiel & Vorobyov, 2005). While the origin of XOS is thought to be primarily cortical, there is also evidence in the cat indicating the involvement of subcortical, monocular sites (Walker et al, 1998;Truchard, Ohzawa, & Freeman, 2000;Carandini, Heeger, & Senn, 2002;Freeman, Durand, Kiper, & Carandini, 2002;Li et al, 2005;Sengpiel & Vorobyov, 2005;Priebe & Citation: Kim, Y. J., Gheiratmand, M., & Mullen, K. T. (2013). Cross-orientation masking in human color vision: Application of a two-stage model to assess dichoptic and monocular sources of suppression.…”

The Whole is Other Than the Sum: Perceived Contrast Summation Within Color and Luminance Plaids

“…In sum, relative to component gratings, color plaids have lower perceived contrast summation than achromatic plaids and this chromatic summation difference is greater at the medium-spatial frequency and smaller at the low-spatial frequency. These results may be reflective of two separate processes: greater cross-orientation suppression in color vision (Kim et al, 2013; Medina & Mullen, 2009) and increased cross-orientation summation for low compared with medium-spatial frequency color stimuli (Gheiratmand et al, 2013, 2016; Gheiratmand & Mullen, 2014). …”