The Functional Asymmetry of ON and OFF Channels in the Lateral Geniculate Nucleus (LGN) during a Perceptual Decision Task

Abstract

Early behavioral studies indicated that separate psychophysical channels underlie the perception of light (i.e. contrast increments) and dark (i.e. contrast decrements) (Anstis 1967; De Valois 1977; Krauskopf 1980; Cavanaugh and Anstis 1986; Chichilnisky and Wandell 1996; Westheimer 2007), and that human observers are faster and more accurate in perceiving contrast decrements rather than increments (Blackwell 1946; Short 1966; Bowen et al. 1989, 1992; Chan and Tyler 1992; Kontsevich and Tyler 1999; but see Komban et al. 2011). In the early visual system, the segregation of ON and OFF channels starts at bipolar cells (Nomura et al. 1994; Masu et al. 1995; Vardi and Morigawa 1997; Wassle 2004) and is preserved throughout the lateral geniculate nucleus (LGN) (Casagrande and Norton 1991; Westheimer 2007; Schiller 2010). These ON and OFF pathways were initially thought of as independent, parallel systems that mirror each other in their light/dark responses (Schiller 1992, 2010; Kremers et al. 1993; Benardete and Kaplan 1997, 1999). Several physiological studies, however, have revealed significant functional asymmetries between the two systems. On the one hand, it was reported that the ON pathway could signal both contrast increments (i.e. via increase in spikes) and decrements (via decrease in spikes) at low contrast, whereas the OFF pathway could only signal contrast decrements (Chichilnisky and Kalmar 2002). On the other hand, it was reported that over a great range of luminance levels, the contrast responses of OFF neurons were stronger and more linear than those of ON neurons (Kremkow et al. 2014), and, under scotopic conditions, OFF neurons responded to much higher temporal frequencies than ON neurons (ArmstrongGold and Rieke 2003; Pandarinath et al. 2010). Additionally, projections from the OFF pathway were reported to dominate the cortical representation of central vision (Jin et al. 2008, 2011), and visual responses to dark stimuli were reported to dominate the superficial layers of V1 (Yeh et al. 2009; Xing et al. 2010). How do the ON and OFF pathways contribute to the perception of light and dark? How can the physiological asymmetry of the ON/OFF pathways be linked to the psychophysical asymmetry of light and dark perception? To answer these questions, we recorded from LGN Parvocellular (P) ON-Center and OFF-Center neurons in awake monkeys while they passively viewed (i.e. simple fixation) and actively detected (i.e. two-alternative, forced-choice detection) contrast increment and decrement changes. Neurometric Sensitivity