Functional Organization of Owl Monkey Lateral Geniculate Nucleus and Visual Cortex

Abstract

O'Keefe, Lawrence P., Jonathan B. Levitt, Daniel C. Kiper, Robert M. Shapley, and J. Anthony Movshon. Functional organization of owl monkey lateral geniculate nucleus and visual cortex. J. Neurophysiol. 80: 594–609, 1998. The nocturnal, New World owl monkey ( Aotus trivirgatus) has a rod-dominated retina containing only a single cone type, supporting only the most rudimentary color vision. However, it does have well-developed magnocellular (M) and parvocellular (P) retinostriate pathways and striate cortical architecture [as defined by the pattern of staining for the activity-dependent marker cytochrome oxidase (CO)] similar to that seen in diurnal primates. We recorded from single neurons in anesthetized, paralyzed owl monkeys using drifting, luminance-modulated sinusoidal gratings, comparing receptive field properties of M and P neurons in the lateral geniculate nucleus and in V1 neurons assigned to CO “blob,” “edge,” and “interblob” regions and across layers. Tested with achromatic stimuli, the receptive field properties of M and P neurons resembled those reported for other primates. The contrast sensitivity of P cells in the owl monkey was similar to that of P cells in the macaque, but the contrast sensitivities of M cells in the owl monkey were markedly lower than those in the macaque. We found no differences in eye dominance, orientation, or spatial frequency tuning, temporal frequency tuning, or contrast response for V1 neurons assigned to different CO compartments; we did find fewer direction-selective cells in blobs than in other compartments. We noticed laminar differences in some receptive field properties. Cells in the supragranular layers preferred higher spatial and lower temporal frequencies and had lower contrast sensitivity than did cells in the granular and infragranular layers. Our data suggest that the receptive field properties across functional compartments in V1 are quite homogeneous, inconsistent with the notion that CO blobs anatomically segregate signals from different functional “streams.”

Oriented Axon Projections in Primary Visual Cortex of the Monkey

“…Field sizes were in excellent agreement with previous reports in anesthetized (Hubel and Wiesel, 1968;Schiller et al, 1976a) and alert (Poggio, 1972;Dow et al, 1981;Snodderly and Gur, 1995) macaques. We did not find any published reports for receptive field sizes in New World monkeys, although O'Keefe et al (1998) report a median optimal spatial frequency of 0.79 cycles/°for their sample of complex cells in the owl monkey.…”

“…To avoid this problem, we chose squirrel monkeys and owl monkeys for our experiments. The cortex of these New World monkeys exhibits weak anatomical segregation by eye (Kaas et al, 1976;Hendrickson et al, 1978;Horton and Hocking, 1996;O'Keefe et al, 1998). The lack of eye dominance in the upper layers is especially dramatic in squirrel monkeys, in which monocular tracer injections label all cytochrome oxidase blobs rather than just those in the ocular dominance columns of the injected eye, as in macaques (Horton and Hocking, 1996).…”

Tuning for Spatiotemporal Frequency and Speed in Directionally Selective Neurons of Macaque Striate Cortex

“…For example, we can think of the transformations between the photoreceptors and LGN neurons primarily as a series of spatial filters, in which the conversion to center-surround spatial organization attenuates responses to low spatial frequencies (EnrothCugell and Robson, 1966;Enroth-Cugell et al, 1983;Shapley and Lennie, 1985). Additional high-pass filtering of the outputs of the LGN attenuates responses at low spatial frequencies still further to create separable bandpass tuning in V1 simple cells at the same time as direction-selectivity emerges (Derrington and Lennie, 1984;Hawken et al, 1996;O'Keefe et al, 1998). Separable spatiotemporal tuning is also evident in V1 complex cells at low contrast, but, at high contrast, the tuning surface tilts to approximate speed tuning.…”

Orientation Selectivity without Orientation Maps in Visual Cortex of a Highly Visual Mammal

“…Two-thirds (133 of 195) of the cells had HWHH below 90°, which is a slightly lower fraction of tuned cells than reported in carnivores (e.g., 85%) (Maldonado et al, 1997) and monkeys. The median half-width of these tuned cells was 28°, similar to carnivores (LeVay et al, 1987) and primates (O'Keefe et al, 1998;Ringach et al, 2002). Finally, we examined orientation-tuning width as a function of stimulus contrast.…”