Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction?

Abstract

There is considerable controversy over the existence of orientation and direction sensitivity in lateral geniculate nucleus (LGN) neurons. Claims for the existence of these properties often were based upon data from cells tested well beyond their peak spatial frequencies. The goals of the present study were to examine the degree of orientation and direction sensitivity of LGN cells when tested at their peak spatial and temporal frequencies and to compare the tuning properties of these subcortical neurons with those of visual cortex. For this investigation, we used conventional extracellular recording to study orientation and direction sensitivities of owl monkey LGN cells by stimulating cells with drifting sinusoidal gratings at peak temporal frequencies, peak or higher spatial frequencies, and moderate contrast. A total of 110 LGN cells (32 koniocellular cells, 34 magnocellular cells, and 44 parvocellular cells) with eccentricities ranging from 2.6 deg to 27.5 deg were examined. Using the peak spatial and temporal frequencies for each cell, 41.8% of the LGN cells were found to be sensitive to orientation and 19.1% were direction sensitive. The degree of bias for orientation and direction did not vary with eccentricity or with cell class. Orientation sensitivity did, however, increase, and in some cases orientation preferences changed, at higher spatial frequencies. Increasing spatial frequency had no consistent effect on direction sensitivity. Compared to cortical cell orientation tuning, the prevalence and strength of LGN cell orientation and direction sensitivity are weak. Nevertheless, the high percentage of LGN cells sensitive to orientation even at peak spatial and temporal frequencies reinforces the view that subcortical biases could, in combination with activity-dependent cortical mechanisms and/or cortical inhibitory mechanisms, account for the much narrower orientation and direction tuning seen in visual cortex.

Orientation-selective Responses in the Mouse Lateral Geniculate Nucleus

“…Orientation-selective dLGN cells have been reported in cats and primates, including macaques, owl monkeys, and marmosets (Smith et al, 1990;White et al, 1998;Xu et al, 2002), but the selectivity appeared less prominent in those species than what we reported here in mice. We converted the reported values in cats (Daniels et al, 1977;Vidyasagar and Urbas, 1982) to the same orientation selectivity index used here for comparisons.…”

Neurons in the Most Superficial Lamina of the Mouse Superior Colliculus Are Highly Selective for Stimulus Direction

“…Consistently, a number of studies have reported direction-and orientation-selective responses in the dLGN of mice (Marshel et al, 2012;Piscopo et al, 2013;Scholl et al, 2013;, cats (Daniels et al, 1977;Vidyasagar and Urbas, 1982;Soodak et al, 1987), and monkeys (Smith et al, 1990;White et al, 1998;Xu et al, 2002;Cheong et al, 2013). In mice, DS cells appear to be more concentrated in the dorsal shell of the dLGN (Marshel et al, 2012;Piscopo et al, 2013), in which some of the DS RGCs terminate (Huberman et al, 2008(Huberman et al, , 2009.…”

Functional Asymmetries in Visual Pathways Carrying S-Cone Signals in Macaque

“…It seems likely that direction biases for achromatic gratings arise from a slight spatial and temporal offset between sources of the S-cone signals and those of the L-and M-cone signals. We made no similar measurements on P-and M-cells, but previous work in other primates (White et al, 2001;Xu et al, 2002) suggests that their direction biases are much less prominent.…”