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Michael Manookin, Christian Puller, Fred Rieke, Jay Neitz, Maureen Neitz; ON parasol ganglion cells of the primate retina exhibit directional sensitivity. Invest. Ophthalmol. Vis. Sci. 2013;54(15):1296. doi: https://doi.org/.
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© ARVO (1962-2015); The Authors (2016-present)
Neurons with direction sensitivity in the primate visual system are thought to arise first in primary visual cortex. However, the mechanisms that give rise to the direction selectivity of neurons in the cortex remain unclear and current theories prove inadequate in explaining the origins of the high degree of directional tuning found in V1 and V2 neurons. These models assume that directional information is not contained in the inputs from retina and LGN. However, starburst amacrine cells, which underlie direction selectivity in rabbit and rodent retina, are also found in the primate retina. Furthermore, in the primate retina, starburst amacrine cells co-fasciculate with ON parasol ganglion cells (Jacoby et al., 1996, J Neurosci), opening the possibility that these cells encode directional information in the primate retina. Here, we investigated direction sensitivity in parasol ganglion cells.
We recorded the spiking responses and whole-cell currents from parasol cells in an in vitro preparation of the macaque monkey retina. The stimulus was a white moving bar on a black background. The bar was moved across a cell’s receptive-field (RF) center testing all directions using 30-45° intervals.
ON parasol cell spike and whole-cell response patterns varied depending on the direction of the moving bar and they all showed distinct preferred and non-preferred directions. Motion in the non-preferred direction elicited a burst of spikes only when the bar reached the stationary RF center, while motion in the preferred direction elicited an early burst of spikes when the bar was ~0.3 mm from the edge of the stationary RF center and another burst at the RF center. The early (but not late) burst of spikes showed a significant directional tuning (DSI, 0.58 +/- 0.12, n=34). Whole-cell voltage-clamp recordings revealed that the early, directionally sensitive spike discharge arose from an increase in synaptic excitation. Pharmacology experiments revealed that this early directionally tuned response was reversibly suppressed by a GABAA receptor antagonist, chloride transporter blockers, or nAChR antagonists.
These results indicate that the spike output of ON parasol cells contains information about the direction of a moving object. This directional selectivity of the retinal output will need to be incorporated into models for how the directional responses of cortical cells are generated.
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