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Michael B Manookin, Todd R Appleby; Approach motion sensitivity in primate retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 2019;60(9):5271.
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© ARVO (1962-2015); The Authors (2016-present)
Avoidance of rapidly approaching objects is a primitive defense mechanism found across vertebrate and invertebrate taxa. Humans and non-human primates exhibit this reflex beginning in infancy (Schiff et al., 1962; Ball and Tronick, 1971) and it persists in primates lacking a functional primary visual cortex indicating that approach sensitivity does not arise through the classical geniculostriate pathway (King and Cowey, 1992; Hervais-Adelman et al., 2015). Moreover, this reflex can be evoked by pharmacological disinhibition of superior colliculus (DesJardin et al., 2013). These observations indicate that approach sensitivity arises in the colliculus or in presynaptic structures such as the retina.A previous study in the mouse retina identified approach motion sensitivity in the Off transient Alpha ganglion cell (Münch et al., 2009), but whether ganglion cells in the primate retina also exhibits approach sensitivity is not known. Several primate retinal ganglion cell types have been identified that project to the superior colliculus including broad thorny and On and Off parasol cells (Rodieck and Watanabe, 1993; Crook et al., 2008). All three of these cell types show sensitivity to visual motion, but sensitivity to approaching motion has not been tested (Puller et al., 2015; Manookin et al., 2018).
Here, we used a battery of visual stimuli to test for approach motion sensitivity in broad thorny and On and Off parasol ganglion cells of the macaque monkey retina. These stimuli included approaching and receding spots and annuli and a tailored noise stimulus. Extracellular recordings were performed to measure spike output and whole-cell voltage-clamp recordings were performed to measure excitatory and inhibitory synaptic inputs.
We observed approach sensitivity in all three types, but it was strongest in parasol ganglion cells. A tailored noise stimulus revealed that speed tuning to approach motion was bandpass, peaking at speeds between 5-10 degrees/s. Recordings of synaptic currents revealed that approach motion engaged excitatory and inhibitory synaptic inputs out-of-phase with each other in a push-pull manner.
Together, these data indicate that the elementary computations for approach motion sensitivity are present in the bipolar and amacrine cell circuits of the inner retina and in the spike outputs of ganglion cells that project to the superior colliculus of primates.
This abstract was presented at the 2019 ARVO Annual Meeting, held in Vancouver, Canada, April 28 - May 2, 2019.
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