A synaptic signature for ON- and OFF-center parasol ganglion cells of the primate retina

Abstract

In the primate retina, parasol ganglion cells contribute to the primary visual pathway via the magnocellular division of the lateral geniculate nucleus, display ON and OFF concentric receptive field structure, nonlinear spatial summation, and high achromatic temporal–contrast sensitivity. Parasol cells may be homologous to the alpha-Y cells of nonprimate mammals where evidence suggests that N-methyl-D-aspartate (NMDA) receptor-mediated synaptic excitation as well as glycinergic disinhibition play critical roles in contrast sensitivity, acting asymmetrically in OFF- but not ON-pathways. Here, light-evoked synaptic currents were recorded in the macaque monkey retina in vitro to examine the circuitry underlying parasol cell receptive field properties. Synaptic excitation in both ON and OFF types was mediated by NMDA as well as α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate glutamate receptors. The NMDA-mediated current–voltage relationship suggested high Mg2+ affinity such that at physiological potentials, NMDA receptors contributed ~20% of the total excitatory conductance evoked by moderate stimulus contrasts and temporal frequencies. Postsynaptic inhibition in both ON and OFF cells was dominated by a large glycinergic “crossover” conductance, with a relatively small contribution from GABAergic feedforward inhibition. However, crossover inhibition was largely rectified, greatly diminished at low stimulus contrasts, and did not contribute, via disinhibition, to contrast sensitivity. In addition, attenuation of GABAergic and glycinergic synaptic inhibition left center–surround and Y-type receptive field structure and high temporal sensitivity fundamentally intact and clearly derived from modulation of excitatory bipolar cell output. Thus, the characteristic spatial and temporal–contrast sensitivity of the primate parasol cell arises presynaptically and is governed primarily by modulation of the large AMPA/kainate receptor-mediated excitatory conductance. Moreover, the negative feedback responsible for the receptive field surround must derive from a nonGABAergic mechanism.

Synaptic Rectification Controls Nonlinear Spatial Integration of Natural Visual Inputs

“…These data show that spatial integration in parasol RGC spike outputs qualitatively resembles that in the cells’ excitatory synaptic inputs (see also Crook, 2014). While there is an asymmetry in the strength of nonlinear integration in the excitatory inputs to On and Off parasol RGCs, the excitatory inputs to both cell types deviate substantially from linear spatial integration.…”

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

“…2c,d) of On and Off parasol RGCs showed classical center-surround RF organization. This confirms previous observations in parasol RGCs [44,43] and other primate RGC types [45]. We then used these properties to identify a disc and annulus, matched to the specific cell, which permitted selective activation of the center or surround (Fig.…”

NMDA and AMPA receptors contribute similarly to temporal processing in mammalian retinal ganglion cells

“…The data from our study and the primate study (Crook et al . ) extend previous results by showing that synaptic NMDAR‐mediated conductances can be modulated by high temporal frequencies within the physiological range (∼10–20 Hz). The NMDAR‐mediated conductances in mammalian ganglion cells apparently are far faster than those measured in salamander ganglion cells (Mittman et al .…”

“…Our relatively fast NMDAR-mediated responses are consistent with recordings from three types of rabbit ganglion cells: postsynaptic responses to low temporal frequency stimuli exhibited NMDAR components that turned on and off rapidly and resembled the AMPAR components in time course (Venkataramani et al 2010;Buldyrev et al 2012). Furthermore, our results are consistent with recent findings from primate ganglion cells in which NMDAR-mediated conductances were recorded in response to stimulation at high temporal frequencies (Crook et al 2014). In addition, the short, ß4-9 ms delay between the peak of the AMPAR and NMDAR components of the 9-18 Hz responses that we observed (Fig.…”