Functional polarity of dendrites and axons of primate A1 amacrine cells

Abstract

The A1 cell is an axon-bearing amacrine cell of the primate retina with a diffusely stratified, moderately branched dendritic tree (~400 µm diameter). Axons arise from proximal dendrites forming a second concentric, larger arborization (>4 mm diameter) of thin processes with boutonlike swellings along their length. A1 cells are ON-OFF transient cells that fire a brief high frequency burst of action potentials in response to light (Stafford & Dacey, 1997). It has been hypothesized that A1 cells receive local input to their dendrites, with action potentials propagating output via the axons across the retina, serving a global inhibitory function. To explore this hypothesis we recorded intracellularly from A1 cells in an in vitro macaque monkey retina preparation. A1 cells have an antagonistic center-surround receptive field structure for the ON and OFF components of the light response. Blocking the ON pathway with L-AP4 eliminated ON center responses but not OFF center responses or ON or OFF surround responses. Blocking GABAergic inhibition with picrotoxin increased response amplitudes without affecting receptive field structure. TTX abolished action potentials, with little effect on the sub-threshold light response or basic receptive field structure. We also used multi-photon laser scanning microscopy to record light-induced calcium transients in morphologically identified dendrites and axons of A1 cells. TTX completely abolished such calcium transients in the axons but not in the dendrites. Together these results support the current model of A1 function, whereby the dendritic tree receives synaptic input that determines the center-surround receptive field; and action potentials arise in the axons, which propagate away from the dendritic field across the retina.

A Polyaxonal Amacrine Cell Population in the Primate Retina

“…In response to steps of light, these PACs exhibited ON-OFF light response characteristics similar to those previously described for PACs in the retinas of primates (Stafford and Dacey, 1997;Davenport et al, 2007). Stimulation with spots of light centered on the receptive field elicited brisk bursts of action potentials at light onset and offset (Fig.…”

“…The receptive field center of each ON-OFF PAC was approximately spatially coincident with its soma and dendritic field, identified from the electrical image (Völgyi et al, 2001;Davenport et al, 2007). Specifically, the center of the receptive field coincided with a region of large amplitude somatic and dendritic spikes near the center of the electrical image, while the discrete radially propagating axons extended much farther (Fig.…”

“…The ON-OFF PACs exhibited center-surround receptive field organization (Völgyi et al, 2001;Davenport et al, 2007). This was revealed by the reduced response strength to large stimuli (Fig.…”

“…A number of PACs, of several distinct morphological types, have been described in various species (Dacey, 1988(Dacey, , 1989Vaney et al, 1988;Famiglietti, 1992;Freed et al, 1996;Taylor, 1996;Stafford and Dacey, 1997;Völgyi et al, 2001;Wright and Vaney, 2004;Davenport et al, 2007), always characterized by small dendritic fields and long axonal processes spanning several millimeters of retina. As with RGCs, correspondences between specific cell types across species are somewhat unclear.…”

“…These cells are characterized by axonal processes that extend radially several millimeters from the tips of their dendrites (Dacey, 1988(Dacey, , 1989Vaney et al, 1988;Mariani, 1990;Famiglietti, 1992;Freed et al, 1996;Taylor, 1996;Völgyi et al, 2001;Olveczky et al, 2003;Wright and Vaney, 2004;Davenport et al, 2007). The axons of PACs are located in the inner plexiform layer, providing opportunities to contact processes of other retinal interneurons as well as ganglion cells, which send visual information to the brain.…”