Spiking and nonspiking models of starburst amacrine cells in the rabbit retina

Abstract

The integrative properties of starburst amacrine cells in the rabbit retina were studied with compartmental models and computer-simulation techniques. The anatomical basis for these simulations was provided by computer reconstructions of intracellularly stained starburst amacrine cells and published data on dendritic diameter and biophysical properties. Passive and active membrane properties were included to simulate spiking and nonspiking behavior. Simulated synaptic inputs into one or more compartments consisted of a bipolar-like conductance change with peak and steady-state components provided by the sum of two Gaussian responses. Simulated impulse generation was achieved by using a model of impulse generation that included five nonlinear channels (/ Na , l Ca , 1A, 'K. /K.CO)-The magnitude of the sodium channel conductance change was altered to meet several different types of impulse generation and propagation behaviors. We studied a range of model constraints which included variations in membrane resistance (R m ) from 4,000 ft-cm 2 to 100,000 fl-cm 2 , and dendritic diameter from 0.1 to 0.3 /xm. In a separate series of simulations, we studied the feasibility of voltage-clamping starburst amacrine cells using a soma-applied, single-electrode voltage clamp, based on models with and without dendritic and somatic spiking behavior. Our simulation studies suggest that single dendrites of starburst amacrine cells can behave as independent functional subunits when the R m is high, provided that one or a small number of dendrites is synaptically co-activated. However, as the number of co-activated dendrites increases, the starburst cell behavior becomes more uniform and independent dendritic function is less prevalent. The presence of impulse activity in the dendrites raises new questions about dendritic function. However, dendritic impulses do not necessarily eliminate independent dendritic function, because dendritic impulses commonly fail as they propagate toward the soma, where they contribute EPSP-like responses which summate with conventional synaptic currents.

A Unique Role for Kv3 Voltage-Gated Potassium Channels in Starburst Amacrine Cell Signaling in Mouse Retina

“…However, subsequent modeling studies indicated that the electrical isolation of dendrites in starburst cells depends on assumptions of either relatively low specific membrane resistance or minimal synaptic coactivation of individual dendrites (Poznanski, 1992;Velte and Miller, 1997). Our observation (illustrated in Figure 1) that it was difficult to depolarize starburst cell somata beyond Ϫ20 mV suggests that Kv3 currents generate a voltage-dependent shunt located proximally, which prevents effective depolarization of the starburst cell soma.…”

“…These data suggest that the direction-selective properties of starburst cells arise from intrinsic mechanisms likely to include both passive and active membrane properties (Poznanski, 1992;Velte and Miller, 1997;Euler et al, 2002). However, the specific ion channels present in starburst cells are essentially unknown.…”

Cellular Inhibitory Behavior Underlying the Formation of Retinal Direction Selectivity in the Starburst Network

“…If SACs show regenerative membrane properties then it would be difficult to justify the existence of electrotonically isolated dendritic compartments within SACs (cf. [116]). The earlier models of SACs incorporating active membrane properties were based on inadequate assumptions (see for example, [107,116]).…”

“…The earlier models of SACs incorporating active membrane properties were based on inadequate assumptions (see for example, [107,116]). For instance, Velte and Miller [116] developed a compartmental model of a single SAC with active ionic currents found in ganglion cells from intact amphibian retina. Such modeling should be treated with skepticism, as there is a serious hazard in generalizing across species.…”

Computation of motion direction in the vertebrate retina

“…4) [31]. In combination with the morphology and the differential distribution of ion channels along the SAC dendrite, this leads to electrical isolation of the sectors from each other [57,82]. As a result, the individual dendritic sectors can be considered as largely independent processing units [10,28,57,77].…”