Electrotonic signal processing in AII amacrine cells: compartmental models and passive membrane properties for a gap junction-coupled retinal neuron

Abstract

Amacrine cells are critical for processing of visual signals, but little is known about their electrotonic structure and passive membrane properties. AII amacrine cells are multifunctional interneurons in the mammalian retina and essential for both rod- and cone-mediated vision. Their dendrites are the site of both input and output chemical synapses and gap junctions that form electrically coupled networks. This electrical coupling is a challenge for developing realistic computer models of single neurons. Here, we combined multiphoton microscopy and electrophysiological recording from dye-filled AII amacrine cells in rat retinal slices to develop morphologically accurate compartmental models. Passive cable properties were estimated by directly fitting the current responses of the models evoked by voltage pulses to the physiologically recorded responses, obtained after blocking electrical coupling. The average best-fit parameters (obtained at − 60 mV and ~ 25 °C) were 0.91 µF cm−2 for specific membrane capacitance, 198 Ω cm for cytoplasmic resistivity, and 30 kΩ cm2 for specific membrane resistance. We examined the passive signal transmission between the cell body and the dendrites by the electrotonic transform and quantified the frequency-dependent voltage attenuation in response to sinusoidal current stimuli. There was significant frequency-dependent attenuation, most pronounced for signals generated at the arboreal dendrites and propagating towards the soma and lobular dendrites. In addition, we explored the consequences of the electrotonic structure for interpreting currents in somatic, whole-cell voltage-clamp recordings. The results indicate that AII amacrines cannot be characterized as electrotonically compact and suggest that their morphology and passive properties can contribute significantly to signal integration and processing.