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Ben Murphy-Baum, William Rowland Taylor; Synaptic circuits that drive a polyaxonal amacrine cell in the rabbit retina. Invest. Ophthalmol. Vis. Sci. 2015;56(7 ):2615.
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© ARVO (1962-2015); The Authors (2016-present)
Inhibitory circuits are critical for many physiological processes in the retina, such as the generation of center-surround receptive fields and object motion sensitivity. Many of these inhibitory roles require spatial integration over broad areas, and are thought to be mediated by wide-field amacrine cells (WFACs). Thus, our understanding of retinal circuit function is contingent upon studying the functional properties of WFACs. Here, we examined the different excitatory and inhibitory inputs to a single type of polyaxonal WFAC and determined how they form the spatiotemporal properties of light-evoked synaptic activity.
Retinas from pigmented rabbits were used in a whole-mount preparation. Synaptic currents were recorded in voltage clamp in response to a variety of light stimuli. Receptor antagonists were bath applied to elucidate how different neurotransmitter receptors affect the excitatory and inhibitory conductances.
Inhibitory inputs comprised ON and OFF glycinergic and OFF GABAA mediated inhibition. GABAA mediated inputs were active during wide-field stimulation (λ=735µm), while glycinergic inputs were only active during narrow-field stimulation (λ=295µm). Excitatory inputs were modulated by local feedback inhibition that was active on spatial scales close to that of single bipolar cells, and involved serial inhibition between GABAA expressing amacrine cells and GABAA/C expressing ON bipolar cells. Blocking GABAA receptors produced an attenuated and more transient (Thalf=10.9±1.0ms) excitation, while blocking GABAC receptors produced larger and more sustained excitatory responses (Thalf=55.6±10.4ms). Surround inhibition was mediated by feedback from spiking amacrine cells, as it was suppressed by TTX. However, action potentials were not involved in local feedback inhibition, as TTX had no effect during local stimulation.
This study demonstrates the prevalence of serial inhibitory circuits in both the ON and OFF visual pathways. Our data suggests that ON excitation combines with OFF inhibition to produce more linear spatial summation in the receptive field center, while feedback inhibition acts in local microcircuits to shape the kinetics and spatial extent of the light response. It is likely that local temporal tuning and wide-field spatial tuning are implemented using the same feedback circuitry, but are functionally separated by a spike threshold.
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