Compartmentalized pooling generates orientation selectivity in wide-field amacrine cells

Orientation is one of the most salient features in visual scenes. Neurons at multiple levels of the visual system detect orientation, but in many cases, the underlying biophysical mechanisms remain unresolved. Here, we studied mechanisms for orientation detection at the earliest stage in the visual system, in B/K wide-field amacrine cells (B/K WACs), a group of giant, nonspiking interneurons in the mouse retina that coexpress Bhlhe22 (B) and Kappa Opioid Receptor (K). B/K WACs exhibit orientation-tuned calcium signals along their long, straight, unbranching dendrites, which contain both synaptic inputs and outputs. Simultaneous dendritic calcium imaging and somatic voltage recordings reveal that individual B/K dendrites are electrotonically isolated, exhibiting a spatially confined yet extended receptive field along the dendrite, which we term "compartmentalized pooling." Further, the receptive field of a B/K WAC dendrite exhibits center-surround antagonism. Phenomenological receptive field models demonstrate that compartmentalized pooling generates orientation selectivity, and center-surround antagonism shapes band-pass spatial frequency tuning. At the microcircuit level, B/K WACs receive excitation driven by one contrast polarity (e.g., "ON") and glycinergic inhibition driven by the opposite polarity (e.g., "OFF"). However, this "crossover" inhibition is not essential for generating orientation selectivity. A minimal biophysical model reproduced compartmentalized pooling from feedforward excitatory inputs combined with a substantial increase in the specific membrane resistance between somatic and dendritic compartments. Collectively, our results reveal the biophysical mechanism for generating orientation selectivity in dendrites of B/K WACs, enriching our understanding of the diverse strategies employed throughout the visual system to detect orientation.