Phase advancing is a common property of multiple neuron classes in the mouse retina

Abstract

Behavioral interactions with moving objects are challenged by response latencies within the sensory and motor nervous systems. In vision, the combined latency from phototransduction and synaptic transmission from the retina to central visual areas amounts to 50-100 ms, depending on stimulus conditions. Time required for generating appropriate motor output adds to this latency and further compounds the behavioral delay. Neuronal adaptations that help counter sensory latency within the retina have been demonstrated in some species, but how general these specializations are, and where in the circuitry they originate, remains unclear. To address this, we studied the timing of object motion-evoked responses at multiple signaling stages within the mouse retina using two-photon fluorescence calcium and glutamate imaging, targeted whole-cell electrophysiology, and computational modeling. We found that both ON and OFF-type ganglion cells, as well as the bipolar cells that innervate them, temporally advance the position encoding of a moving object and so help counter the inherent signaling delay in the retina. Model simulations show that this predictive capability is a direct consequence of the spatial extent of the cells’ linear visual receptive field, with no apparent specialized circuits that help predict beyond it.

Significance Statement

Signal transduction and synaptic transmission within sensory signaling pathways costs time. Not a lot of time, just tens to a few hundred milliseconds depending on the sensory system, but enough to challenge fast behavioral interactions under dynamic stimulus conditions, like catching a moving fly. To counter neuronal delays, nervous systems of many species use anticipatory mechanisms. One such mechanism in the mammalian visual system helps predict the future position of a moving target through a process called phase advancing. Here we ask for functionally diverse neuron populations in the mouse retina how common is phase advancing and demonstrate that it is common and generated at multiple signaling stages.