Direction Selectivity in the Retina Is Established Independent of Visual Experience and Cholinergic Retinal Waves

Abstract

Direction selectivity in the retina requires the asymmetric wiring of inhibitory inputs onto four subtypes of On-Off direction-selective ganglion cells (DSGCs), each preferring motion in one of four cardinal directions. The primary model for the development of direction selectivity is that patterned activity plays an instructive role. Here, we use a unique, large-scale multielectrode array to demonstrate that DSGCs are present at eye opening, in mice that have been reared in darkness and in mice that lack cholinergic retinal waves. These data suggest that direction selectivity in the retina is established largely independent of patterned activity and is therefore likely to emerge as a result of complex molecular interactions.

Role for Visual Experience in the Development of Direction-Selective Circuits

“…In contrast to our results reported here, previous reports from our laboratory that were based on multi-electrode array (MEA) recordings indicated that the cardinal distribution of preferred directions was established at eye-opening [5]. One potentially important difference is that the current study was the use of light stimulation of cones dominated by S-opsin in A second difference with the previous MEA study is that alignment of the preferred directions along the temporal and ventral quadrants were overrepresented [5,32], a bias that persisted in recordings from V1 at eye-opening [33] but was not seen here (Figure 2; Figure S3).…”

“…A second difference with the previous MEA study is that alignment of the preferred directions along the temporal and ventral quadrants were overrepresented [5,32], a bias that persisted in recordings from V1 at eye-opening [33] but was not seen here ( Figure 2; Figure S3). Interestingly, it was recently shown that DSGC preferred directions vary retinotopically (Sabbah, S., Gemmer, J., Castro, G., Siegel, J.…”

“…We found no significant difference for the DSIs of either ON and ON-OFF DSGCs across conditions [3,6], and a small but significant increase in the vector sum for ON-OFF DSGCs across development, as described previously [5,8], suggesting a visually-driven maturation …”

“…We found no significant difference for the DSIs of either ON and ON-OFF DSGCs across conditions [3,6], and a small but significant increase in the vector sum for ON-OFF DSGCs across development, as described previously [5,8], suggesting a visually-driven maturation of tuning properties. Though DSGCs were strongly tuned at eye-opening and after darkrearing, both ON and ON-OFF DSGCs in young and dark-reared mice retained the immature distribution of preferred directions, failing to cluster along the cardinal axes ( Figure 2; Figure S2).…”

“…How these preferred directions emerge during development is still not understood. Several studies have demonstrated that ON [2] and ON-OFF DSGCs are well tuned at eye-opening, and even a few days prior to eye-opening, in rabbits [3], rats [4] and mice [5][6][7][8], suggesting that visual experience is not required to produce direction selective tuning. However, here we show that at eye-opening the preferred directions of both ON and ON-OFF DSGCs are diffusely distributed and that visual deprivation prevents the preferred directions from clustering along the cardinal axes.…”