Identification of Retinal Ganglion Cells and Their Projections Involved in Central Transmission of Information about Upward and Downward Image Motion

Keisuke Yonehara,Masaharu Noda,Takafumi Shintani,Hiroshi Ishikane,Shiro Usui,Hiraki Sakuta,Nilton L Kamiji,Kayo Nakamura-Yonehara,Andrew Iwaniuk

doi:10.1371/journal.pone.0004320

Abstract

The direction of image motion is coded by direction-selective (DS) ganglion cells in the retina. Particularly, the ON DS ganglion cells project their axons specifically to terminal nuclei of the accessory optic system (AOS) responsible for optokinetic reflex (OKR). We recently generated a knock-in mouse in which SPIG1 (SPARC-related protein containing immunoglobulin domains 1)-expressing cells are visualized with GFP, and found that retinal ganglion cells projecting to the medial terminal nucleus (MTN), the principal nucleus of the AOS, are comprised of SPIG1+ and SPIG1− ganglion cells distributed in distinct mosaic patterns in the retina. Here we examined light responses of these two subtypes of MTN-projecting cells by targeted electrophysiological recordings. SPIG1+ and SPIG1− ganglion cells respond preferentially to upward motion and downward motion, respectively, in the visual field. The direction selectivity of SPIG1+ ganglion cells develops normally in dark-reared mice. The MTN neurons are activated by optokinetic stimuli only of the vertical motion as shown by Fos expression analysis. Combination of genetic labeling and conventional retrograde labeling revealed that axons of SPIG1+ and SPIG1− ganglion cells project to the MTN via different pathways. The axon terminals of the two subtypes are organized into discrete clusters in the MTN. These results suggest that information about upward and downward image motion transmitted by distinct ON DS cells is separately processed in the MTN, if not independently. Our findings provide insights into the neural mechanisms of OKR, how information about the direction of image motion is deciphered by the AOS.

Highlights

Visual information is segregated into modalities such as color, form, and motion at the level of the retina [1]
We found again that axons belonging to the AOT-IF and terminating in the MTN was subdivided into the dorsal division (MTNd) are predominantly positive for green fluorescent protein (GFP) (Figure S2, B, lower panels), whereas axons belonging to the AOTSF are almost negative for GFP (Figure S2, A, B, upper panels)
We show that the each mosaic population corresponds to a physiological subtype of ON DS cells with distinct preferred direction, upward or downward

Summary

Introduction

Visual information is segregated into modalities such as color, form, and motion at the level of the retina [1]. Two types of direction-selective (DS) ganglion cells, ON DS ganglion cells and ON-OFF DS ganglion cells, present in the retina of many vertebrate species [6], are known to code the direction of image motion [7,8]. It is known that ON DS cells comprise three physiological subtypes distinguished by their preferred directions, each corresponding to upward, downward, or temporal-to-nasal motion in the visual field [9]. ON-OFF DS cells are of four subtypes; their preferred directions are orthogonal and correspond roughly to upward, downward, temporal-to-nasal, and nasal-to-temporal motion [10]. The mechanism underlying the detection of motion direction is presumably common to ON and ON-OFF types [14,15], how direction-selective retinal circuitry is established during development still remains unknown. Identification of molecular markers for a single physiological subtype of DS cells would be useful to study its developmental mechanism

Methods

Results

Conclusion