Functional properties of retinal ganglion cells during optic nerve regeneration in the goldfish

Abstract

After being severed, optic axons in goldfish regenerate and eventually restore the retinotectal map; refinement of the map depends upon impulse activity generated by the ganglion cells. Because little is known about the changes in activity and receptive-field properties of ganglion cells during regeneration, we made extracellular recordings from them in the intact eye up to 95 days after sectioning their axons in the optic tract. Their receptive fields were classified as OFF-, ON–OFF-, or ON-centers, and their axonal conduction velocities measured by antidromic activation. The rate of encountering single units dropped drastically at 4–8 days postsection when only a few OFF-center units could be recorded, recovering to normal between 42 and 63 days. Receptive-field centers were normal in size, except for the few OFF-centers at 4–8 days which were abnormally large. Maintained discharge rates of all types were depressed up to 42 days, but ON–OFF-center units were more spontaneously active than normal around 42 days. Light-evoked responses in OFF-center units were subnormal at 4–8 days, becoming supernormal at 16 days and normal thereafter. ON–OFF- and ON-center units started to regain responsiveness at 16 days, and became supernormal at 42 days, before returning to normal. Conduction velocities of all fiber groups dropped to a minimum at 8 days, the fastest being affected most. There was a gradual recovery to normal conduction velocity by 63 days. The conduction latencies of OFF- and ON–OFF-center units recovered to normal by 42 days, and ON-center units by 63 days. Recovery of ganglion cell responsiveness correlates with functional recovery in the retinotectal system: OFF-center units recover light-evoked responses at about the time OFF activity first reappears in the tectum. ON- and ON–OFF-center units recover later, exhibiting supernormal spiking activity around the time that ON responses reappear in the tectum.