Recovery of C-starts, equilibrium and targeted feeding after whole spinal cord crush in the adult goldfishCarassius auratus

Abstract

SUMMARYCentral nervous system neurons of many adult teleost fish are capable of regrowth across spinal cord lesions, which may result in behavioral recovery of swimming. Since there have been few, if any, studies that examine the return of behaviors other than swimming, we provide a quantitative analysis of the recovery of C-starts that occur in adult goldfish after spinal cord injury. In addition, we include a qualitative analysis of the return of targeted feeding and equilibrium. Whole spinal cord crushes near the junction of the brain and spinal cord [spinomedullary level (SML)] were made in 45 experimental fish. Eight sham-operated goldfish served as controls for the effects of the surgery procedures alone. After spinal cord crush and recovery from the anesthetic, experimental fish lay on their sides with no movement caudal to the wound. The fish were monitored for the return of behaviors for up to 190 days postoperatively. Twenty-five fish survived the course of this study. Of these fish, 12 regained equilibrium and C-starts, two regained equilibrium but not C-starts, and 11 did not regain equilibrium (one of these did display a C-start). Twenty-two of the 25 experimental fish that survived the 190 days were able to target food from the water surface. Quantitative analysis of recovered C-starts in this study revealed that the probability of eliciting the response is reduced, that latencies from stimulus to response are longer and that movement parameters (i.e. angles, distance and velocity)are reduced compared with those of sham-operated control animals for up to 190 days postoperatively. The recovery of C-starts, equilibrium and targeted feeding was due to re-growth across the wound site, since re-crushing the spinal cord at the SML resulted in the loss of these behaviors. Mauthner cells are known to initiate C-starts in goldfish. Since the majority of M-axons that regrow across a crush wound associate with an inappropriate pathway (i.e. the first ventral root), it is unlikely that these cells play a major role in the return of C-starts. We propose that regeneration of Mauthner cell homologues across the wound site is responsible for the recovery of most C-starts. The identifiability of the M-cell and its homologues provides a unique opportunity to analyze the mechanisms underlying behavioral recovery at the cellular level.