Swimming kinematics and performance of spinal transected lampreys with different levels of axon regeneration

Abstract

Neural and functional recovery in lampreys from spinal cord transection has been well documented. However, the extent of axon regeneration is highly variable and it is not known whether it is related to the level of behavioral recovery. To address this, we examined how swimming kinematics were related to axon regeneration by quantifying the relationship between swimming performance and percent axon regeneration of transected lampreys after 11 weeks of recovery. We found that swimming speed was not related to percent axon regeneration but it was closely related to body wave frequency and speed. However, wave frequency and speed varied greatly within individuals which resulted in swimming speed also varying within individuals. In fact, most recovered individuals, regardless of percent axon regeneration, could swim at fast and slow speeds. However, none of the transected individuals were able to generate body waves as large as the control lampreys. In order to swim faster, transected lampreys increased their wave frequencies and, as a result, transected lampreys had much higher frequencies than control lamprey at comparable swimming velocities. These data suggest that the control lampreys swam more efficiently than transected lampreys. In conclusion, there appears to be a minimal recovery threshold in terms of percent axon regeneration required for lampreys to be capable of swimming, however, there also seems to be a limit to how much they can behaviorally recover.

Resilience of neural networks for locomotion

“…Remarkably, lampreys can recover nearly normal swimming after one or two complete spinal transections (Fig. 3A and B) (Hanslik et al 2019), though with slower swim speed and mildly altered body kinematics (Oliphint et al 2010;Fies et al 2021). Functional recovery occurs even when only 30-50% of the descending reticulospinal axons regenerate across the lesion site, regrow in atypical paths, and terminate prematurely (Fig.…”

“…2010; Fies et al . 2021). Functional recovery occurs even when only 30–50% of the descending reticulospinal axons regenerate across the lesion site, regrow in atypical paths, and terminate prematurely (Fig.…”