Abstract
ABSTRACTAxon regeneration is critical for restoring neural function after spinal cord injury. This has prompted a series of studies on the neural and functional recovery of lampreys after spinal cord transection. Despite this, there are still many basic questions remaining about how much functional recovery depends on axon regeneration. Our goal was to examine how swimming performance is related to degree of axon regeneration in lampreys recovering from spinal cord transection by quantifying the relationship between swimming performance and percent axon regeneration of transected lampreys after 11 weeks of recovery. We found that while swimming speeds varied, they did not relate to percent axon regeneration. In fact, swimming speeds were highly variable within individuals, meaning that most individuals could swim at both moderate and slow speeds, regardless of percent axon regeneration. However, none of the transected individuals were able to swim as fast as the control lampreys. To swim fast, control lampreys generated high amplitude body waves with long wavelengths. Transected lampreys generated body waves with lower amplitude and shorter wavelengths than controls, and to compensate, transected lampreys increased their wave frequencies to swim faster. As a result, transected lampreys had significantly higher frequencies than control lampreys 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.
Highlights
Spinal cord injury in mammals, including humans, leads to permanent loss of movement and sensation because the regeneration of damaged or lost axons within the central nervous system is limited
In this cohort of animals, the percent axon regeneration in the spinal cords of individuals was between 33.3 and 84.2% with a median of 58.6%, which is similar to that reported in previous studies (Lau et al, 2013; Oliphint et al, 2010; Yin and Selzer, 1983), providing a range of neural regeneration to compare with behavioral performance
One of the primary goals of this study was to examine how swimming performance was related to degree of RS axon regeneration in lampreys recovering from spinal cord transection
Summary
Spinal cord injury in mammals, including humans, leads to permanent loss of movement and sensation because the regeneration of damaged or lost axons within the central nervous system is limited. Amongst the highly regenerative species, lampreys (family Petromyzontidae) have become a leading model for the study of neural mechanisms of spinal cord regeneration over the last 50 years owing to the robustness and reproducibility with which behavioral recovery occurs after injury, combined with the ability to image long-distance regeneration of descending reticulospinal (RS) axons and to perform electrophysiology recordings from regenerating neurons (Rovainen, 1976; Selzer, 1978; Cohen et al, 1986; Cooke and Parker, 2009; Oliphint et al, 2010; Parker, 2017; Hanslik et al, 2019). We still do not fully understand how behavioral recovery relates to regeneration of descending RS axons or plasticity within other neuronal subtypes comprising the spinal locomotor circuits
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