Abstract
Axonal plasticity allows neurons to control their output, which critically determines the flow of information in the brain. Axon diameter can be regulated by activity, yet how morphological changes in an axon impact its function remains poorly understood. Axonal swellings have been found on Purkinje cell axons in the cerebellum both in healthy development and in neurodegenerative diseases, and computational models predicts that axonal swellings impair axonal function. Here we report that in young Purkinje cells, axons with swellings propagated action potentials with higher fidelity than those without, and that axonal swellings form when axonal failures are high. Furthermore, we observed that healthy young adult mice with more axonal swellings learn better on cerebellar-related tasks than mice with fewer swellings. Our findings suggest that axonal swellings underlie a form of axonal plasticity that optimizes the fidelity of action potential propagation in axons, resulting in enhanced learning.
Highlights
Axonal plasticity allows neurons to control their output, which critically determines the flow of information in the brain
A large proportion of axons with swellings propagated action potentials with very high fidelity, whereas only the occasional axon without a swelling propagated with similar fidelity (9.1% of control axons were high-fidelity; 55.5% of axons with swellings were high-fidelity; Mann–Whitney U-test, P = 0.05; Fig. 1d)
We found no differences in the axosomatic delay between recordings in axons with swelling and control axons (Fig. 1e and Supplementary Fig. 2), suggesting that swellings do not change the propagation speed of action potentials, or at least not over the relatively short distances that we have measured (Supplementary Fig. 2 and Supplementary Table 1)
Summary
Axonal plasticity allows neurons to control their output, which critically determines the flow of information in the brain. We report that in young Purkinje cells, axons with swellings propagated action potentials with higher fidelity than those without, and that axonal swellings form when axonal failures are high. Purkinje cell axonal swellings appear transiently during cerebellar development[3,4] and are observed during normal aging[5], including in healthy human samples[6,7] These data suggest that axonal swellings play a physiological role in the brain. By examining cerebellar-related behavior, we observed that mice exhibiting higher levels of cerebellar learning had higher numbers of axonal swellings These data suggest that the enhancement of action potential propagation associated with axonal swellings in healthy young animals positively impacts behavior
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