Activity-dependent homeostatic synaptic plasticity widens the temperature range of synaptic transmission

Abstract

The framework of homeostatic plasticity posits that neurons regulate cellular properties through feedback homeostasis to maintain activity during changes in the environment. However, when disturbances occur in wild animals they are often caused by environmental variables that induce their own acclimation effects, making it difficult to discern if activity-sensitive feedback plays a role in ecological settings. We addressed this problem using a natural activity perturbation, where frogs hibernate in cold water, leaving brainstem motor circuits that generate breathing inactive for long periods. We show here that motor inactivity, amid complex environmental variables in the hibernation environment, represents a key signal for increasing AMPA-glutamate receptors (AMPARs) on motoneurons. Homeostatic upregulation of AMPARs do not regulate neural activity per se but instead correspond with enhanced evoked transmission selectively at cool temperatures. The results show how homeostatic synaptic plasticity may allow animals to restart motor behavior after chronic inactivity encountered in the natural environment. More broadly, these results introduce the concept of homeostatic plasticity as a mechanism to shape thermal tolerance ranges of neural performance in ecological settings.