Subterranean Fishes of the World

6015

2022

Sensory systems are the nexus between the brain and the environment, and therefore must maintain a constant physiological state of responsiveness to accurately detect change and perceive the world around them. There are many challenges sensors must overcome to maintain responsiveness, such as fatigue from overstimulation and physiochemical imbalance in unstable environments. Meanwhile the lateral line is a critical regulator of behaviors such as predator avoidance, navigation, and prey detection. Therefore, reliable stimulus detection and accurate sensory processing is key to survival. Despite frequent circumstances that increases noise or theoretically blocks signal transduction, lateral line hair cells exhibit neurophysiological mechanisms to robustly maintain accurate responsiveness to relevant stimuli. Electrophysiological recordings revealed zebrafish (Danio rerio) lateral line afferent neurons are partially inhibited during motor commands. Selective ablation of hindbrain efferent neurons eliminated the inhibitory corollary discharges necessary to filter afferent signaling and mitigate sensor fatigue during locomotion. Our understanding of such sensory mechanisms and behavior is challenging to contextualize within the framework of evolution without the use of a comparative model. Therefore, we compared activity of lateral line afferent neurons across Mexican tetra (Astyanax mexicanus) populations to investigate how shifts in sensory function impacts behavioral diversity. We identified differences in intrinsic afferent signaling, evoked responses, and gain control between surface fish and three independently-derived blind cavefish populations. Our results indicate that, following eye-loss, partial loss of efferent function convergently evolved and increased lateral line sensitivity during motor commands. We hypothesize this facilitates adaptive behaviors such as active flow sensing which are dependent on self-generated flow stimuli. Both zebrafish and Mexican tetra are freshwater species, and it is understood that their lateral line hair cells follow a cation driven mechanotransduction process despite typical freshwater habitats being severely cation deficient. Using larval zebrafish, we upend a long-standing assumption that the cupula maintains a cationic microenvironment that facilitates hair cell activation. Our findings indicate an alternative mechanism of anion efflux supports hair cell depolarization via calcium-activated chloride channels in cation deficient environments. Altogether, this dissertation uncovers novel neurophysiological mechanisms of maintaining lateral line sensitivity on both developmental and evolutionary timescales.

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