Postembryonic growth of the macula neglecta auditory detector in the ray, <i>Raja clavata</i>: Continual increases in hair cell number, neural convergence, and physiological sensitivity

TLDR

The study proposes a double‑gradient interaction between growing nerves and new hair cells to explain continuous production of functional, oriented hair cells. The proposed mechanism involves a double‑gradient interaction between nerve growth and hair cell proliferation that shapes synaptic connectivity. Quantitative analysis shows that the macula neglecta of Raja clavata continuously generates 1–3 new hair cells per day, expanding from ~500 at birth to 6,000 at seven years, while neurons hypertrophy rather than proliferate, leading to increased convergence and a 500‑fold rise in sensitivity (40–200 Hz) with stable directional tuning and minimal gravity dependence, contrasting with the postnatal immaturity of mammalian ears.

Abstract

Abstract Quantitative scanning electron microscopy in an age series demon‐strated that the macula neglecta auditory epithelium of the ray, Raja clavata , produces and accumulates sensory cells perpetually at 1–3 cells/ day, so that the total increases from approximately 500 cells at birth to 6,000 at 7 years of age. The shape of the macula also changes with growth, and changes in the marginal zones of small and intermediate size hair cells are consistent with this differential growth and their proposed role as hair cell production sites. The neurons contacting the epithelium do not increase in number as animals age; instead they hypertrophy, increasing axon diame‐ter and terminal field size. A hypothetical double‐gradient interaction be‐tween the growing nerves and new hair cells is proposed to explain the devel‐opment of synaptic connections and the continual production of individually oriented, functional hair cells. Electrophysiological recordings from the neu‐rons demonstrated best sensitivities between 40 Hz and 200 Hz, directional receptive fields, and little or no effect of changes in the ear's position relative to gravity. The convergence ratio from sensory cells to neurons increases because of their unequal patterns of growth, and physiological sensitivity improves 500‐fold and more as these animals age. These results contrast with current information on mammalian ears, where it appears that sensory cells are not produced at any time after birth.