Particle motion is broadly represented in the vestibular medulla of the bullfrog across larval development

Abstract

In their shallow-water habitats, bullfrog (Rana catesbeiana) tadpoles are exposed to both underwater and airborne sources of acoustic stimulation. We probed the representation of underwater particle motion throughout the tadpole’s dorsal medulla to determine its spatial extent over larval life. Using neurobiotin-filled micropipettes, we recorded neural activity to z-axis particle motion (frequencies of 40–200 Hz) in the medial vestibular nucleus, lateral vestibular nucleus, dorsal medullary nucleus (DMN), and along the dorsal arcuate pathway. Sensitivity was comparable in the medial and lateral vestibular nuclei, with estimated thresholds between 0.016 and 12.5 μm displacement. Neither best responding frequency nor estimated threshold varied significantly over larval stage. Transport of neurobiotin from active recording sites was also stable over development. The DMN responded poorly to z-axis particle motion, but did respond to low-frequency pressure stimulation. These data suggest that particle motion is represented widely and stably in the tadpole’s vestibular medulla. This is in marked contrast to the representation of pressure stimulation in the auditory midbrain, where a transient “deaf period” of non-responsiveness and decreased connectivity occurs immediately prior to metamorphic climax. We suggest that, in bullfrogs, sensitivity to particle motion and to pressure follows different developmental trajectories.

Representation of particle motion in the auditory midbrain of a developing anuran

“…As previously discussed (Simmons and Flores 2012), thresholds in the vestibular medulla are higher without agar embedding. Still, in this region, there is no relationship between threshold at BRF and developmental stage.…”

“…Driven response rates (spike rate in the stimulus interval compared to that in the interstimulus interval) were calculated from dot raster plots. Consistent with a previous study of particle motion sensitivity in the vestibular medulla (Simmons and Flores 2012), the best frequency of response (BRF) was defined as that stimulus frequency producing the best driven response at the lowest stimulus amplitude tested. Because spontaneous activity was low or absent, threshold was estimated as the lowest stimulus amplitude in which spikes were obtained in the stimulus interval.…”

“…In subsequent experiments (n = 21), the animal was embedded, up to the level of the surgical opening, into 10 % ultra-low gelling temperature agarose (Type IX, Sigma; as used by Flores 2012 andLu andDeSmidt 2013), and then the agarose block was secured to the platform. Experiments using this second method found generally lower thresholds to particle motion from the vestibular medulla, although a range of neural sensitivity was observed using both methods (Horowitz et al 2007a;Simmons and Flores 2012).…”

“…Underwater particle motion in the z (vertical) plane was produced using a shaker table system, as previously described (Horowitz et al 2007a;Simmons and Flores 2012). A water-filled cylindrical (18 cm diameter, 7.6 cm depth) aluminum recording dish, with an attached perforated Lucite platform, was used to hold the animal.…”

Better than fish on land? Hearing across metamorphosis in salamanders

“…In most anurans, it is overcome by development of a tympanic middle ear during or after metamorphosis [14], resulting in improved pressure sensitivity of the adults in addition to the particle-motion-sensitive ear found in the aquatic juveniles [15]. However, not all amphibians develop a tympanic middle ear during metamorphosis.…”