Androgen-Induced Changes in the Response Dynamics of Ampullary Electrosensory Primary Afferent Neurons

Abstract

Male stingrays use their ampullary electroreceptors to locate mates, but the effect of gonadal androgens on electrosensory encoding during the reproductive season is unknown. We tested the hypothesis that gonadal androgens induce neurophysiological changes in the electrosense of male Atlantic stingrays. During the primary androgen increase in wild males, the electrosensory primary afferent neurons show an increase in discharge regularity, a downshift in best frequency (BF) and bandpass, and a greater sensitivity to low-frequency stimuli from 0.01 to 4 Hz. Experimental implants of dihydrotestosterone in male stingrays induced a similar lowered BF and bandpass and increased average neural sensitivity to low-frequency stimuli (0.5-2 Hz) by a factor of 1.5. Primary afferents from long ampullary canals (Ͼ3 cm) were more sensitive and had a lower bandpass and BF than did afferents from short canals (Ͻ2 cm). We propose that these androgen-induced changes in the frequency response properties of electrosensory afferents enhance mate detection by male stingrays and may ultimately increase the number of male reproductive encounters with females. Furthermore, differences in primary afferent sensitivity among short and long canals may facilitate detection, orientation, and localization of conspecifics during social interactions.

Feedback and Feedforward Control of Frequency Tuning to Naturalistic Stimuli

“…However, these shifts are often observed in higher centers of the nervous system and typically involve developmental, experience-dependent, or hormonal changes, and develop over time scales of minutes to months (Kilgard and Merzenich, 1998;Sisneros and Tricas, 2000;Xiao and Suga, 2002;Sisneros and Bass, 2003;Sisneros et al, 2004;Tsodyks and Gilbert, 2004). Changes in tuning described here are rapid or switch like, appear immediately after altered stimulus geometry, and are more similar to changes in temporal response properties of retinal ganglion cells or V1 neurons seen, contingent on changes in stimulus spatial characteristics (Kuffler, 1951;Gallant, 2000, 2002).…”

Seasonal Plasticity of Peripheral Auditory Frequency Sensitivity

“…The time course of these events is consistent with a possible genomic effect on auditory receptors elicited via a reduction in natural circulating gonadal steroid levels. Similarly, naturally elevated levels of gonadal steroids before spawning may have a direct effect on the frequency sensitivity of auditory hair cells as proposed for the steroid-related changes in the frequency sensitivity characteristics of electroreceptors (Keller et al, 1986;Sisneros and Tricas, 2000). Among vertebrates in general, including the closely related toadfish (same Family and Order as midshipman), electrical resonance arising from the ion channel current kinetics of the basolateral membrane of the auditory hair cell is considered the major Relationship between vector strength (VS) of synchronization at best frequency (BF ) and resting discharge rate for auditory saccular afferent neurons recorded from female midshipman.…”

Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system

“…All work with these animals was done during June through to September of 2006 and 2007 according to approved IACUC protocols at both USC and UCLA. Species were studied at the same time of year to avoid effects of breeding season (Sisneros and Tricas, 2000).…”