Reproductive and diurnal rhythms regulate vocal motor plasticity in a teleost fish

Abstract

SUMMARYSeasonal and circadian rhythms control fundamental physiological processes including neural excitability and synaptic plasticity that can lead to the periodic modulation of motor behaviors like social vocalizations. Parental male midshipman fish produce three call types during the breeding season: long duration (min to >1 h) advertisement 'hums', frequency and amplitude modulated agonistic 'growls' (s), and very brief (ms) agonistic 'grunts' produced either singly or repetitively as 'grunt trains' for up to several minutes. Fictive grunts that establish the temporal properties of natural grunts are readily evoked and recorded in vivo from vocal occipital nerve roots at any time of day or year by electrical microstimulation in either the midbrain periaqueductal gray or a hindbrain vocal pre-pacemaker nucleus. Now, as shown here, the longer duration fictive growls and hums can also be elicited, but are restricted to the nocturnal reproductive season. A significant drop in call threshold accompanies the fictive growls and hums that are distinguished by their much longer duration and lower and more regular firing frequency. Lastly, the long duration fictive calls are dependent upon increased stimulation time and intensity and hence may result from activitydependent changes in the vocal motor circuit that are themselves modulated by seasonal and circadian rhythms.

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

“…Unlike the vocal motor system (Rubow and Bass, 2009), we found no photoperiod-dependent sensitivity in any measures of evoked saccular potentials in reproductive type I males. The results may reflect the divergent demands on vocal and auditory systems.…”

“…Additionally, we investigated whether saccular physiology and steroid levels vary as a function of morphometric measures (standard length, relative gonad mass), time in captivity, and time of day. Unlike vocal motor excitability (Rubow and Bass, 2009), we found no measurable diel shifts in saccular hair cell physiology in reproductive males, showing the restriction of this form of acoustic plasticity to comparatively longer-term seasonal patterns. .…”

“…Our primary goal was to test the hypothesis that type I males exhibit seasonal auditory plasticity at the hair cell level comparable to that recently shown for females (Sisneros, 2009), and that this seasonality correlates with reproductive state and levels of circulating steroid hormones. Type I males were the focus because they show seasonal plasticity in vocal physiology (unknown for type IIs) and wild-caught populations of both non-reproductive and reproductive individuals are readily available (Rubow and Bass, 2009). Our findings are significant in several regards.…”

“…Type I males show diel and seasonal shifts in vocal motor excitability: compared with non-reproductive males tested any time of day and reproductive males tested during the day, nocturnal reproductive type I males show both a marked increase in duration of, and decrease in threshold to elicit, the vocal motor volley that directly sets natural call duration and frequency (Rubow and Bass, 2009). Because the vocal system has direct input to central auditory circuitry Chagnaud et al, 2009;Weeg et al, 2005), a subset of reproductive type I males (N4 animals, nine tuning curves) were tested during the subjective night.…”

“…above background noise measurements. Plasticity of hair cell sensitivity Eastern Standard Time (EST) (Rubow and Bass, 2009). All experiments were conducted during the subjective day except for a subset that were conducted after 18:00h EST during the subjective night to test the hypothesis that peripheral auditory plasticity has a daily cycle as found in the vocal motor system (Rubow and Bass, 2009).…”