Melatonin action in a midbrain vocal-acoustic network

Abstract

Melatonin is a well-documented time-keeping hormone that can entrain an individual's physiology and behavior to the day-night cycle, though surprisingly little is known about its influence on the neural basis of social behavior, including vocalization. Male midshipman fish (Porichthys notatus) produce several call types distinguishable by duration and by daily and seasonal cycles in their production. We investigated melatonin's influence on the known nocturnal-and breeding season-dependent increase in excitability of the midshipman's vocal network (VN) that directly patterns natural calls. VN output is readily recorded from the vocal nerve as a 'fictive call'. Five days of constant light significantly increased stimulus threshold levels for calls electrically evoked from vocally active sites in the medial midbrain, supporting previous findings that light suppresses VN excitability, while 2-iodomelatonin (2-IMel; a melatonin analog) implantation decreased threshold. 2-IMel also increased fictive call duration evoked from medial sites as well as lateral midbrain sites that produced several-fold longer calls irrespective of photoregime or drug treatment. When stimulus intensity was incrementally increased, 2-IMel increased duration only at lateral sites, suggesting that melatonin action is stronger in the lateral midbrain. For animals receiving 5 days of constant darkness, known to increase VN excitability, systemic injections of either of two mammalian melatonin receptor antagonists increased threshold and decreased duration for calls evoked from medial sites. Our results demonstrate melatonin modulation of VN excitability and suggest that social contextdependent call types differing in duration may be determined by neuro-hormonal action within specific regions of a midbrain vocalacoustic network.

Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish

“…This seasonal migration is quite remarkable as it requires adaptations to extreme changes in water depth and habitat which includes transitioning from the deep water benthos (down to 300m) to rocky subtidal/ intertidal shoreline (e.g., Tomales Bay, Puget Sound) where fish are often found within rocky nest shelters without water for several hours during low tide [6; 7; 8]. Little is known about specific environmental (abiotic or biotic) cues that induce the migration to shallow waters for spawning, although light/ dark cycle has recently been demonstrated to change neural excitability/ responsiveness of the vocal system (see below; [9; 10]) and is thus a likely cue. Interestingly, Foran et al [11] showed that gonadotropin-releasing hormone mRNA in neurons of the ventrolateral thalamic nucleus is modulated by retinal input, and these neurons, which project back to the retina may in turn modulate the visual system in response to seasonal changes in environmental light conditions.…”

“…The vocal occipital nerve volley described in the previous section is often referred to as a fictive call in an in vivo neurophysiological preparation because it is produced in the absence of muscle activation and directly determines natural call characters such as duration and PRR. Fictive calls are readily evoked following electrical stimulation or localized injections of glutamate in midbrain and forebrain (preoptic area-anterior hypothalamus) sites (e.g., [9; 42; 45; 46]). Several studies in midshipman and Gulf toadfish have used the fictive call in vivo preparation to identify rapid modulation of vocal motor activity by androgens (11-KT, testosterone), estrogens (17beta-estradiol), cortisol, vasoactive intestinal polypeptide (VIP), arginine-vasotocin (AVT; the non-mammalian homolog of arginine-vasopressin, AVP), and isotocin (IT; the non-mammalian homolog of oxytocin) and melatonin ([9; 24; 65; 79; 81; 82; 83; 84]).…”

“…Fictive calls are readily evoked following electrical stimulation or localized injections of glutamate in midbrain and forebrain (preoptic area-anterior hypothalamus) sites (e.g., [9; 42; 45; 46]). Several studies in midshipman and Gulf toadfish have used the fictive call in vivo preparation to identify rapid modulation of vocal motor activity by androgens (11-KT, testosterone), estrogens (17beta-estradiol), cortisol, vasoactive intestinal polypeptide (VIP), arginine-vasotocin (AVT; the non-mammalian homolog of arginine-vasopressin, AVP), and isotocin (IT; the non-mammalian homolog of oxytocin) and melatonin ([9; 24; 65; 79; 81; 82; 83; 84]). In general, each of these neurohormones can rapidly (within 5 – 10 minutes) modify fictive call duration when injected either exogenously into dorsal trunk (steroids and receptor antagonists) muscle or directly into the preoptic area-anterior hypothalamus (AVT, IT, and receptor antagonists) or midbrain (VIP and a receptor antagonist).…”

“…Pilot studies showed that melatonin did not exert rapid effects on fictive call properties as shown for steroids and the neuropeptides AVT and IT (see above). Adopting the experimental design of Rubow and Bass [10], Feng and Bass [9] showed that five day treatments with either melatonin (via a single intraperitoneal implants) or melatonin receptor antagonists (via daily intramuscular injections into the body wall) could essentially antagonize the effects of housing under 5LL (suppression of vocal motor excitability) or 5DD (potentiation of vocal excitability) conditions, respectively (Fig. 6B).…”

Comparative Neurobiology of Sound Production in Fishes

“…Since the vertebrate time-keeping hormone melatonin shows elevated levels at night that is abolished under constant light (Falcón et al 2010), we recently tested whether changes in vocal excitability under constant photo-regimes are melatonindependent in type I male midshipman (Feng and Bass 2014). Melatonin implants in fish held under 5 days of constant light decreased fictive call threshold and increased fictive call duration, effectively rescuing the decreased vocal excitability seen in control animals.…”