Estrogen synthesis and signaling in the brains of vertebrates has pleotropic effects ranging from neurogenesis to modulation of behaviors. The majority of studies on brain‐derived estrogens focus on males, but estrogenic signaling in females likely plays important roles in regulation of reproductive cycling and social behaviors. We used females of the mouth brooding African cichlid fish,
Nitric oxide (NO) produced by the enzyme neuronal nitric oxide synthase serves as an important neurotransmitter in the central nervous system that is involved in reproductive regulation, learning, sensory processing, and other forms of neural plasticity. Here, we map the distribution of
- NSF-PAR ID:
- 10372599
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Journal of Comparative Neurology
- Volume:
- 530
- Issue:
- 16
- ISSN:
- 0021-9967
- Format(s):
- Medium: X Size: p. 2901-2917
- Size(s):
- ["p. 2901-2917"]
- Sponsoring Org:
- National Science Foundation
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Abstract Astatotilapia burtoni , to test for reproductive state‐dependent changes in estrogenic signaling capacity within microdissected brain nuclei that are important for social behaviors. Expression levels of the rate‐limiting enzyme aromatase, but not estrogen receptors, measured by qPCR changes across the reproductive cycle. Gravid females that are close to spawning had higher aromatase levels in all brain regions compared to females with lower reproductive potential. This brain aromatase expression was positively correlated with circulating estradiol levels and ovarian readiness. Using chromogenic in situ hybridization we localized aromatase‐expressing cells to ependymal regions bordering the ventricles from the forebrain to the hindbrain, and observed more abundant staining in gravid compared to mouth brooding females in most regions. Staining was most prominent in subpallial telencephalic regions, and diencephalic regions of the preoptic area, thalamus, and hypothalamus, but was also observed in sensory and sensorimotor areas of the midbrain and hindbrain. Aromatase expression was observed in radial glial cells, revealed by co‐localization with the glial marker GFAP and absence of co‐localization with the neuronal marker HuC/D. Collectively these results support the idea that brain‐derived estradiol in females may serve important functions in reproductive state‐dependent physiological and behavioral processes across vertebrates. -
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Neural communication depends on release and reception of different neurotransmitters within complex circuits that ultimately mediate basic biological functions. We mapped the distribution of glutamatergic, GABAergic, and cholinergic neurons in the brain of the African cichlid fish
Astatotilapia burtoni using in situ hybridization to label vesicular glutamate transporters (vglut1, vglut2.1, vglut3 ), glutamate decarboxylases (gad1, gad2 ), and choline acetyltransferase (chat ). Cells expressing the glutamatergic markersvgluts 1–3 show primarily nonoverlapping distribution patterns, with the most widespread expression observed forvglut2.1 , and more restricted expression ofvglut1 andvglut3. vglut1 is prominent in granular layers of the cerebellum, habenula, preglomerular nuclei, and several other diencephalic, mesencephalic, and rhombencephalic regions.vglut2.1 is widely expressed in many nuclei from the olfactory bulbs to the hindbrain, whilevglut3 is restricted to the hypothalamus and hindbrain. GABAergic cells show largely overlappinggad1 andgad2 expression in most brain regions. GABAergic expression dominates nuclei of the subpallial ventral telencephalon, while glutamatergic expression dominates nuclei of the pallial dorsal telencephalon.chat ‐expressing cells are prominent in motor cranial nerve nuclei, and some scattered cells lie in the preoptic area and ventral part of the ventral telencephalon. A localization summary of these markers within regions of the conserved social decision‐making network reveals a predominance of either GABAergic or glutamatergic cells within individual nuclei. The neurotransmitter distributions described here in the brain of a single fish species provide an important resource for identification of brain nuclei in other fishes, as well as future comparative studies on circuit organization and function. J. Comp. Neurol. 525:610–638, 2017. © 2016 Wiley Periodicals, Inc. -
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Abstract Galanin is a peptide that regulates pituitary hormone release, feeding, and reproductive and parental care behaviors. In teleost fish, increased galanin expression is associated with territorial, reproductively active males. Prior transcriptome studies of the plainfin midshipman (
Porichthys notatus ), a highly vocal teleost fish with two male morphs that follow alternative reproductive tactics, show that galanin is upregulated in the preoptic area‐anterior hypothalamus (POA‐AH) of nest‐holding, courting type I males during spawning compared to cuckolding type II males. Here, we investigate possible differences in galanin immunoreactivity in the brain of both male morphs and females with a focus on vocal‐acoustic and neuroendocrine networks. We find that females differ dramatically from both male morphs in the number of galanin‐expressing somata and in the distribution of fibers, especially in brainstem vocal‐acoustic nuclei and other sensory integration sites that also differ, though less extensively, between the male morphs. Double labeling shows that primarily separate populations of POA‐AH neurons express galanin and the nonapeptides arginine‐vasotocin or isotocin, homologues of mammalian arginine vasopressin and oxytocin that are broadly implicated in neural mechanisms of vertebrate social behavior including morph‐specific actions on vocal neurophysiology in midshipman. Finally, we report a small population of POA‐AH neurons that coexpress galanin and the neurotransmitter γ‐aminobutyric acid. Together, the results indicate that galanin neurons in midshipman fish likely modulate brain activity at a broad scale, including targeted effects on vocal motor, sensory and neuroendocrine systems; are unique from nonapeptide‐expressing populations; and play a role in male‐specific behaviors. -
Synopsis Intra- and inter-sexual communications are vital to the survival and reproductive success of animals. In species that cycle in and out of breeding or other physiological condition, sensory function can be modulated to optimize communication at crucial times. Little is known, however, about how widespread this sensory plasticity is across taxa, whether it occurs in multiple senses or both sexes within a species, and what potential modulatory substances and substrates are involved. Thus, studying modulation of sensory communication in a single species can provide valuable insights for understanding how sensory abilities can be altered to optimize detection of salient signals in different sensory channels and social contexts. The African cichlid fish Astatotilapia burtoni uses multimodal communication in social contexts such as courtship, territoriality, and parental care and shows plasticity in sensory abilities. In this review, we synthesize what is known about how visual, acoustic, and chemosensory communication is used in A. burtoni in inter- and intra-specific social contexts, how sensory funtion is modulated by an individual’s reproductive, metabolic, and social state, and discuss evidence for plasticity in potential modulators that may contribute to changes in sensory abilities and behaviors. Sensory plasticity in females is primarily associated with the natural reproductive cycle and functions to improve detection of courtship signals (visual, auditory, chemosensory, and likely mechanosensory) from high-quality males for reproduction. Plasticity in male sensory abilities seems to function in altering their ability to detect the status of other males in the service of territory ownership and future reproductive opportunities. Changes in different classes of potential modulators or their receptors (steroids, neuropeptides, and biogenic amines) occur at both peripheral sensory organs (eye, inner ear, and olfactory epithelium) and central visual, olfactory, and auditory processing regions, suggesting complex mechanisms contributing to plasticity of sensory function. This type of sensory plasticity revealed in males and females of A. burtoni is likely more widespread among diverse animals than currently realized, and future studies should take an integrative and comparative approach to better understand the proximate and ultimate mechanisms modulating communication abilities across taxa.more » « less
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Synopsis Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared with non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g., sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared with mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.
