Dataset Information

Attention and Motivated Response to Simulated Male Advertisement Call Activates Forebrain Dopaminergic and Social Decision-Making Network Nuclei in Female Midshipman Fish.

ABSTRACT: Little is known regarding the coordination of audition with decision-making and subsequent motor responses that initiate social behavior including mate localization during courtship. Using the midshipman fish model, we tested the hypothesis that the time spent by females attending and responding to the advertisement call is correlated with the activation of a specific subset of catecholaminergic (CA) and social decision-making network (SDM) nuclei underlying auditory- driven sexual motivation. In addition, we quantified the relationship of neural activation between CA and SDM nuclei in all responders with the goal of providing a map of functional connectivity of the circuitry underlying a motivated state responsive to acoustic cues during mate localization. In order to make a baseline qualitative comparison of this functional brain map to unmotivated females, we made a similar correlative comparison of brain activation in females who were unresponsive to the advertisement call playback. Our results support an important role for dopaminergic neurons in the periventricular posterior tuberculum and ventral thalamus, putative A11 and A13 tetrapod homologues, respectively, as well as the posterior parvocellular preoptic area and dorsomedial telencephalon, (laterobasal amygdala homologue) in auditory attention and appetitive sexual behavior in fishes. These findings may also offer insights into the function of these highly conserved nuclei in the context of auditory-driven reproductive social behavior across vertebrates.

SUBMITTER: Forlano PM

PROVIDER: S-EPMC5886316 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Attention and Motivated Response to Simulated Male Advertisement Call Activates Forebrain Dopaminergic and Social Decision-Making Network Nuclei in Female Midshipman Fish.

Forlano Paul M PM Licorish Roshney R RR Ghahramani Zachary N ZN Timothy Miky M Ferrari Melissa M Palmer William C WC Sisneros Joseph A JA

Integrative and comparative biology 20171001 4

Little is known regarding the coordination of audition with decision-making and subsequent motor responses that initiate social behavior including mate localization during courtship. Using the midshipman fish model, we tested the hypothesis that the time spent by females attending and responding to the advertisement call is correlated with the activation of a specific subset of catecholaminergic (CA) and social decision-making network (SDM) nuclei underlying auditory- driven sexual motivation. I ...[more]

PMID: 28992072

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Project description:Background: Left cervical vagus nerve stimulation (l-VNS) is an FDA-approved treatment for neurological disorders including epilepsy, major depressive disorder, and stroke, and l-VNS is increasingly under investigation for a range of other neurological indications. Traditional l-VNS is thought to induce therapeutic neuroplasticity in part through the coordinated activation of multiple broadly projecting neuromodulatory systems in the brain. Recently, it has been reported that striking lateralization exists in the anatomical and functional connectivity between the vagus nerves and the dopaminergic midbrain. These emerging findings suggest that VNS-driven activation of this important plasticity-promoting neuromodulatory system may be preferentially driven by targeting the right, rather than the left, cervical nerve. Objective: To compare the effects of right cervical VNS (r-VNS) vs. traditional l-VNS on self-administration behavior and midbrain dopaminergic activation in rats. Methods: Rats were implanted with a stimulating cuff electrode targeting either the right or left cervical vagus nerve. After surgical recovery, rats underwent a VNS self-administration assay in which lever pressing was paired with r-VNS or l-VNS delivery. Self-administration was followed by extinction, cue-only reinstatement, and stimulation reinstatement sessions. Rats were sacrificed 90 min after completion of behavioral training, and brains were removed for immunohistochemical analysis of c-Fos expression in the dopaminergic ventral tegmental area (VTA) and substantia nigra pars compacta (SNc), as well as in the noradrenergic locus coeruleus (LC). Results: Rats in the r-VNS cohort performed significantly more lever presses throughout self-administration and reinstatement sessions than did rats in the l-VNS cohort. Moreover, this appetitive behavioral responding was associated with significantly greater c-Fos expression among neuronal populations within the VTA, SNc, and LC. Differential c-Fos expression following r-VNS vs. l-VNS was particularly prominent within dopaminergic midbrain neurons. Conclusion: Our results support the existence of strong lateralization within vagal-mesencephalic signaling pathways, and suggest that VNS targeted to the right, rather than left, cervical nerve preferentially activates the midbrain dopaminergic system. These findings raise the possibility that r-VNS could provide a promising strategy for enhancing dopamine-dependent neuroplasticity, opening broad avenues for future research into the efficacy and safety of r-VNS in the treatment of neurological disease.

Project description:Background:Brachycephalus are among the smallest terrestrial vertebrates in the world. The genus encompasses 34 species endemic to the Brazilian Atlantic Rainforest, occurring mostly in montane forests, with many species showing microendemic distributions to single mountaintops. It includes diurnal species living in the leaf litter and calling during the day, mainly during the warmer months of the year. The natural history of the vast majority of the species is unknown, such as their advertisement call, which has been described only for seven species of the genus. In the present study, we describe the advertisement call of Brachycephalus albolineatus, a recently described microendemic species from Santa Catarina, southern Brazil. Methods:We analyzed 34 advertisement calls from 20 individuals of B. albolineatus, recorded between 5 and 6 February 2016 in the type locality of the species, Morro Boa Vista, on the border between the municipalities of Jaraguá do Sul and Massaranduba, Santa Catarina, southern Brazil. We collected five individuals as vouchers (they are from the type series of the species). We used the note-centered approach to describe the advertisement calls of the species. Results:B. albolineatus have a long advertisement call of 40-191 s (mean of 88 s) composed of 8-29 notes (mean of 17 notes) emitted at a rate of 6-18 notes per minute (mean of 11 notes per minute) and at a note dominant frequency of five to seven kHz (mean of six kHz). Advertisement calls are composed of isolated notes and note groups (two notes involved in each particular note group); the former is composed by one to three pulses (mean of 2.0) and the note groups by two or three pulses in each note (mean of 2.7). Most advertisement calls present both isolated notes and note groups, with a few cases showing only the former. Note groups are emitted invariably in the last third of the advertisement call. Most isolated notes escalate their number of pulses along the advertisement call (1-2, 1-3 or 2-3). Note duration of isolated notes varies from 0.002 to 0.037 s (mean of 0.020 s) and duration of note group vary from 0.360 to 0.578 s (mean of 0.465 s). Discussion:Individuals increase the complexity of their calls as they proceed, incorporating note groups and pulses per note. Intra-individual variation analysis also demonstrated that less structured advertisement calls (i.e., with notes with fewer pulses) are not stereotyped. It is possible that isolated notes and note groups could have distinct functions, perhaps territorial defense and mating, respectively. We argue that using a note-centered approach facilitates comparisons with calls of congeners, as well as underscores the considerable differences in call structure between species in a single group and among species groups.

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Project description:BackgroundIn anurans, differences in male mating calls have intensively been studied with respect to taxonomic classification, phylogeographic comparisons among different populations and sexual selection. Although overall successful, there is often much unexplained variation in these studies. Potential causes for such variation include differences among genotypes and breeding systems, as well as differences between populations. We investigated how these three factors affect call properties in male water frogs of Pelophylax lessonae (genotype LL), P. ridibundus (RR) and their interspecific hybrid P. esculentus which comes in diploid (LR) and triploid types (LLR, LRR).ResultsWe investigated five call parameters that all showed a genomic dosage effect, i.e. they either decreased or increased with the L/R ratio in the order LL-LLR-LR-LRR-RR. Not all parameters differentiated equally well between the five genotypes, but combined they provided a good separation. Two of the five call parameters were also affected by the breeding system. Calls of diploid LR males varied, depending on whether these males mated with one or both of the parental species (diploid systems) or triploid hybrids (mixed ploidy systems). With the exception of the northernmost mixed-ploidy population, call differences were not related to the geographic location of the population and they were not correlated with genetic distances in the R and L genomes.ConclusionsWe found an influence of all three tested factors on call parameters, with the effect size decreasing from genotype through breeding system to geographic location of the population. Overall, results were in line with predictions from a dosage effect in L/R ratios, but in three call parameters all three hybrid types were more similar to one or the other parental species. Also calls of diploid hybrids varied between breeding systems in agreement with the sexual host required for successful reproduction. The lack of hybrid call differences in a mixed-ploidy population at the northern edge of the water frog distribution is likely to be associated with genetic particularities, including a) low genetic variability and/or b) a local loss of genes coding for genotype-dependent call differentiation under conditions where female discrimination between diploid and triploid males is not beneficial.

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Dataset Information

Attention and Motivated Response to Simulated Male Advertisement Call Activates Forebrain Dopaminergic and Social Decision-Making Network Nuclei in Female Midshipman Fish.

Publications

Attention and Motivated Response to Simulated Male Advertisement Call Activates Forebrain Dopaminergic and Social Decision-Making Network Nuclei in Female Midshipman Fish.

Similar Datasets

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