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Article ; Online: The medial preoptic area and its projections to the ventral tegmental area and the periaqueductal gray are activated in response to social play behavior in juvenile rats.

Zhao, Changjiu / Riters, Lauren V

2023 Volume 137, Issue 4, Page(s) 223–235

Abstract: The medial preoptic area (MPOA) is well known for its role in sexual and maternal behaviors. This region also plays an important role in affiliative social behaviors outside reproductive contexts. We recently demonstrated that the MPOA is a central ... ...

Abstract	The medial preoptic area (MPOA) is well known for its role in sexual and maternal behaviors. This region also plays an important role in affiliative social behaviors outside reproductive contexts. We recently demonstrated that the MPOA is a central nucleus in which opioids govern highly rewarding social play behavior in adolescent rats. However, the neural circuit mechanisms underlying MPOA-mediated social play remain largely unresolved. We hypothesized that the MPOA unites a complementary neural system through which social play induces reward via a projection to the ventral tegmental area (VTA) and reduces a negative affective state through a projection to the periaqueductal gray (PAG). To test whether the two projection pathways are activated in response to social play behavior, we combined retrograde tract tracing with immediate early gene (IEG) expression and immunofluorescent labeling to identify opioid-sensitive projection pathways from the MPOA to VTA and PAG that are activated after performance of social play. Retrograde tracer, fluoro-gold (FG), was microinjected into the VTA or PAG. IEG expression (i.e., Egr1) was assessed and triple immunofluorescent labeling for mu opioid receptor (MOR), Egr1, and FG in the MPOA was performed after social play. We revealed that play animals displayed an increase in neurons double labeled for Egr1 + FG and triple labeled for MOR + Egr1 + FG in the MPOA projecting to both the VTA and PAG when compared to no-play rats. The increased activation of projection neurons that express MORs from MPOA to VTA or PAG after social play suggests that opioids may act through these projection pathways to govern social play. (PsycInfo Database Record (c) 2023 APA, all rights reserved).
MeSH term(s)	Female ; Rats ; Animals ; Preoptic Area/physiology ; Periaqueductal Gray ; Neural Pathways/physiology ; Ventral Tegmental Area ; Analgesics, Opioid
Chemical Substances	Analgesics, Opioid
Language	English
Publishing date	2023-03-06
Publishing country	United States
Document type	Journal Article
ZDB-ID	230159-3
ISSN	1939-0084 ; 0735-7044
ISSN (online)	1939-0084
ISSN	0735-7044
DOI	10.1037/bne0000555
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Article ; Online: Using seasonality and birdsong to understand mechanisms underlying context-appropriate shifts in social motivation and reward.

Riters, Lauren V / Stevenson, Sharon A

Hormones and behavior

2022 Volume 142, Page(s) 105156

Abstract: Social motivation and reward are dynamic and flexible, shifting adaptively across contexts to meet changing social demands. This is exceptionally apparent when seasonal contexts are considered in seasonally breeding songbirds as they cycle from periods ... ...

Abstract	Social motivation and reward are dynamic and flexible, shifting adaptively across contexts to meet changing social demands. This is exceptionally apparent when seasonal contexts are considered in seasonally breeding songbirds as they cycle from periods of sexual motivation and reward during the breeding season to periods of extreme gregariousness outside the breeding season when non-sexual social interactions gain reward value, motivating birds to form flocks. Here we review evidence demonstrating a key integrative role for the medial preoptic area (mPOA) in the seasonally-appropriate adjustment of behaviors, with seasonal changes in dopamine activity in mPOA adjusting social motivation and changes in opioid activity modifying social reward. Experiments demonstrate that dramatic seasonal fluctuations in steroid hormone concentrations alter patterns of opioid- and dopamine-related protein and gene expression in mPOA to modify social motivation and reward to meet seasonal changes in social demands. These studies of birdsong and seasonality provide new insights into neural and endocrine mechanisms underlying adaptive changes in social motivation and reward and highlight an underappreciated, evolutionarily conserved role for the mPOA in important social behaviors in non-reproductive contexts.
MeSH term(s)	Analgesics, Opioid ; Animals ; Dopamine ; Motivation ; Preoptic Area ; Reward ; Sexual Behavior, Animal ; Starlings ; Vocalization, Animal
Chemical Substances	Analgesics, Opioid ; Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2022-03-18
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural
ZDB-ID	214409-8
ISSN	1095-6867 ; 0018-506X
ISSN (online)	1095-6867
ISSN	0018-506X
DOI	10.1016/j.yhbeh.2022.105156
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Article ; Online: Distinct patterns of gene expression in the medial preoptic area are related to gregarious singing behavior in European starlings (Sturnus vulgaris).

Polzin, Brandon J / Stevenson, Sharon A / Gammie, Stephen C / Riters, Lauren V

BMC neuroscience

2023 Volume 24, Issue 1, Page(s) 41

Abstract: Background: Song performed in flocks by European starlings (Sturnus vulgaris), referred to here as gregarious song, is a non-sexual, social behavior performed by adult birds. Gregarious song is thought to be an intrinsically reinforced behavior ... ...

Abstract	Background: Song performed in flocks by European starlings (Sturnus vulgaris), referred to here as gregarious song, is a non-sexual, social behavior performed by adult birds. Gregarious song is thought to be an intrinsically reinforced behavior facilitated by a low-stress, positive affective state that increases social cohesion within a flock. The medial preoptic area (mPOA) is a region known to have a role in the production of gregarious song. However, the neurochemical systems that potentially act within this region to regulate song remain largely unexplored. In this study, we used RNA sequencing to characterize patterns of gene expression in the mPOA of male and female starlings singing gregarious song to identify possibly novel neurotransmitter, neuromodulator, and hormonal pathways that may be involved in the production of gregarious song. Results: Differential gene expression analysis and rank rank hypergeometric analysis indicated that dopaminergic, cholinergic, and GABAergic systems were associated with the production of gregarious song, with multiple receptor genes (e.g., DRD2, DRD5, CHRM4, GABRD) upregulated in the mPOA of starlings who sang at high rates. Additionally, co-expression network analyses identified co-expressing gene clusters of glutamate signaling-related genes associated with song. One of these clusters contained five glutamate receptor genes and two glutamate scaffolding genes and was significantly enriched for genetic pathways involved in neurodevelopmental disorders associated with social deficits in humans. Two of these genes, GRIN1 and SHANK2, were positively correlated with performance of gregarious song. Conclusions: This work provides new insights into the role of the mPOA in non-sexual, gregarious song in starlings and highlights candidate genes that may play a role in gregarious social interactions across vertebrates. The provided data will also allow other researchers to compare across species to identify conserved systems that regulate social behavior.
MeSH term(s)	Animals ; Humans ; Male ; Female ; Starlings/metabolism ; Vocalization, Animal/physiology ; Singing ; Preoptic Area/metabolism ; Gene Expression
Language	English
Publishing date	2023-08-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2041344-0
ISSN	1471-2202 ; 1471-2202
ISSN (online)	1471-2202
ISSN	1471-2202
DOI	10.1186/s12868-023-00813-4
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Article ; Online: Conditioned preferences: Gated by experience, context, and endocrine systems.

Monari, Patrick K / Hammond, Emma R / Zhao, Xin / Maksimoski, Alyse N / Petric, Radmila / Malone, Candice L / Riters, Lauren V / Marler, Catherine A

Hormones and behavior

2024 Volume 161, Page(s) 105529

Abstract: Central to the navigation of an ever-changing environment is the ability to form positive associations with places and conspecifics. The functions of location and social conditioned preferences are often studied independently, limiting our understanding ... ...

Abstract	Central to the navigation of an ever-changing environment is the ability to form positive associations with places and conspecifics. The functions of location and social conditioned preferences are often studied independently, limiting our understanding of their interplay. Furthermore, a de-emphasis on natural functions of conditioned preferences has led to neurobiological interpretations separated from ecological context. By adopting a naturalistic and ethological perspective, we uncover complexities underlying the expression of conditioned preferences. Development of conditioned preferences is a combination of motivation, reward, associative learning, and context, including for social and spatial environments. Both social- and location-dependent reward-responsive behaviors and their conditioning rely on internal state-gating mechanisms that include neuroendocrine and hormone systems such as opioids, dopamine, testosterone, estradiol, and oxytocin. Such reinforced behavior emerges from mechanisms integrating past experience and current social and environmental conditions. Moreover, social context, environmental stimuli, and internal state gate and modulate motivation and learning via associative reward, shaping the conditioning process. We highlight research incorporating these concepts, focusing on the integration of social neuroendocrine mechanisms and behavioral conditioning. We explore three paradigms: 1) conditioned place preference, 2) conditioned social preference, and 3) social conditioned place preference. We highlight nonclassical species to emphasize the naturalistic applications of these conditioned preferences. To fully appreciate the complex integration of spatial and social information, future research must identify neural networks where endocrine systems exert influence on such behaviors. Such research promises to provide valuable insights into conditioned preferences within a broader naturalistic context.
Language	English
Publishing date	2024-03-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	214409-8
ISSN	1095-6867 ; 0018-506X
ISSN (online)	1095-6867
ISSN	0018-506X
DOI	10.1016/j.yhbeh.2024.105529
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Article ; Online: Immunolabeling Provides Evidence for Subregions in the Songbird Nucleus Accumbens and Suggests a Context-Dependent Role in Song in Male European Starlings (Sturnus vulgaris).

Polzin, Brandon J / Heimovics, Sarah A / Riters, Lauren V

Brain, behavior and evolution

2021 Volume 96, Issue 3, Page(s) 147–162

Abstract: Birdsong is well known for its role in mate attraction during the breeding season. However, many birds, including European starlings (Sturnus vulgaris), also sing outside the breeding season as part of large flocks. Song in a breeding context can be ... ...

Abstract	Birdsong is well known for its role in mate attraction during the breeding season. However, many birds, including European starlings (Sturnus vulgaris), also sing outside the breeding season as part of large flocks. Song in a breeding context can be extrinsically rewarded by mate attraction; however, song in nonbreeding flocks, referred to here as gregarious song, results in no obvious extrinsic reward and is proposed to be intrinsically rewarded. The nucleus accumbens (NAC) is a brain region well known to mediate reward and motivation, which suggests it is an ideal candidate to regulate reward associated with gregarious song. The goal of this study was to provide new histochemical information on the songbird NAC and its subregions (rostral pole, core, and shell) and to begin to determine subregion-specific contributions to gregarious song in male starlings. We examined immunolabeling for tyrosine hydroxylase (TH), neurotensin, and enkephalin (ENK) in the NAC. We then examined the extent to which gregarious and sexually motivated song differentially correlated with immunolabeling for the immediate early genes FOS and ZENK in each subdivision of the NAC. We found that TH and ENK labeling within subregions of the starling NAC was generally similar to patterns seen in the core and shell of NACs in mammals and birds. Additionally, we found that gregarious song, but not sexually motivated song, positively correlated with FOS in all NAC subregions. Our observations provide further evidence for distinct subregions within the songbird NAC and suggest the NAC may play an important role in regulating gregarious song in songbirds.
MeSH term(s)	Animals ; Brain ; Male ; Mammals ; Motivation ; Nucleus Accumbens ; Starlings ; Tyrosine 3-Monooxygenase ; Vocalization, Animal/physiology
Chemical Substances	Tyrosine 3-Monooxygenase (EC 1.14.16.2)
Language	English
Publishing date	2021-12-08
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1199-x
ISSN	1421-9743 ; 0006-8977
ISSN (online)	1421-9743
ISSN	0006-8977
DOI	10.1159/000521310
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Article: Mu opioid receptor stimulation in the medial preoptic area or nucleus accumbens facilitates song and reward in flocking European starlings.

Polzin, Brandon J / Maksimoski, Alyse N / Stevenson, Sharon A / Zhao, Changjiu / Riters, Lauren V

Frontiers in physiology

2022 Volume 13, Page(s) 970920

Abstract: It has been proposed that social cohesion in gregarious animals is reinforced both by a positive affective state induced by social interactions and by the prevention of a negative state that would be caused by social separation. Opioids that bind to mu ... ...

Abstract	It has been proposed that social cohesion in gregarious animals is reinforced both by a positive affective state induced by social interactions and by the prevention of a negative state that would be caused by social separation. Opioids that bind to mu opioid receptors (MORs) act in numerous brain regions to induce positive and to reduce negative affective states. Here we explored a potential role for MORs in affective states that may impact flocking behavior in mixed-sex flocks of nonbreeding European starlings,
Language	English
Publishing date	2022-09-12
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2022.970920
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Article: Birdsong and the Neural Regulation of Positive Emotion.

Riters, Lauren V / Polzin, Brandon J / Maksimoski, Alyse N / Stevenson, Sharon A / Alger, Sarah J

Frontiers in psychology

2022 Volume 13, Page(s) 903857

Abstract: Birds are not commonly admired for emotional expression, and when they are, the focus is typically on negative states; yet vocal behavior is considered a direct reflection of an individual's emotional state. Given that over 4000 species of songbird ... ...

Abstract	Birds are not commonly admired for emotional expression, and when they are, the focus is typically on negative states; yet vocal behavior is considered a direct reflection of an individual's emotional state. Given that over 4000 species of songbird produce learned, complex, context-specific vocalizations, we make the case that songbirds are conspicuously broadcasting distinct positive emotional states and that hearing songs can also induce positive states in other birds. Studies are reviewed that demonstrate that that the production of sexually motivated song reflects an emotional state of anticipatory reward-seeking (i.e., mate-seeking), while outside the mating context song in gregarious flocks reflects a state of intrinsic reward. Studies are also reviewed that demonstrate that hearing song induces states of positive anticipation and reward. This review brings together numerous studies that highlight a potentially important role for the songbird nucleus accumbens, a region nearly synonymous with reward in mammals, in positive emotional states that underlie singing behavior and responses to song. It is proposed that the nucleus accumbens is part of an evolutionarily conserved circuitry that contributes context-dependently to positive emotional states that motivate and reward singing behavior and responses to song. Neural mechanisms that underlie basic emotions appear to be conserved and similar across vertebrates. Thus, these findings in songbirds have the potential to provide insights into interventions that can restore positive social interactions disrupted by mental health disorders in humans.
Language	English
Publishing date	2022-06-22
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2563826-9
ISSN	1664-1078
ISSN	1664-1078
DOI	10.3389/fpsyg.2022.903857
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Article ; Online: The motivation to flock correlates with vocal-social behaviors and dopamine-related gene expression in male European starlings.

Maksimoski, Alyse N / Stevenson, Sharon A / Polzin, Brandon J / Zhao, Changjiu / Luebke, Elsa M / Riters, Lauren V

Hormones and behavior

2023 Volume 153, Page(s) 105374

Abstract: It is proposed that songbird flocks are partly reinforced by positive social interactions, however not all flock mate interactions are positive. The combination of both positive and negative social interactions with flock mates may play a role in the ... ...

Abstract	It is proposed that songbird flocks are partly reinforced by positive social interactions, however not all flock mate interactions are positive. The combination of both positive and negative social interactions with flock mates may play a role in the motivation for birds to flock. The nucleus accumbens (NAc), medial preoptic area (POM), and ventral tegmental area (VTA) are implicated in vocal-social behaviors in flocks, including singing. Dopamine (DA) within these regions modifies motivated, reward-directed behaviors. Here, we begin to test the hypothesis that individual social interactions and DA within these regions are involved in the motivation to flock. Vocal-social behaviors were recorded in eighteen male European starlings in mixed-sex flocks in fall, when starlings are highly social and form large flocks. Males were then singly removed from their flock and the motivation to flock was quantified as the amount of time spent attempting to join a flock following separation. We used quantitative real-time polymerase chain reaction to measure expression of DA-related genes in the NAc, POM, and VTA. Birds producing high levels of vocal behaviors were more highly motivated to flock and had higher tyrosine hydroxylase (the rate-limiting enzyme in DA synthesis) expression in the NAc and VTA. Birds that received high levels of agonistic behaviors were less motivated to flock and had higher DA receptor subtype 1 expression in the POM. Overall, our findings suggest that interplay between social experience and DA activity in NAc, POM, and VTA plays a key role in social motivation in flocking songbirds.
MeSH term(s)	Animals ; Male ; Motivation ; Starlings/metabolism ; Dopamine/metabolism ; Vocalization, Animal ; Sexual Behavior, Animal ; Social Behavior ; Ventral Tegmental Area/metabolism ; Gene Expression
Chemical Substances	Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2023-06-02
Publishing country	United States
Document type	Journal Article
ZDB-ID	214409-8
ISSN	1095-6867 ; 0018-506X
ISSN (online)	1095-6867
ISSN	0018-506X
DOI	10.1016/j.yhbeh.2023.105374
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Article ; Online: Distinct patterns of activity within columns of the periaqueductal gray are associated with functionally distinct birdsongs.

Asogwa, Chinweike N / Zhao, Changjiu / Polzin, Brandon J / Maksimoski, Alyse N / Heimovics, Sarah A / Riters, Lauren V

Annals of the New York Academy of Sciences

2023 Volume 1530, Issue 1, Page(s) 161–181

Abstract: Male songbirds produce female-directed songs in spring that convey a state of sexual motivation. Many songbirds also sing in fall flocks in affiliative/gregarious contexts in which song is linked to an intrinsic positive affective state. The ... ...

Abstract	Male songbirds produce female-directed songs in spring that convey a state of sexual motivation. Many songbirds also sing in fall flocks in affiliative/gregarious contexts in which song is linked to an intrinsic positive affective state. The periaqueductal gray (PAG) in mammals, which is organized into functional columns, integrates information from multiple brain regions and relays this information to vocal motor areas so that an animal emits a vocal signal reflective of its affective state. Here, we test the hypothesis that distinct columns in the songbird PAG play roles in the distinct affective states communicated by sexually motivated and gregarious song. We quantified the numbers of immediate early gene ZENK-positive cells in 16 PAG subregions in male European starlings (Sturnus vulgaris) after singing gregarious or sexually motivated song. Results suggest that distinct PAG columns in songbirds context-specifically regulate song, agonistic, and courtship behaviors. A second exploratory, functional tract-tracing study also demonstrated that inputs to the PAG from specific subregions of the medial preoptic nucleus may contribute to gregarious song and behaviors indicative of social dominance. Together, findings suggest that conserved PAG columns and inputs from the preoptic nucleus may play a role in context-specific vocal and other social behaviors.
MeSH term(s)	Animals ; Male ; Female ; Periaqueductal Gray/physiology ; Sexual Behavior, Animal/physiology ; Vocalization, Animal/physiology ; Brain/physiology ; Motivation ; Starlings/physiology ; Mammals
Language	English
Publishing date	2023-10-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	211003-9
ISSN	1749-6632 ; 0077-8923
ISSN (online)	1749-6632
ISSN	0077-8923
DOI	10.1111/nyas.15066
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Article ; Online: Behavioral convergence in defense behaviors in pair bonded individuals correlates with neuroendocrine receptors in the medial amygdala.

Malone, Candice L / Rieger, Nathaniel S / Spool, Jeremy A / Payette, Alexis / Riters, Lauren V / Marler, Catherine A

Behavioural brain research

2023 Volume 452, Page(s) 114556

Abstract: Monogamous, pair-bonded animals coordinate intra-pair behavior for spatially separated challenges including territorial defense and nest attendance. Paired California mice, a monogamous, territorial and biparental species, approach intruders together or ... ...

Abstract	Monogamous, pair-bonded animals coordinate intra-pair behavior for spatially separated challenges including territorial defense and nest attendance. Paired California mice, a monogamous, territorial and biparental species, approach intruders together or separately, but often express behavioral convergence across intruder challenges. To gain a more systems-wide perspective of potential mechanisms contributing to behavioral convergence across two conspecific intruder challenges, we conducted an exploratory study correlating behavior and receptor mRNA (Days 10 and 17 post-pairing). We examined associations between convergence variability in pair time for intruder-oriented behaviors with a pair mRNA index for oxytocin (OXTR), androgen (AR), and estrogen alpha (ERα) receptors within the medial amygdala (MeA) and the anterior olfactory nucleus (AON), brain regions associated with social behavior. An intruder behavior index revealed a bimodal distribution of intruder-related behaviors in Challenge 1 and a unimodal distribution in Challenge 2, suggesting population behavioral convergence, but no significant correlations with neuroendocrine measures. However, OXTR, AR, and ERα mRNA in the MeA were positively associated with convergence in individual intruder-related behaviors, suggesting multiple mechanisms may influence convergence. Mice could also occupy the nest during intruder challenges and convergence in nest attendance was positively correlated with MeA OXTR. At an individual level, nest attendance was positively associated with MeA ERα. Vocalizations were positively associated with AR and ERα mRNA. No positive associations were found in the AON. Overall, neuroendocrine receptors were implicated in convergence of a monogamous pair's defense behavior, highlighting the potential importance of the MeA as part of a circuit underlying convergence.
MeSH term(s)	Animals ; Estrogen Receptor alpha/metabolism ; Social Behavior ; Corticomedial Nuclear Complex/metabolism ; Oxytocin ; RNA, Messenger ; Receptors, Oxytocin/genetics
Chemical Substances	Estrogen Receptor alpha ; Oxytocin (50-56-6) ; RNA, Messenger ; Receptors, Oxytocin
Language	English
Publishing date	2023-06-24
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	449927-x
ISSN	1872-7549 ; 0166-4328
ISSN (online)	1872-7549
ISSN	0166-4328
DOI	10.1016/j.bbr.2023.114556
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