Behavioral indices of breeding readiness in female European starlings correlate with immunolabeling for catecholamine markers in brain areas involved in sexual motivation

Pawlisch, Benjamin A.; Kelm‐Nelson, Cynthia A.; Stevenson, Sharon A.; Riters, Lauren V.

doi:10.1016/j.ygcen.2012.09.007

Cited by 14 publications

(21 citation statements)

References 54 publications

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“…Dopamine in the nucleus accumbens (Ac) rises in female rats presented with a sexual partner, a finding that was interpreted to support the hypothesis that dopamine in Ac motivates a female to seek sexual contact [22]. Consistent with these studies, in female starlings we found that labeling for tyrosine hydroxylase (a rate limiting enzyme for dopamine synthesis) in the nucleus accumbens (Ac) correlated positively with nesting behavior (which we consider a reflection of the motivation to breed) [23]. …”

Section: Introductionsupporting

confidence: 74%

“…To promote breeding activities while avoiding the possibility that exposure to long daylengths would induce refractoriness we treated females with estradiol, which facilitates breeding behaviors in photosensitive females (e.g., [23]). Specifically, after the 6 weeks of exposure to 8h light (described above), each female received subcutaneous estradiol implants to facilitate breeding activities in captivity.…”

Section: Methodsmentioning

confidence: 99%

“…The same threshold was used within a brain region for each individual. Labeling was quantified in POM, VMH, a putative location for the avian Ac [49, 50], and additionally the periaqueductal gray (PAG) (locations identified as in [48] and [23]). The POM and VMH were selected based on studies in female rats showing opioids in these areas to reward mating activities [28].…”

Section: Methodsmentioning

confidence: 99%

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Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)

Riters

Ellis

Angyal

et al. 2013

Behavioural Brain Research

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Male courtship vocalizations represent a potent signal designed to attract females; however, not all females find male signals equally attractive. We explored the possibility that the affective state induced by hearing courtship vocalizations depends on the motivational state of a receiver. We used a conditioned place preference test of reward to determine the extent to which the rewarding properties of hearing male courtship song differed in female European starlings categorized as nest box owners (a sign of breeding readiness) or non-owners. Nest box owners developed a preference for a chamber in which they previously heard male courtship song. Non-owners displayed no preference for a chamber in which they previously heard song. Positive correlations were identified between the preference a female developed for the song-paired chamber and female nesting and dominance behaviors observed prior to conditioning (indices of the motivation to breed). Immunolabeling for met-enkephalin (an opioid neuropeptide involved in reward) in the medial preoptic nucleus, ventromedial nucleus of the hypothalamus, nucleus accumbens, and periaqueductal gray was higher in females with compared to those without nest boxes. Both nest box entries and song-induced place preference also correlated positively with met-enkephalin labeling in the ventromedial nucleus of the hypothalamus. These findings indicate that the reward value of vocal signals is linked to individual differences in motivational state; and that differences in enkephalin activity may play a role in modifying an individual’s motivational state and/or the reward value of song.

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Section: Introductionsupporting

confidence: 74%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)

Riters

Ellis

Angyal

et al. 2013

Behavioural Brain Research

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“…The immunogen for the rabbit polyclonal anti‐DBH antibody was purified DBH from bovine adrenal medulla and recognizes a triplet of 72–74 kDa in rat brain extract on western blot (manufacturer's information). This antibody has been previously used to identify noradrenergic neurons and fibers in the brains of rodents (Bullman, Hartig, Holzer, & Arendt, ; Tsuneoka et al 2013), birds (Castelino & Ball, ; Pawlisch, Kelm‐Nelson, Stevenson, & Riters, ), and in the peripheral nervous system of turtle (Belfry & Cowan, ) and hachetfish (Zaccone et al, 2011). In the present study, in midshipman, this DBH antibody labels neurons with a position and morphology in the locus coeruleus (LC) that is consistent with LC noradrenergic (NA) neurons found in all vertebrates examined to date (Smeets & González, ).…”

Section: Methodsmentioning

confidence: 99%

Connectivity and ultrastructure of dopaminergic innervation of the inner ear and auditory efferent system of a vocal fish

Perelmuter

Forlano

2017

J of Comparative Neurology

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Dopamine (DA) is a conserved modulator of vertebrate neural circuitry, yet our knowledge of its role in peripheral auditory processing is limited to mammals. The present study combines immunohistochemistry, neural tract tracing, and electron microscopy to investigate the origin and synaptic characteristics of DA fibers innervating the inner ear and the hindbrain auditory efferent nucleus in the plainfin midshipman, a vocal fish that relies upon the detection of mate calls for reproductive success. We identify a DA cell group in the diencephalon as a common source for innervation of both the hindbrain auditory efferent nucleus and saccule, the main hearing endorgan of the inner ear. We show that DA terminals in the saccule contain vesicles but transmitter release appears paracrine in nature, due to the apparent lack of synaptic contacts. In contrast, in the hindbrain, DA terminals form traditional synaptic contacts with auditory efferent neuronal cell bodies and dendrites, as well as unlabeled axon terminals, which, in turn, form inhibitory-like synapses on auditory efferent somata. Our results suggest a distinct functional role for brain-derived DA in the direct and indirect modulation of the peripheral auditory system of a vocal nonmammalian vertebrate.

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“…These areas are involved in motivational processes for affiliative behavior and other natural rewards (Kelley and Berridge, 2002; Stuber et al, 2008). Further, a critical role of dopaminergic systems in courtship and pair formation has been demonstrated in mammals (Aragona et al, 2006) and suggested in birds (Goodson et al, 2009; Alger et al, 2011; Pawlisch et al, 2012; Banerjee et al, 2013; Iyilikci et al, 2014). In songbirds, both dopaminergic and non-dopaminergic neurons in VTA are selectively active when male zebra finches sing to court females but not when they sing in a non-courtship context (Yanagihara and Hessler, 2006; Hara et al, 2007; Huang and Hessler, 2008).…”

Section: Introductionmentioning

confidence: 96%

Sexually dimorphic activation of dopaminergic areas depends on affiliation during courtship and pair formation

Iwasaki

Poulsen

Oka

et al. 2014

Front. Behav. Neurosci.

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For many species, dyadic interaction during courtship and pair bonding engage intense emotional states that control approach or avoidance behavior. Previous studies have shown that one component of a common social brain network (SBN), dopaminergic areas, are highly engaged during male songbird courtship of females. We tested whether the level of activity in dopaminergic systems of both females and males during courtship is related to their level of affiliation. In order to objectively quantify affiliative behaviors, we developed a system for tracking the position of both birds during free interaction sessions. During a third successive daily interaction session, there was a range of levels of affiliation among bird pairs, as quantified by several position and movement parameters. Because both positive and negative social interactions were present, we chose to characterize affiliation strength by pair valence. As a potential neural system involved in regulating pair valence, the level of activity of the dopaminergic group A11 (within the central gray) was selectively reduced in females of positive valence pairs. Further, activation of non-dopaminergic neurons in VTA was negatively related to valence, with this relationship strongest in ventral VTA of females. Together, these results suggest that inhibition of fear or avoidance networks may be associated with development of close affiliation, and highlight the importance of negative as well as positive emotional states in the process of courtship, and in development of long-lasting social bonds.

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Behavioral indices of breeding readiness in female European starlings correlate with immunolabeling for catecholamine markers in brain areas involved in sexual motivation

Cited by 14 publications

References 54 publications

Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)

Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)

Connectivity and ultrastructure of dopaminergic innervation of the inner ear and auditory efferent system of a vocal fish

Sexually dimorphic activation of dopaminergic areas depends on affiliation during courtship and pair formation

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