Mechanisms, development, and comparative perspectives on experience‐dependent plasticity in social behavior

Sakata, Jon T.; Catalano, Isabella; Woolley, Sarah C.

doi:10.1002/jez.2539

Cited by 10 publications

(3 citation statements)

References 193 publications

(276 reference statements)

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“…In particular, while developmental sensory experiences and manipulations can have lasting effects on sensory organization, social experiences can lead to sensory learning and plasticity in adults even after the closure of developmental sensitive periods. In a number of species, mating can lead to learning and plasticity, especially in species in which mating induces the formation of pair bonds: selective, enduring, and often monogamous relationships [8][9][10][11]. Pair bonded individuals recognize and prefer their mate or their mate's signals (vocalizations, scent, etc) over unfamiliar individuals, indicating that there is plasticity and learning of sensory signals or representations of a mate in bonded animals [12][13][14][15].…”

Section: Introductionmentioning

confidence: 99%

Social experiences shape song preference learning independent of developmental exposure to song

Wall

Woolley

2023

Preprint

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Communication governs the formation and maintenance of social relationships. The interpretation of communication signals depends not only on the signal′s content, but also on a receiver′s individual experience. Experiences throughout life may interact to affect behavioral plasticity, such that a lack of developmental sensory exposure could constrain adult learning, while salient adult social experiences could remedy developmental deficits. We investigated how experiences impact the formation and direction of female auditory preferences in the zebra finch. Zebra finches form long-lasting pair bonds and females learn preferences for their mate′s vocalizations. We found that after two weeks of cohabitation with a male, females formed pair-bonds and learned to prefer their mate′s song regardless of whether they were reared with (normally-reared) or without (song-naïve) developmental exposure to song. In contrast, females that heard but did not physically interact with a male did not prefer his song. Moreover, even following mating, song-naïve females failed to show species-typical preferences for courtship song, hinting that mating is insufficient to ameliorate broader deficits in sensory processing that arise during development. Thus, courtship and mating interactions, but not acoustic-only interactions, strongly influence preference learning regardless of rearing experience, and may dynamically drive auditory plasticity for recognition and preference.

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Section: Introductionmentioning

confidence: 99%

Social experiences shape song preference learning independent of developmental exposure to song

Wall

Woolley

2023

Preprint

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“…The roles of mating and social experience in shaping male mating behaviors have been compared across species since the 1950’s 1 . Many similarities and differences exist among species in the effects of mating experiences on the motivational and performance aspects of mating behaviors 2 – 5 .…”

Section: Introductionmentioning

confidence: 99%

Mating experiences with the same partner enhanced mating activities of naïve male medaka fish

Daimon

Katsumura

Sakamoto

et al. 2022

Sci Rep

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Mating experience shapes male mating behavior across species, from insects, fish, and birds, to rodents. Here, we investigated the effect of multiple mating experiences on male mating behavior in “naïve” (defined as sexually inexperienced) male medaka fish. The latency to mate with the same female partner significantly decreased after the second encounter, whereas when the partner was changed, the latency to mate was not decreased. These findings suggest that mating experiences enhanced the mating activity of naïve males for the familiar female, but not for an unfamiliar female. In contrast, the mating experiences of “experienced” (defined as those having mated > 7 times) males with the same partner did not influence their latency to mate. Furthermore, we identified 10 highly and differentially expressed genes in the brains of the naïve males after the mating experience and revealed 3 genes that are required for a functional cascade of the thyroid hormone system. Together, these findings suggest that the mating experience of naïve male medaka fish influences their mating behaviors, with neural changes triggered by thyroid hormone activation in the brain.

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“…One reward-related behavior that develops during adolescence is social behavior (Andrews et al, 2021; Lamblin et al, 2017; Sakata et al, 2022; Vanderschuren & Trezza, 2014). In rodents, social behavior milestones during adolescence include a reduction in juvenile social play behavior and an increase in copulatory behavior, both of which need to occur for normal adult social behaviors to be achieved (Chu et al, 2021; Kopec et al, 2018).…”

mentioning

confidence: 99%

Morphine exposure during adolescence induces enduring social changes dependent on adolescent stage of exposure, sex, and social test.

King'uyu,

Edgar,

Figueroa

et al. 2024

Behavioral Neuroscience

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Drug exposure during adolescence, when the “reward” circuitry of the brain is developing, can permanently impact reward-related behavior into adulthood. Epidemiological studies show that opioid treatment during adolescence, such as pain management for a dental procedure or surgery, increases the incidence of psychiatric illness including substance use disorders. Moreover, the opioid epidemic currently in the United States is affecting younger individuals raising the impetus to understand the pathogenesis of the negative effects of opioids. One reward-related behavior that develops during adolescence is social behavior. We previously demonstrated that developmental changes in the nucleus accumbens reward region regulate social development in rats during sex-specific adolescent periods: early to mid-adolescence in males (postnatal day, P30–40) and preearly adolescence in females (P20–30). We thus hypothesized that the developmental stage of morphine exposure will differentially impact social behavior development such that drug administered during the female critical period would result in adult sociability deficits in females, but not males, and morphine administered during the male critical period would result in adult sociability deficits in males, but not females. We found that morphine exposure during the female critical period primarily resulted in deficits in sociability in females, while morphine exposure during the male critical period primarily resulted in deficits in sociability primarily in males. However, depending on the test performed and the social parameter measured, social alterations could be found in both sexes that received morphine exposure at either adolescent stage. These data indicate that when drug exposure occurs during adolescence, and how the endpoint data are measured, will play a large role in determining the effects of drug exposures on social development.

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Mechanisms, development, and comparative perspectives on experience‐dependent plasticity in social behavior

Cited by 10 publications

References 193 publications

Social experiences shape song preference learning independent of developmental exposure to song

Social experiences shape song preference learning independent of developmental exposure to song

Mating experiences with the same partner enhanced mating activities of naïve male medaka fish

Morphine exposure during adolescence induces enduring social changes dependent on adolescent stage of exposure, sex, and social test.

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