Neural and Hormonal Control of Sexual Behavior

Abstract Gonadal hormones contribute to the sexual differentiation of brain and behavior throughout the lifespan, from initial neural patterning to “activation” of adult circuits. Sexual behavior is an ideal system in which to investigate the mechanisms underlying hormonal activation of neural circuits. Sexual behavior is a hormonally regulated, innate social behavior found across species. Although both sexes seek out and engage in sexual behavior, the specific actions involved in mating are sexually dimorphic. Thus, the neural circuits mediating sexual motivation and behavior in males and females are overlapping yet distinct. Furthermore, sexual behavior is strongly dependent on circulating gonadal hormones in both sexes. There has been significant recent progress on elucidating how gonadal hormones modulate physiological properties within sexual behavior circuits with consequences for behavior. Therefore, in this mini-review we review the neural circuits of male and female sexual motivation and behavior, from initial sensory detection of pheromones to the extended amygdala and on to medial hypothalamic nuclei and reward systems. We also discuss how gonadal hormones impact the physiology and functioning of each node within these circuits. By better understanding the myriad of ways in which gonadal hormones impact sexual behavior circuits, we can gain a richer and more complete appreciation for the neural substrates of complex behavior.

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Hormonal control of motivational circuitry orchestrates the transition to sexuality in Drosophila

10.1101/852335 ◽

2019 ◽

Author(s):

Stephen X. Zhang ◽

Ethan H. Glantz ◽

Dragana Rogulja ◽

Michael A. Crickmore

Keyword(s):

Sexual Behavior ◽

Juvenile Hormone ◽

Sexual Activity ◽

Sexual Motivation ◽

Hormonal Control ◽

Complete Suppression ◽

Hormonal Changes ◽

Inhibitory Mechanisms ◽

Circuit Elements ◽

And Behavior

SUMMARYNewborns and hatchlings of many species perform incredibly sophisticated behaviors, but all vertebrates and many invertebrates selectively abstain from sexual activity at the beginning of life. Hormonal changes have long been associated with adolescence, but it is not clear how these circulating factors create a new motivation and drive its associated behaviors. We show that the transition to sexuality in male Drosophila is controlled by juvenile hormone, which spikes at eclosion and declines over days as the propensity for courtship gradually increases. Juvenile hormone directly inhibits the activity of at least three courtship-motivating circuit elements, ensuring the complete suppression of sexual motivation and behavior. Blocking or overriding these inhibitory mechanisms evokes immediate and robust sexual behavior from very young and otherwise asexual males. These results provide a first example of hormonal changes gating the transition to sexuality by activating latent, but largely developed and functional, motivational circuitry.

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Oxytocin and Vasopressin: Mechanisms for Potential Sex Differences Observed in Autism Spectrum Disorders

10.1093/med/9780199744312.003.0018 ◽

2013 ◽

Author(s):

C. Sue Carter ◽

Suma Jacob

Keyword(s):

Autism Spectrum Disorders ◽

Arginine Vasopressin ◽

Protective Factor ◽

Brain Regions ◽

Autism Spectrum ◽

Sexually Dimorphic ◽

Unique Role ◽

Spectrum Disorders ◽

Brain And Behavior ◽

And Behavior

The effects of oxytocin and vasopressin on the brain and behavior can be sexually dimorphic, especially during the course of development (Bales, Kim, et al., 2004; Bales, Pfeifer, et al., 2004; Bales, Plotsky, et al., 2007; Bielsky et al., 2005a; Carter, 2003; Thompson et al., 2006; Yamamoto et al., 2005; Yamamoto et al., 2004). Given the sexual discrepancy observed in autism spectrum disorders (ASDs), these two neuropeptides, oxytocin (OT) and arginine vasopressin (AVP), have received attention for their potential role in ASDs (Green and Hollander, 2010; Insel et al., 1999; Leckman & Herman, 2002; Welch et al., 2005; Winslow, 2005; Young et al., 2002). Changes in either OT or AVP and their receptors could be capable of influencing symptom domains or behaviors associated with ASDs. Arginine vasopressin is androgen dependent in some brain regions (De Vries & Panzica, 2006), and males are more sensitive to AVP, especially during development. We hypothesize here that AVP, which has a unique role in males, must be present in optimal levels to be protective against ASDs. Either excess AVP or disruptions in the AVP system could play a role in development of the traits found in ASDs. In contrast, OT may possibly be secreted in response to adversity, especially in females, serving as a protective factor.

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Role of Puberty on Adult Behaviors

Oxford Research Encyclopedia of Neuroscience ◽

10.1093/acrefore/9780190264086.013.248 ◽

2020 ◽

Author(s):

Kristen Delevich ◽

Linda Wilbrecht

Keyword(s):

Transition To Adulthood ◽

Gonadal Hormones ◽

Gonadal Hormone ◽

Hormone Production ◽

Early 21St Century ◽

Adult Behavior ◽

Organizational Effects ◽

Brain And Behavior ◽

And Behavior ◽

The Brain

Puberty onset marks the beginning of adolescence and an organism’s transition to adulthood. Across species, adolescence is a dynamic period of maturation for brain and behavior. Pubertal processes, including the increase in gonadal hormone production, or gonadarche, can influence a broad array of neural processes and circuits to ultimately shape adult behavior. Decades of research in rodent models have shown that gonadal hormones at puberty promote adult-typical patterns of behavior across social, affective, and cognitive realms. Importantly, hormonal activation of sex-specific patterns of adult behavior relies on sexual differentiation of the brain around the time of birth, mediated by testicular hormones in males – and lack thereof in females. While it was originally believed that gonadal hormones play a purely activational role at puberty, studies in the early 21st century provide examples where the timing and relative levels of gonadal hormones exert long-lasting, or organizational effects on brain and behavior. In this way, adolescent exposure to gonadal hormones can orchestrate brain and body changes in unison and in some cases tune how the brain responds to gonadal hormones in adulthood. Notably, many of the effects of puberty on behavior may occur indirectly by altering sensitivity to environmental events and an organism’s ability to respond to or learn from experience. These insights from the animal literature provide a framework for understanding how puberty may influence the maturation of complex behaviors and modify risk or resilience to mental health disorders during human adolescence. In sum, puberty interacts with genetics, early life organizational effects of gonadal hormones, experience, and learning processes to shape behavior in adulthood.

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Addiction: Taking the brain seriously

Behavioral and Brain Sciences ◽

10.1017/s0140525x00043090 ◽

1996 ◽

Vol 19 (4) ◽

pp. 582-582

Author(s):

Steven E. Hyman

Keyword(s):

Neural Circuits ◽

Behavioral Analysis ◽

Interacting Agents ◽

Target Article ◽

Brain And Behavior ◽

And Behavior ◽

The Brain

AbstractHeyman's target article is an analytical tour de force, but it makes too hard a distinction between voluntary and driven behavior. It is more fruitful to think about brain and behavior as shifting, interacting “agents,” represented by multiple neural circuits. This has the virtue of better connecting behavioral analysis with wet neuroscience.

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Differential responsiveness in brain and behavior to sexually dimorphic long calls in male and female zebra finches

The Journal of Comparative Neurology ◽

10.1002/cne.22113 ◽

2009 ◽

Vol 516 (4) ◽

pp. 312-320 ◽

Cited By ~ 34

Author(s):

Sharon M.H. Gobes ◽

Sita M. ter Haar ◽

Clémentine Vignal ◽

Amélie L. Vergne ◽

Nicolas Mathevon ◽

...

Keyword(s):

Sexually Dimorphic ◽

Zebra Finches ◽

Male And Female ◽

Brain And Behavior ◽

Differential Responsiveness ◽

And Behavior ◽

Long Calls

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Gonadal Hormones Organize the Adolescent Brain and Behavior

Brain Crosstalk in Puberty and Adolescence - Research and Perspectives in Endocrine Interactions ◽

10.1007/978-3-319-09168-6_2 ◽

2014 ◽

pp. 15-27

Author(s):

Cheryl L. Sisk

Keyword(s):

Gonadal Hormones ◽

Brain And Behavior ◽

And Behavior

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Oxytocin, sexually-dimorphic social brain and behavior, and autism

Neuropsychiatrie de l Enfance et de l Adolescence ◽

10.1016/j.neurenf.2012.05.256 ◽

2012 ◽

Vol 60 (5) ◽

pp. S66

Author(s):

H. Yamasue

Keyword(s):

Sexually Dimorphic ◽

Social Brain ◽

Brain And Behavior ◽

And Behavior

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Sensitive Periods in the Development of the Brain and Behavior

Journal of Cognitive Neuroscience ◽

10.1162/0898929042304796 ◽

2004 ◽

Vol 16 (8) ◽

pp. 1412-1425 ◽

Cited By ~ 695

Author(s):

Eric I. Knudsen

Keyword(s):

Neural Circuits ◽

Neural Circuit ◽

Critical Role ◽

Sensitive Period ◽

Critical Periods ◽

Sensitive Periods ◽

Brain And Behavior ◽

The Individual ◽

And Behavior ◽

The Brain

Experience exerts a profound influence on the brain and, therefore, on behavior. When the effect of experience on the brain is particularly strong during a limited period in development, this period is referred to as a sensitive period. Such periods allow experience to instruct neural circuits to process or represent information in a way that is adaptive for the individual. When experience provides information that is essential for normal development and alters performance permanently, such sensitive periods are referred to as critical periods. Although sensitive periods are reflected in behavior, they are actually a property of neural circuits. Mechanisms of plasticity at the circuit level are discussed that have been shown to operate during sensitive periods. A hypothesis is proposed that experience during a sensitive period modifies the architecture of a circuit in fundamental ways, causing certain patterns of connectivity to become highly stable and, therefore, energetically preferred. Plasticity that occurs beyond the end of a sensitive period, which is substantial in many circuits, alters connectivity patterns within the architectural constraints established during the sensitive period. Preferences in a circuit that result from experience during sensitive periods are illustrated graphically as changes in a “stability landscape,” a metaphor that represents the relative contributions of genetic and experiential influences in shaping the information processing capabilities of a neural circuit. By understanding sensitive periods at the circuit level, as well as understanding the relationship between circuit properties and behavior, we gain a deeper insight into the critical role that experience plays in shaping the development of the brain and behavior.

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Puberty, Hormones, and the Social Brain

Coming of Age ◽

10.1093/oso/9780195314373.003.0006 ◽

2019 ◽

pp. 69-95

Author(s):

Cheryl L. Sisk ◽

Russell D. Romeo

Keyword(s):

Social Cognition ◽

Sensory Information ◽

Social Behaviors ◽

Gonadal Hormones ◽

Sensitive Period ◽

The Social ◽

History Of ◽

Brain And Behavior ◽

And Behavior ◽

The Brain

This chapter begins with some history of the field of behavioral neuroendocrinology and traces the origins of the classic organizational-activational hypothesis to explain sexual differentiation of the brain and behavior and hormonal influences on sex-typical social behaviors. The classic hypothesis posits that testicular hormones masculinize and defeminize neural circuits during a perinatal sensitive period, programming sex-typical activational responses to gonadal hormones in adulthood. Research since the mid- to late 1980s shows that a second wave of hormone-dependent organization of the brain and behavior occurs during puberty and adolescence and that ovarian hormones are actively involved in feminization of the brain during the adolescent period of organization. Next, a conceptual framework is presented for studying adolescent development of social cognition (the mental processes by which an individual encodes, interprets, and responds to sensory information from an animal of the same species) in the context of social reorientation, when during adolescence the source of social reward shifts from family to peers. The chapter reviews the literature on what social behaviors and aspects of social cognition are organized by pubertal hormones in males, as well as the nonsocial behaviors that are organized by pubertal hormones in males and females.

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