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An Introduction to Hormones and Behavior

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An Introduction to Hormones and Behavior

First Edition

Edited by Karen L. Bales

Chapter 1: Endocrine Principles and Methods 1Key Words 1Prewriting 1Introduction 2

The Transplantation of Testes By Arnold Adolph Berthold, translated by D. P. Quiring 8

Post Reading 10References Cited 11

Chapter 2: Sexual Differentiation and Sex Differences 14Key Words 14Prewriting 14Introduction 15

The Sex Chromosome Trisomy Mouse Model of XXY and XYY: Metabolism and Motor Performance By Xuqi Chen, et al. 18

Post Reading 39Characterization of Juvenile Play in Rats: Importance of Self and Sex of Partner By Kathryn J. Argue and Margaret M. McCarthy 39


Contents

Chapter 3: Development 59Key Words 59Prewriting 59Introduction 59

Developmental Exposure to Vasopressin Increases Aggression in Adult Prairie Voles By John M. Stribley and C. Sue Carter 61


Chapter 4: Female Reproduction 70Key Words 70Prewriting 70Introduction 71

The Rodent Estrous Cycle: Characterization of Vaginal Cytology and its Utility in Toxicological Studies By Jerome M. Goldman, et al. 76

Post Reading 99Bisphenol A Exposure is Associated with In Vivo Estrogenic Gene Expression in Adults By David Melzer, et al. 100


Chapter 5: Female Parental Behavior 117Key Words 117Prewriting 117Introduction 117

Impairments in the Initiation of Maternal Behavior in Oxytocin Receptor Knockout Mice By Megan E. Rich, et al. 123

Post Reading 140Nongenomic Transmission across Generations of Maternal Behavior and Stress Responses in the Rat By Darlene Francis, et al. 140


Chapter 6: Male Reproduction 152Key Words 152Prewriting 152Introduction 152

Note on the Effects Produced on Man by Subcutaneous Injections of a Liquid Obtained from the Testicles of Animals By Dr. Brown-Séquard 156

Post Reading 161Brown-Séquard Revisited: A Lesson from History on the Placebo Effect of Androgen Treatment By Andrea J Cussons, et al. 162

Post Reading 165Extracellular Dopamine in the Medial Preoptic Area: Implications for Sexual Motivation and Hormonal Control of Copulation By Elaine M. Hull, et al. 166

Post Reading 179Effects of Anabolic-Androgens on Brain Reward Function By Emanuela Mhillaj, et al. 180


Chapter 7: Male Parenting 208Key Words 208Prewriting 208Introduction 208

The “Challenge Hypothesis”: Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies By John C. Wingfield, et al. 212

Post Reading 231Behavioral and Genetic Correlates of the Neural Response to Infant Crying among Human Fathers By Jennifer S. Mascaro, et al. 231


Chapter 8: Social Behavior 252Key Words 252Prewriting 252Introduction 252

Monogamous Brains and Alternative Tactics: Neuronal V1ar, Space Use, and Sexual Infidelity Among Male Prairie Voles By Steven M. Phelps and Alexander G. Ophir 257

Post Reading 276Marmosets Treated with Oxytocin are More Socially Attractive to their Long-Term Mate By Jon Cavanaugh, et al. 277


Chapter 9: Stress 298Key Words 298Prewriting 298Introduction 298

Integrating Stress Physiology, Environmental Change, and Behavior in Free-Living Sparrows By Creagh W. Breuner, and Thomas P. Hahn 302

Post Reading 316Behavioral Inhibition and Stress Reactivity: The Moderating Role of Attachment Security By Melissa Nachmias, et al. 317


Chapter 10: Hormones and Human Behavior 338Key Words 338Prewriting 338Introduction 338

The Acute Effects of Intranasal Oxytocin Administration on Endocrine and Sexual Function in Males By Andrea Burri, et al. 341

Post Reading 357Oxytocin Increases the Influence of Public Service Advertisements By Pei-Ying Lin, et al. 358


1

Key WordsHormoneCompetitive bindingAntagonistEnzyme immunoassayAntigenSamplesNeurotransmitter

ReceptorAgonistRadioimmunoassayAntibodyStandardsBehavioral endocrinologyEndocrine gland

Prewriting1. How do you think hormones affect your daily life? 2. See how much you know! Classify each of the following as a hormone, a neurotrans-

mitter, neither, or both:a. Testosteroneb. Estrogenc. Oxytocind. Vitamin De. Vasopressinf. Dopamineg. Serotonin

CHAPTER ONEEndocrine Principles and Methods

2 • An Introduction to Hormones and Behavior

Introduction What are Hormones, Where are They Produced, and How Do They Act?Hormones are chemicals produced in an organ (the brain, pituitary, ovaries, etc.), which then travel to target sites through the bloodstream.1 “Behavioral endocrinology,” or “behavioral neuroendocrinology,” is the field in which we study the relationship between hormones and behavior.2 Classic hormone action differs from that of neurotransmitters, which, rather than traveling through the bloodstream, act to carry a message across the synapse between two neurons; however, some chemicals, such as oxytocin and vasopressin, can act both as hormones and also as neurotransmitters.3

Hormones are produced in endocrine glands (sometimes called ductless glands), which by definition produce substances that are secreted into the blood. These glands include the thyroid, parathyroid, pituitary, testes, pancreas, ovaries, etc. (and the brain)4 (Table 1.1).

Different Types of HormonesHormones are grouped based on their chemical characteristics. Hormones are also char-acterized as either lipophilic (fat-soluble) or hydrophilic (water-soluble). Solubility can affect whether or not the hormone can easily pass through the cell membrane to act on receptors in the nucleus (see below). Out of the groups in Table 1.1, steroids and eicosanoids are lipophilic, whereas protein and monoamine hormones are hydrophilic.5

TABLE 1.1 Major groups of hormones and where they are produced6

Hormone Group ExamplesEndocrine Glands Where They are Produced

Steroids Glucocorticoids (cortisol, corticosterone)

Adrenal gland (cortex)

Mineralocorticoids (aldosterone) Adrenal gland (medulla)

Estrogens (estrone, estradiol) Ovaries, brain

Progestins (progesterone) Ovaries

Androgens (testosterone, DHEA) Testes, adrenal glands, brain

Proteins/Peptides Oxytocin, vasopressin, LH, FSH, TSH Brain, ovaries, pituitary

1 I.P. Stolerman, “Hormone,” in Encyclopedia of Psychopharmacology, ed. I.P. Stolerman (Berlin: Spring-er-Verlag, 2010).

2 P. Marler, “Ethology and the Origins of Behavioral Endocrinology,” Hormones and Behavior 47 (2005). 3 H.H. Zingg, “Oxytocin,” in Hormones, Brain, and Behavior, ed. D. Pfaff, et al. (New York, 779–802:

Academic Press, 2002). 4 C.H. Giraud, “The Endocrine Glands,” The Australasian Journal of Optometry 15 (1932). 5 H. Lodish et al., Molecular Cell Biology, 6th edition (New York: W.H. Freeman, 2007). 6 H.L. Henry and A.W. Norman, in Encyclopedia of Hormones, ed. H.L. Henry and A.W. Norman (Academic

Press, 2003).

Chapter One: Endocrine Principles and Methods • 3

Hormone Group ExamplesEndocrine Glands Where They are Produced

Monoamines Catecholamine (epinephrine, norepinephrine, dopamine)

Adrenal medulla, brain

Indoleamines (serotonin, melatonin) Brain, intestines

Eicosanoids Prostaglandins Most tissues and organs

After hormones reach their target site, they must bind to receptors in order to act. Hormones may have just one receptor, such as oxytocin, or multiple receptors, such as vasopressin. Sometimes hormones can also bind to each other’s receptors to varying degrees. For instance, oxytocin and vasopressin can bind to each other’s receptors.7

Some receptors are on cell membranes and act through “second messenger systems” in which they activate intracellular signaling molecules, leading to a cellular response. There are many types of second messengers.8 It is also possible for the same hormone to activate more than one type of second messenger, depending on the context.9

Other hormones pass through the cell membrane and bind to receptors in the nucleus of the cell. They then directly affect gene expression and translation to protein. This is usually a slower process than the use of second messenger systems.10 In the past, it was thought that steroid hormones bound to nuclear receptors, and peptide hormones bound to membrane receptors, one reason that steroid hormones typically take longer to act than peptides. More recently, it has been shown that estrogens, for example, can act via fast- acting membrane receptors or slower-acting nuclear receptors. For instance, male beach mice (Peromyscus polionotus) decrease aggression during long days (winter photoperiod) using nuclear receptors, and increase aggression in short days (summer photoperiod) using membrane receptors.11 Glucocorticoids and mineralocorticoids also act on both membrane and nuclear receptors.12

Measuring Hormones: The Principle of Competitive BindingMany of the techniques we use to measure hormones are based on the principle of compet-itive binding, developed by Rosalyn Yalow and Solomon Berson; Yalow received a Nobel Prize in Physiology or Medicine for her discovery in 1977 (Berson died five years earlier,

7 C. Barberis and E. Tribollet, “Vasopressin and Oxytocin Receptors in the Central Nervous System,” Critical Reviews in Neurobiology 10, no. 1 (1996).

8 D. Purves et al., Neuroscience, 2nd Edition (Sunderland, MA: Sinauer Associates, 2001). 9 E.H. van den Burg and I.D. Neumann, “Bridging the Gap between Gpcr Activation and Behaviour: Oxytocin

and Prolactin Signalling in the Hypothalamus,” Journal of Molecular Neuroscience 43 (2011).10 M. Beato and J. Klug, “Steroid Hormone Receptors: An Update,” Human reproduction update 6 (2000).11 B.C. Trainor et al., “Photoperiod Reverses the Effects of Estrogens on Male Aggression Via Genomic and

Nongenomic Pathways,” Proceedings of the National Academy of Sciences 104 (2007).12 F.L. Groeneweg et al., “Mineralocorticoid and Glucocorticoid Receptors at the Neuronal Membrane,

Regulators of Nongenomic Corticosteroid Signalling,” Molecular and Cellular Endocrinology 350 (2012).


so could not receive the prize with her).13 The principle states that unlabeled hormone will compete with labeled hormone for antibody binding sites, and the fraction of labeled hormone bound will decrease with an increase in the unlabeled hormone. This was first used to measure human insulin.14

This principle was used to create radioimmunoassays, which work as follows:

1. An antibody is created that binds with the substance we want to measure.2. A radioactive label is attached to the substance we want to measure. This is called

the tracer.3. Known amounts of the substance (unlabeled, called “standards”) are allowed to

bind to the antibody. 4. Unknown amounts (unlabeled, called “samples”) are allowed to bind to the antibody.5. The tracer is incubated with the standards and the samples. It will bind to any

antibody binding sites not occupied already. The number of antibody sites occupied by the tracer will be inverse to those occupied by the standard/sample. Therefore, the more hormone in your sample, the less tracer will bind there. This means the lower the hormone in your sample, the more radioactive it is; and vice versa.

6. The standards are used to create a regression curve or line. This is used to calculate the values in the samples (Figure 1.1).15

13 C.R. Kahn and J. Roth, “Berson, Yalow, and the Jci: The Agony and the Ecstasy,” The Journal of Clinical Investigation 114 (2004).

14 R.S. Yalow and S.A. Berson, “Immunoassay of Endogenous Plasma Insulin in Man,” ibid.39 (1960).15 Ibid.

FIGURE 1.1 Radioimmunoassay procedure

1) An antibody to thehormone is made andplaced in tubes.

2) Known amounts ofunlabeled hormones areadded to some tubes.�ese are calledstandards.

3) Your samples areadded to tubes. Eachsample has an unknownamount of unlabeledhormone.

4) Add a known amountof labeled (radioactive)hormone to all test tubes.�is will compete with theunlabeled hormone forantibody binding sites.

5) �e more unlabeled hormonein your sample, the less labeledhormone will bind. �is will allowyou to create a “standard curve”using your known amounts.

6) You can then use regressiontechniques to place your unknownamounts (samples) on the curve,and get �nal concentrations of thehormone.

Am

ount

of

horm

one

Am

ount

of

horm

one

Radioactivity

Radioactivity


Enzyme immunoassays were based on the same principle, but instead of using radioac-tive labels, they used enzymatic labels that changed color in relation to how much or how little was bound to the antibody. These have the advantage of not using radioactivity, and therefore being safer.16

Other Endocrine MethodsThere are now a number of other techniques used to address questions in behavioral endocri-nology, most of which we will not cover in detail here. Many techniques, such as optogenetics or electrical stimulation, are behavioral neuroscience methods that focus on affecting the function of neurons, rather than hormones. Other methods to measure hormones include high-pressure liquid chromatography and mass spectroscopy; such methods have been used recently to advance our measurement and understanding of hormones such as ghrelin17 and oxytocin.18

Research DesignThere are a number of key principles involved in research design in behavioral endocrinology.

Controls: Among the most important aspects of experimental design are proper controls. Theoretically, a control subject should undergo the same actions your experimental subject is undergoing, except for the actual experimental treatment. For instance, a control for an estrogen injection would be an injection of the vehicle in which the estrogen was dissolved; a control for a surgical manipulation (such as castration) would be a sham surgery.

Since the usual controls for injected hormones are vehicle controls, it is important to remember that steroid hormones are hydrophobic (lipophilic) and dissolve in oil while peptide hormones are hydrophilic (lipophobic) and usually dissolve in saline or water.

Ablation and replacement: A critical way to examine the effect of a hormone is to remove it (ablation) and then replace it. Ablation of a hormone could be accomplished by such varied techniques as removal of the organ that makes the hormone; use of an antago-nist to bind to the receptor and prevent it from activating; lesion (temporary or permanent) of the brain area that makes the hormone; use of RNAi, which is a process by which RNA molecules block gene expression; etc. Replacement can then occur by giving the hormone to the subject, reactivating the brain area, etc. See this chapter’s reading for a classic example of an ablation and replacement experiment.19

16 R.M. Lequin, “Enzume Immunoassay (Eia)/Enzyme-Linked Immunosorbent Assay (Elisa),” Clinical Chemistry 51 (2005); A.H.B. Wu, “A Selected History and Future of Immunoassay Development and Applications in Clinical Chemistry,” Clinica Chimica Acta 269 (2006).

17 Z. Eslami, A. Ghassempour, and H.Y. Aboul-Enein, “Recent Developments in Liquid Chromatography-Mass Spectrometry Analyses of Ghrelin and Related Peptides,” Biomedical Chromatography (2016).

18 O.K. Brandtzaeg et al., “Proteomics Tools Reveal Startlingly High Amounts of Oxytocin in Plasma and Serum,” Scientific Reports 6 (2016).

19 D.P. Quiring, “Transplantation of Testes (by A.A. Berthold),” Bulletin of the History of Medicine 16 (1944).


Sex differences. The early behavioral endocrinologists often focused on males. This is changing, especially with the discovery that males and females can respond differently to the same medical treatments.20 The National Institutes of Health now requires grant proposals to consider the role of sex in research questions and study design.21 There are a large number of issues pertinent to the consideration of sex differences, including whether gonadal hormones (from the testes or ovaries) are involved at the time of testing, whether the trait is differentiated by sex during development, etc. In addition, the researcher must pay attention to the stage of the estrous/menstrual cycle in females, the forms of hormones given and routes of administration, etc.22

Circadian rhythms, and other types of systematic considerations. Many hor-mones, most notably glucocorticoids, display marked changes throughout the day. Cortisol in humans is highest at waking, and declines throughout the day.23 This can be viewed as a nuisance variable, and accounted for by collecting all samples at the same time of day. Changes in the circadian rhythms of cortisol, however, can also be important outcome variables and potential indications of affective disorders.24 Cortisol also varies with the estrous cycle and with pregnancy.25 To fully understand what is going on with any partic-ular hormone, we must pay close attention to all these sorts of systematic considerations.

Feedback loops. When studying hormones, it is important to remember that most act through negative feedback loops. That is, the released hormone acts on some part of the system (often the organ that released it), to reduce its own release. This allows the system to return to homeostasis. The hypothalamo-pituitary-adrenal (HPA) axis is a classic example of negative feedback (see Chapter 9 and Figure 9.1). There are also a few examples of positive feedback loops, in which a rise in a hormone leads to a further rise. One of these examples is ovulation (see Chapter 4).

Where Do We Measure Hormones?Should we measure hormones in blood, urine, saliva, feces, or cerebrospinal fluid? How about directly in the brain? These decisions should be informed by which hormone we want to measure, and what sort of access we have to our subjects. Measurement of plasma directly

20 A.K. Beery and I. Zucker, “Sex Bias in Neuroscience and Biomedical Research,” Neuroscience and Biobe-havioral Reviews 35 (2011).

21 National Institutes of Health, NOT-OD-15-102, “Consideration of Sex as a Biological Variable in NIH-funded Research” (2015).

22 J.B. Becker et al., “Strategies and Methods for Research on Sex Differences in Brain and Behavior,” Endocrinology 146 (2005).

23 J.D. Guerry and P.D. Hastings, “In Search of Hpa Axis Dysregulation in Child and Adolescent Depression,” Clinical Child and Family Psychology Review 14 (2011).

24 Ibid.25 K.L. Bales et al., “Social and Reproductive Factors Affecting Cortisol Levels in Wild Female Golden Lion

Tamarins,” American Journal of Primatology 67 (2005).

informs us about current release, but may not always be feasible.26 For humans (especially children) and companion or zoo animals, saliva is often the easiest fluid to obtain, and steroids are robustly measurable in saliva samples.27 Steroids are also measurable in urine and fecal samples, and these types of excretions are easier to obtain from wild animals.28 But both urine and fecal samples typically contain metabolized hormone that has accumulated since the animal last urinated or defecated, making these sorts of samples more difficult to interpret.29 Nonetheless, they have been successfully used both for conservation biology30 and also the study of basic behavioral processes in the field.31

Cerebrospinal fluid (CSF) is much more difficult to obtain (usually by lumbar puncture), and is often only obtained as a by-product of clinical procedures.32 It is, however, often thought to more accurately reflect the concentration of hormone present in the brain33.

Peptide hormones can be much more difficult to measure than steroid hormones, and for many reasons, including faster breakdown in the blood. While oxytocin and vasopressin are frequently measured in plasma, it appears release there may only sometimes be coordinated with release in the brain; for instance, in response to a social stimulus,34 and may sometimes be dissociated.35 It is also unclear how well urinary oxytocin reflects either plasma or brain oxytocin—one study found that while salivary oxytocin correlated with plasma oxytocin, urinary oxytocin did not correlate with either.36 Therefore, much more caution should be used when interpreting the meaning of peptide hormone concentrations in saliva or urine.

26 B.G. Walker, P.D. Boersma, and J.C. Wingfield, “Field Endocrinology and Conservation Biology,” Integrative and comparative biology 45 (2005).

27 N.A. Dreschel and D.A. Granger, “Advancing the Social Neuroscience of Human-Animal Interaction: The Role of Salivary Bioscience,” in The Social Neuroscience of Human-Animal Interaction, ed. L.S. Freund, et al. (Washington, D.C.: American Psychological Association, 2016).

28 P.L. Whitten, D.K. Brockman, and R.C. Stavisky, “Recent Advances in Noninvasive Techniques to Monitor Hormone-Behavior Interactions,” American Journal of Physical Anthropology S27 (1998).

29 Walker, Boersma, and Wingfield, “Field Endocrinology and Conservation Biology.”30 S. Creel et al., “Snowmobile Activity and Glucocorticoid Stress Responses in Wolves and Elk,” Conser-

vation Biology 16 (2002).31 K. Bales, J.A. French, and J.M. Dietz, “Explaining Variation in Maternal Care in a Cooperatively Breeding

Mammal,” Animal Behaviour 63 (2002).32 D.S. Carson et al., “Cerebrospinal Fluid and Plasma Oxytocin Concentrations Are Positively Correlated

and Negatively Predict Anxiety in Children,” Molecular Psychiatry 20 (2015).33 J.A. Amico, S.M. Challinor, and J.L. Cameron, “Pattern of Oxytocin Concentration in the Plasma and Cere-

brospinal Fluid of Lactating Rhesus Monkeys (Macaca Mulatta): Evidence for Functionally Independent Pathways in Primates,” Journal of Clinical Endocrinology and Metabolism 71 (1990).

34 W.M. Kenkel et al., “Neuroendocrine and Behavioural Responses to Exposure to an Infant in Male Prairie Voles,” Journal of Neuroendocrinology 24 (2012).

35 R. Landgraf and I.D. Neumann, “Vasopressin and Oxytocin Release within the Brain: A Dynamic Concept of Multiple and Variable Modes of Neuropeptide Communication,” Frontiers in Neuroendocrinology 25 (2004).

36 R. Feldman, I. Gordon, and O. Zagoory-Sharon, “Maternal and Paternal Plasma, Salivary, and Urinary Oxy-tocin and Parent-Infant Synchrony: Considering Stress and Affiliation Components of Human Bonding,” Developmental Science 14 (2011).



Behavioral Endocrinology in the Laboratory and in the FieldThe papers you will read as part of this course take place in the laboratory and in the field, with humans and with animals. Behavioral endocrinology is used in the context of creating new biomedical treatments; understanding the lives of wild animals; and giving us insight into the psychology of human beings. As you read the articles, consider how issues of hor-mones and behavior may affect your daily life. In the rest of this textbook, we consider the different major topical areas covered by behavioral endocrinology.


Post Reading (critical thinking/interpretation)1. Berthold does not explicitly state his hypotheses or reasons for doing this experi-

ment. What is he trying to find out?2. Did Berthold have controls? If so, what were they?3. What experimental treatment did each cockerel (a–f) receive? What was the result

for each individual?4. Why was it significant that a and d did not develop nice wattles and combs, and

fought only “in a half-hearted manner”?

5. Why was it significant that the testes in b, c, e, and f reattached and that comb and wattle growth was normal?

6. Why was it significant that testes c and f attached to the intestine rather than in their original places?

References CitedAmico, J.A., S.M. Challinor, and J.L. Cameron. “Pattern of Oxytocin Concentration in the Plasma

and Cerebrospinal Fluid of Lactating Rhesus Monkeys (Macaca Mulatta): Evidence for Func-tionally Independent Pathways in Primates.” Journal of Clinical Endocrinology and Metabolism 71 (1990): 1531–35.

Bales, K., J.A. French, and J.M. Dietz. “Explaining Variation in Maternal Care in a Cooperatively Breeding Mammal.” Animal Behaviour 63 (2002): 453–61.

Bales, K.L., J.A. French, C.M. Hostetler, and J.M. Dietz. “Social and Reproductive Factors Affecting Cortisol Levels in Wild Female Golden Lion Tamarins.” American Journal of Primatology 67 (2005): 25–35.

Barberis, C., and E. Tribollet. “Vasopressin and Oxytocin Receptors in the Central Nervous System.” Critical Reviews in Neurobiology 10, no. 1 (1996 1996): 119–54.

Beato, M., and J. Klug. “Steroid Hormone Receptors: An Update.” Human reproduction update 6 (2000): 225–36.

Becker, J.B., A.P. Arnold, K.J. Berkley, J.D. Blaustein, L.A. Eckel, E. Hampson, J.P. Herman, et al. “Strategies and Methods for Research on Sex Differences in Brain and Behavior.” Endocrinology 146 (2005 2005): 1650–73.

Beery, A.K., and I. Zucker. “Sex Bias in Neuroscience and Biomedical Research.” Neuroscience and Biobehavioral Reviews 35 (2011): 565–72.

Brandtzaeg, O.K., E. Johnsen, H. Roberg-Larsen, F.K. Seip, E.L. MacLean, L.R. Gesquiere, S. Leknes, E. Lundanes, and S.R. WIlson. “Proteomics Tools Reveal Startlingly High Amounts of Oxytocin in Plasma and Serum.” Scientific Reports 6 (2016): 31693.

Carson, D.S., S.W. Berquist, T.H. Trujillo, J.P. Garner, S.L. Hannah, S.A. Hyde, R.D. Sumiyoshi, et al. “Cerebrospinal Fluid and Plasma Oxytocin Concentrations Are Positively Correlated and Negatively Predict Anxiety in Children.” Molecular Psychiatry 20 (2015): 1085–90.

Creel, S., J.E. Fox, A. Hardy, J. Sands, B. Garrott, and R.O. Peterson. “Snowmobile Activity and Glucocorticoid Stress Responses in Wolves and Elk.” Conservation Biology 16 (2002): 809–14.

Dreschel, N.A., and D.A. Granger. “Advancing the Social Neuroscience of Human-Animal Interac-tion: The Role of Salivary Bioscience.” In The Social Neuroscience of Human-Animal Interaction, edited by L.S. Freund, S. McCune, L. Esposito, N.R. Gee and P. McCardle. Washington, D.C.: American Psychological Association, 2016.

Eslami, Z., A. Ghassempour, and H.Y. Aboul-Enein. “Recent Developments in Liquid Chromatogra-phy-Mass Spectrometry Analyses of Ghrelin and Related Peptides.” Biomedical Chromatography (2016).



Feldman, R., I. Gordon, and O. Zagoory-Sharon. “Maternal and Paternal Plasma, Salivary, and Urinary Oxytocin and Parent-Infant Synchrony: Considering Stress and Affiliation Components of Human Bonding.” Developmental Science 14 (2011): 752–61.

Giraud, C.H. “The Endocrine Glands.” The Australasian Journal of Optometry 15 (1932): 21–39.Groeneweg, F.L., H. Karst, E.R. de Kloet, and M. Joels. “Mineralocorticoid and Glucocorticoid

Receptors at the Neuronal Membrane, Regulators of Nongenomic Corticosteroid Signalling.” Molecular and Cellular Endocrinology 350 (2012): 299–309.

Guerry, J.D., and P.D. Hastings. “In Search of Hpa Axis Dysregulation in Child and Adolescent Depression.” Clinical Child and Family Psychology Review 14 (2011): 135–60.

Henry, H.L., and A.W. Norman. In Encyclopedia of Hormones, edited by H.L. Henry and A.W. Norman: Academic Press, 2003.

Kahn, C.R., and J. Roth. “Berson, Yalow, and the Jci: The Agony and the Ecstasy.” The Journal of Clinical Investigation 114 (2004): 1051–54.

Kenkel, W.M., J. Paredes, J.R. Yee, H. Pournajafi-Nazarloo, K.L. Bales, and C.S. Carter. “Neuroen-docrine and Behavioural Responses to Exposure to an Infant in Male Prairie Voles.” Journal of Neuroendocrinology 24 (2012): 874–86.

Landgraf, R., and I.D. Neumann. “Vasopressin and Oxytocin Release within the Brain: A Dynamic Concept of Multiple and Variable Modes of Neuropeptide Communication.” Frontiers in Neu-roendocrinology 25 (2004): 150–76.

Lequin, R.M. “Enzyme Immunoassay (EIA)/Enzyme-Linked Immunosorbent Assay (Elisa).” Clinical Chemistry 51 (2005): 2415–18.

Lodish, H., A. Berk, C.A. Kaiser, M. Krieger, M.P. Scott, A. Bretscher, H. Ploegh, P. Matsudaira. Molecular Cell Biology, 6th Edition. New York: W.H. Freeman, 2007.

Marler, P. “Ethology and the Origins of Behavioral Endocrinology.” Hormones and Behavior 47 (2005): 493–502.

Purves, D., G.J. Augustine, D. Fitzpatrick, L.C. Katz, A.-S. LaMantia, J.O. McNamara, and S.M. Williams. Neuroscience, 2nd Edition. Sunderland, MA: Sinauer Associates, 2001.

Quiring, D.P. “Transplantation of Testes (by A.A. Berthold).” Bulletin of the History of Medicine 16 (1944): 399–401.

Stolerman, I.P. “Hormone.” In Encyclopedia of Psychopharmacology, edited by I.P. Stolerman. Berlin: Springer-Verlag, 2010.

Trainor, B.C., S. Lin, M.S. Finy, M.R. Rowland, and R.J. Nelson. “Photoperiod Reverses the Effects of Estrogens on Male Aggression Via Genomic and Nongenomic Pathways.” Proceedings of the National Academy of Sciences 104 (2007): 9840–45.

van den Burg, E.H., and I.D. Neumann. “Bridging the Gap between Gpcr Activation and Behaviour: Oxytocin and Prolactin Signalling in the Hypothalamus.” Journal of Molecular Neuroscience 43 (2011): 200–08.

Walker, B.G., P.D. Boersma, and J.C. Wingfield. “Field Endocrinology and Conservation Biology.” Integrative and comparative biology 45 (2005): 12–18.

Whitten, P.L., D.K. Brockman, and R.C. Stavisky. “Recent Advances in Noninvasive Techniques to Monitor Hormone-Behavior Interactions.” American Journal of Physical Anthropology S27 (1998): 1–23.

Wu, A.H.B. “A Selected History and Future of Immunoassay Development and Applications in Clinical Chemistry.” Clinica Chimica Acta 269 (2006): 119–24.

Yalow, R.S., and S.A. Berson. “Immunoassay of Endogenous Plasma Insulin in Man.” The Journal of Clinical Investigation 39 (1960): 1157–75.

Zingg, H.H. “Oxytocin.” In Hormones, Brain, and Behavior, edited by D. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach and R.T. Rubin. New York, 779–802: Academic Press, 2002.


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