Elsevier

Hormones and Behavior

Volume 47, Issue 3, March 2005, Pages 241-255
Hormones and Behavior

Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones

https://doi.org/10.1016/j.yhbeh.2004.11.001Get rights and content

Abstract

Changes in emotional behavior occur across the reproductive cycle in female rodents, with reduced anxiety found during the postpartum period, but relatively little is known about factors contributing to this decreased anxiety. Using increased duration of time spent in the open arms of an elevated plus-maze as an indicator of reduced anxiety, it was found in a series of experiments that (1) anxiety is significantly reduced in Long–Evans females during the first week of lactation, but not thereafter, (2) relatively recent contact with pups before testing (within 4 h) is necessary for their reduced anxiety, (3) dams that receive only distal sensory cues from pups for the 4 h prior to testing do not show reduced anxiety, (4) the absence of nipples, and therefore a lack of suckling by pups, has no effect on dams' anxiety, (5) cesarean delivery of pups 2 days prior to expected parturition did not alter later anxiety in dams, (6) hypophysectomy during mid-pregnancy or ovariectomy within 24 h after parturition also did not prevent reduced anxiety in dams, and (7) differences in anxiety between lactating and virgin females are greatest 4–8 min after being placed in the plus-maze. Therefore, exposure to their own peripheral hormones through mid-pregnancy is sufficient to prime female rats to show reduced anxiety, but only if they later have recent physical interaction with pups. Furthermore, because suckling and the peripheral hormones released during suckling appear to be unnecessary, decreased anxiety in maternal rats may instead be regulated by the transient intracerebral release of neuropeptides or neurotransmitters while dams receive other types of tactile inputs from their infants.

Section snippets

Subjects

Subjects were female Long–Evans rats, descended from male and female rats purchased from Harlan Laboratories (Indianapolis, IN), that were born and raised in our colony. After weaning at 21 days of age, subjects were housed in clear polypropylene cages (48 × 28 × 16 cm) with wood shavings for bedding in groups of 2–3 female littermates per cage. Beginning at 75 days old, females' estrous cycles were monitored daily with a vaginal impedance meter (Fine Science Tools, Foster City, CA) and females

Temporal factors influencing anxiety during lactation

In almost all studies demonstrating the anxiolytic effects of lactation in rats, dams have been tested during the early postpartum period. This may have been fortuitous, because we demonstrate here that reduced anxiety is not found throughout all of lactation and is only evident soon after parturition and through the first postpartum week. Some studies reporting no differences between the behavior of lactating and virgin females in the elevated plus-maze did, in fact, test females during the

Acknowledgments

The assistance of Tami Menard and Naffie Ceesay in completing these experiments is greatly appreciated. This research was funded by an intramural research grant for new faculty provided by Michigan State University.

References (109)

  • S. Hansen

    Mechanisms involved in the control of punished responding in mother rats

    Horm. Behav.

    (1990)
  • E. Hard et al.

    Reduced fearfulness in the lactating rat

    Physiol. Behav.

    (1985)
  • J.R. Inglefield et al.

    Alterations in behavioral responses to stressors following excitotoxin lesion of dorsomedial hypothalamic regions

    Brain Res.

    (1994)
  • C.K. Kellogg et al.

    Reduced progesterone metabolites are not critical for plus-maze performance of lactating female rats

    Pharm. Biochem. Behav.

    (1999)
  • M.B. Kristal

    Enhancement of opioid-mediated analgesia: a solution to the enigma of placentophagia

    Neurosci. Biobehav. Rev.

    (1991)
  • S.L. Lightman et al.

    Peripartum plasticity within the hypothalamo–pituitary–adrenal axis

    Prog. Brain Res.

    (2001)
  • J.S. Lonstein et al.

    Sensory, hormonal, and neural control of maternal aggression in laboratory rodents

    Neurosci. Biobehav. Rev.

    (2002)
  • J.S. Lonstein et al.

    Somatosensory contributions to c-fos activation within the caudal periaqueductal gray of lactating rats: effects of perioral, rooting, and suckling stimuli from pups

    Horm. Behav.

    (1997)
  • D. Maestripieri et al.

    Maternal responsiveness increases during pregnancy and after estrogen treatment in macaques

    Horm. Behav.

    (1998)
  • F.K. Marcondes et al.

    Estrous cycle influences the response of female rats in the elevated plus-maze test

    Physiol. Behav.

    (2001)
  • W.B. Mens et al.

    Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): half-times of disappearance of these neuropeptide from CSF

    Brain Res.

    (1983)
  • S. Mora et al.

    Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats

    Psychoneuroendocrinology

    (1996)
  • H.D. Morgan et al.

    Somatosensory control of the onset and retention of maternal responsiveness in primiparous Sprague–Dawley rats

    Physiol. Behav.

    (1992)
  • I.D. Neumann

    Alterations in behavior and neuroendocrine stress coping strategies in pregnant, parturient, and lactating rats

    Prog. Brain Res.

    (2001)
  • G.G. Nomikos et al.

    Influence of oestrogen on spontaneous and diazepam-induced exploration of rats in an elevated plus-maze

    Neuropharmacology

    (1988)
  • B.G. Orpen et al.

    Hormonal influences on the duration of postpartum maternal responsiveness in the rat

    Physiol. Behav.

    (1987)
  • S. Pellow et al.

    Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat

    J. Neurosci. Methods

    (1985)
  • O. Picazo et al.

    Changes in experimental anxiety during pregnancy and lactation

    Physiol. Behav.

    (1993)
  • O. Picazo et al.

    The differential effect of the anxiolytic agent 8-OH-DPAT during lactation is independent of pup withdrawal and maternal behavior

    Psychoneuroendocrinology

    (2000)
  • U. Schmitt et al.

    Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling

    Pharmacol. Biochem. Behav.

    (1998)
  • J. Schulkin et al.

    Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implications for understanding the states of fear and anxiety and allostatic load

    Psychoneuroendocrinology

    (1998)
  • A. Shekhar

    GABA receptors in the region of the dorsomedial hypothalamus of rats regulate anxiety in the elevated plus-maze test. I. Behavioral measures

    Brain Res.

    (1993)
  • E. Sibolboro-Mezzacappa et al.

    Lactation and weaning effects on physiological and behavioral response to stressors

    Physiol. Behav.

    (2003)
  • J.M. Stern et al.

    Maternal aggression of rats is impaired by cutaneous anesthesia of the ventral trunk, but not by nipple removal

    Physiol. Behav.

    (1993)
  • J.M. Stern et al.

    Pituitary–adrenal activity in the postpartum rat in the absence of suckling stimulation

    Horm. Behav.

    (1972)
  • J.M. Stern et al.

    Postpartum, hormonal, and nonhormonal induction of maternal behavior in rats: effects on T-maze retrieval of pups

    Horm. Behav.

    (1976)
  • J.M. Stern et al.

    Dissociation of open-field behavior and pituitary–adrenal function

    Horm. Behav.

    (1973)
  • J.M. Stern et al.

    Do pup ultrasonic cries provoke prolactin secretion in lactating rats?

    Horm. Behav.

    (1984)
  • J. Terkel et al.

    Ultrasonic cries from infant rats stimulate prolactin release in lactating mothers

    Horm. Behav.

    (1979)
  • K. Uvnas-Moberg et al.

    High doses of oxytocin cause sedations and low doses cause an anxiolytic effect in male rats

    Pharmacol. Biochem. Behav.

    (1994)
  • M. Altemus et al.

    Responses to psychosocial stress in postpartum women

    Psychosom. Med.

    (2001)
  • I. Asher et al.

    Mood and hormonal changes during late pregnancy and puerperium

    Clin. Exp. Obstet. Gynacol.

    (1995)
  • T.L. Bale et al.

    CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior

    J. Neurosci.

    (2001)
  • C.G. Ballard et al.

    Postpartum anxiety in mother and fathers

    Eur. J. Psychiatry

    (1993)
  • Z. Banky et al.

    Effect of various partial separations of the litters from their mother on plasma prolactin levels of lactating rats

    Acta Biol. Hung.

    (1994)
  • D. Bitran et al.

    Ovarian endocrine status modulates the anxiolytic potency of diazepam and the efficacy of gamma-aminobutyric acid-benzodiazepine receptor-mediated chloride ion transport

    Behav. Neurosci.

    (1991)
  • D. Bitran et al.

    Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABAa receptors

    J. Neuroendocrinol.

    (1995)
  • R.S. Bridges

    A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat

    Endocrinology

    (1984)
  • R.S. Bridges et al.

    Suckling and LH-induced progesterone secretion in lactating hamsters (Mesocricetus auratus)

    Neuroendocrinology

    (1976)
  • P.J. Cooper et al.

    Non-psychotic psychiatric disorder after child birth: a prospective study of prevalence, incidence, course and nature

    Br. J. Psychiatry

    (1988)
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