Review
Neural basis of maternal behavior in the rat

https://doi.org/10.1016/0306-4530(88)90006-6Get rights and content

Abstract

This article presents a review of the neural and neurochemical regulation of maternal behavior in the rat, emphasizing the role of the medial preoptic area (MPOA) and its neural connections in this regulation. Evidence for the role of the MPOA includes the following and will be discussed: (1) Axon-sparing lesions of the MPOA disrupt maternal behavior, indicating the involvement of MPOA neurons rather than fibers of passage. (2) Estradiol acts on the MPOA to facilitate maternal behavior. (3) An MPOA-to-lateral preoptic area-to-ventral tegmental area circuit may be part of the output pathway by which the MPOA influences maternal behavior. (4) MPOA neural circuitry may interact with olfactory neural circuitry and with the motor system to influence maternal responsiveness. (5) Opioid neural pathways appear to inhibit, and oxytocinergic neural pathways appear to promote, maternal behavior.

References (94)

  • J.R. Franz et al.

    Effects of hypothalamic knife cuts and experience on maternal behavior in the rat

    Physiol Behav

    (1986)
  • A.R. Fuchs

    The role of oxytocin in parturition

  • O. Gaffori et al.

    Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmentum lesions

    Physiol Behav

    (1979)
  • C.T. Grimm et al.

    Opiate regulation of maternal behavior in the rat

    Pharmacol Biochem Behav

    (1983)
  • R.P. Hammer

    The sexually dimorphic region of the preoptic area in rats contains denser opiate receptor binding sites in females

    Brain Res

    (1984)
  • M.H. Hastings et al.

    Neurotoxic amino acid lesions of the lateral hypothalamus: a parametric comparison of ibotenate, N-methyl-D,L-aspartate and quisqualate in the rat

    Brain Res

    (1985)
  • J. Hawthorn et al.

    Effects of lesions in the hypothalamic paraventricular, supraoptic and suprachiasmatic nuclei on vasopressin and oxytocin in rat brain and spinal cord

    Brain Res

    (1985)
  • L. Heimer et al.

    Ventral striatum and ventral pallidum — components of the motor system?

    Trends Neurosci

    (1982)
  • C.D. Jacobson et al.

    Effects of small medial preoptic area lesions on maternal behavior: retrieving and nestbuilding in the rat

    Brain Res

    (1980)
  • H. Khachaturian et al.

    Anatomy of the CNS opioid systems

    Trends Neurosci

    (1985)
  • R.E. Lang et al.

    Effects of lesions in the paraventricular nucleus of the hypothalamus on vasopressin and oxytocin contents in brainstem and spinal cord of rat

    Brain Res

    (1983)
  • A.D. Mayer et al.

    Effects of intranasal zinc sulfate on open field and maternal behavior in female rats

    Physiol Behav

    (1977)
  • B.S. McEwen et al.

    Hormone effects on hypothalamic neurons: analysing gene expression and neuromodulator action

    Trends Neurosci

    (1985)
  • W.B.J. Mens et al.

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

    Brain Res

    (1983)
  • M.O. Miceli et al.

    Disruption of maternal behavior in virgin and postparturient rats following sagittal plane knife cuts in the preoptic area-hypothalamus

    Behav Brain Res

    (1983)
  • R.L. Moss et al.

    Excitation of antidromically identified neurosecretory cells of the paraventricular nucleus by oxytoxin applied iontophoretically

    Exp Neurol

    (1972)
  • W.J.H. Nauta et al.

    Efferent connections and nigral afferents of the nucleus accumbens septi in the rat

    Neurosci

    (1978)
  • M. Numan

    Progesterone inhibition of maternal behavior in the rat

    Horm Behav

    (1978)
  • M. Numan et al.

    The connections of the medial preoptic region and maternal behavior in the rat

    Physiol Behav

    (1980)
  • M. Numan et al.

    The effects of paraventricular hypothalamic lesions on maternal behavior in rats

    Physiol Behav

    (1985)
  • C.A. Pedersen et al.

    Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior

    Neuropeptides

    (1985)
  • R. Ravid et al.

    Immunocytochemically stained binding sites for oxytocin and α-melanocyte-stimulating hormone in rat brain following ventricular administration

    Brain Res

    (1986)
  • B.S. Rubin et al.

    Disruption of ongoing maternal responsiveness by central administration of morphine sulfate

    Brain Res

    (1984)
  • P.E. Sawchenko et al.

    A method for tracing biochemically defined pathways in the central nervous system using combined fluorescence retrograde transport and immunohistochemical techniques

    Brain Res

    (1981)
  • H. Simon et al.

    Efferents and afferents of the ventral tegmental area—A10 region studied after local injection of [3H] leucine and horseradish peroxidase

    Brain Res

    (1979)
  • M.V. Sofroniew

    Morphology of vasopressin and oxytocin neurones and their central and vascular projections

  • D.A. Steindler et al.

    Combined immunocytochemistry and autoradiographic retrograde axonal tracing for identification of transmitters of projection neurons

    J Neurosci Meth

    (1983)
  • G.R. Stewart et al.

    N-methylaspartate: an effective tool for lesioning basal forebrain cholinergic neurons of the rat

    Brain Res

    (1986)
  • L.W. Swanson

    The projections of the ventral tegmental area and adjacent regions: a combined retrograde fluorescent tracer and immunofluorescence study in the rat

    Brain Res Bull

    (1982)
  • L.W. Swanson et al.

    Evidence for a projection from the lateral preoptic area and substantia innominata to the mesencephalic locomotor region in the rat

    Brain Res

    (1984)
  • J. Terkel et al.

    Effects of transecting lateral neural connections of the medial preoptic area on maternal behavior in the rat: nest building, pup retrieval and prolactin secretion

    Brain Res

    (1979)
  • F.W. Van Leeuwen et al.

    Light microscopic autoradiographic localization of [3H]-oxytocin binding sites in the rat brain, pituitary and mammary gland

    Brain Res

    (1985)
  • M. Alexandrova et al.

    Oxytocin receptors and parturition. I. Control of oxytocin receptor concentration in the rat myometrium at term

    Endocrinology

    (1980)
  • R.S. Bridges et al.

    Reversal of morphine disruption of maternal behavior by concurrent treatment with the opiate antagonist naloxone

    Science

    (1982)
  • R.S. Bridges et al.

    Changes in beta-endorphin concentrations in the medial preoptic area during pregnancy in the rat

    Ann Meet Soc Neurosci

    (1983)
  • L.C. Conrad et al.

    Efferents from the medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area

    J Comp Neurol

    (1976)
  • S.E. Fahrbach et al.

    Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats

    Neuroendocrinology

    (1985)
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