The effects of gonadal steroids on brain stimulation reward in female rats

Bless, Elizabeth P.; McGinnis, Kelley A.; Mitchell, Amy L.; Hartwell, Amy; Mitchell, John B.

doi:10.1016/s0166-4328(96)00129-5

Cited by 52Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesEstrogen and related hormone effects

The effects of gonadal steroids on brain stimulation reward in female rats

Bless, Elizabeth P., McGinnis, Kelley A., Mitchell, Amy L., Hartwell, Amy, Mitchell, John B.·1997·Behavioural Brain Research

DOI 10.1016/s0166-4328(96)00129-5

Open this paper in CoChat — free account

Abstract

The present study examined possible estrogen and/or progesterone effects on the mesolimbic dopamine (DA) system using brain stimulation reward (BSR). It is well known that BSR with electrical stimulation of the medial forebrain bundle (MFB) depends on the functioning of the mesolimbic DA system. If estrogen affects this system in a manner similar to its effects on the nigrostriatal DA system, reward measures would be expected to vary across the estrous cycle. Cycling female rats were trained to bar press for electrical stimulation to the MFB. Animals were tested at each stage of the estrous cycle, after ovariectomy and 4, 24, 48, 72 and 96 h after hormone replacement with estradiol (10 micrograms, s.c.), estradiol and progesterone (0.5 mg, s.c.), or oil (s.c.). The rewarding value of the stimulation and the maximum rate of bar pressing increased during estrus, but not during proestrus or metestrus, as compared with diestrus. Hormone replacement had differing effects on reward and motor performance. Motor performance increased 4 and 24 h after estrogen alone and 24 h after estrogen with the addition of progesterone 4 h before testing. The rewarding value of the stimulation increased only 24 h after estrogen together with an injection of progesterone 4 h before testing. These results indicate that gonadal steroids affect the functioning of the mesolimbic DA system.

Integrity signals

Registry

Crossref · 10.1016/s0166-4328(96)00129-5

Cites

52 of 52 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Testosterone and/or estradiol administration increases conditioned place preference, lever pressing for drug and saccharin, and reward-related brain stimulation in animals.
“administrations of testosterone and/or estradiol have been tied to increased conditioned place preference (Alexander, Packard, & Hines, 1994), lever pressing for drug and saccharin administration (Clark, Lindenfield, & Gibbons, 1996; Miele, Rosellin, & Svare, 1988), and reward-related brain stimulation (Bless et al., 1997).”
From Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking (2013) · cites this paper as Bless et al., 1997

The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Essentials of Behavioral Research: Methods and Data Analysis
Rosenthal, R., & Rosnow, R. L. (1984) · Cited by 3,925 · see citing works
Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain.
Olds, J., & Milner, P. (1954) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0058775 · Cited by 3,176 · see citing works
The Control of Progesterone Secretion During the Estrous Cycle and Early Pseudopregnancy in the Rat: Prolactin, Gonadotropin and Steroid Levels Associated with Rescue of the Corpus Luteum of Pseudopregnancy 1 2
Smith, M. S., Freeman, M. E., & Neill, J. D. (1975) · Endocrinology · doi:10.1210/endo-96-1-219 · Cited by 1,286 · see citing works
Sexual attractivity, proceptivity, and receptivity in female mammals
Beach, F. A. (1976) · Hormones and Behavior · doi:10.1016/0018-506x(76)90008-8 · Cited by 1,148 · see citing works
Methods of Assessing the Reinforcing Properties of Abused Drugs
Bozarth, M. A. (1987) · Springer eBooks · doi:10.1007/978-1-4612-4812-5 · Cited by 693 · see citing works
Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis
Hernandez, L., & Hoebel, B. G. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90036-7 · Cited by 627 · see citing works
Morphine-induced activation of A10 dopamine neurons in the rat
Gysling, K., & Wang, R. Y. (1983) · Brain Research · doi:10.1016/0006-8993(83)90913-7 · Cited by 493 · see citing works
Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine
Matthews, R. T., & German, D. C. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90048-4 · Cited by 426 · see citing works
Estrone and Estradiol Levels in the Ovarian Venous Blood from Rats During the Estrous Cycle and Pregnancy*
Shaikh, A. A. (1971) · Biology of Reproduction · doi:10.1093/biolreprod/5.3.297 · Cited by 385 · see citing works
Neuroendocrinology of Reproduction
(1981) · Springer eBooks · doi:10.1007/978-1-4684-3875-8 · Cited by 347 · see citing works
Sex differences in striatal dopamine: in vivo microdialysis and behavioral studies
Castner, S. A., Li, X., & Becker, J. B. (1993) · Brain Research · doi:10.1016/0006-8993(93)91225-h · Cited by 253 · see citing works
Brain reward circuitry: Four circuit elements “wired” in apparent series
Wise, R. A., & Bozarth, M. A. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90190-4 · Cited by 252 · see citing works
The curve-shift paradigm in self-stimulation
Miliaressis, E., Rompré, P.-P., Laviolette, P., Philippe, L., & Coulombe, D. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90388-4 · Cited by 243 · see citing works
Increased Dopamine Receptor Sensitivity After Estrogen Treatment Using the Rat Rotation Model
Hruska, R. E., & Silbergeld, E. K. (1980) · Science · doi:10.1126/science.7189902 · Cited by 225 · see citing works
Problems of measurement and interpretation with reinforcing brain stimulation.
Valenstein, E. S. (1964) · Psychological Review · doi:10.1037/h0040694 · Cited by 222 · see citing works
Quantitative microdialysis determination of extracellular striatal dopamine concentration in male and female rats: effects of estrous cycle and gonadectomy
Li, X., & Becker, J. B. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90510-x · Cited by 214 · see citing works
Sex differences in the amphetamine stimulated release of catecholamines from rat striatal tissue in vitro
Becker, J. B., & RAMIREZ, V. D. (1981) · Brain Research · doi:10.1016/0006-8993(81)90595-3 · Cited by 211 · see citing works
PERIPHERAL PLASMA OESTRADIOL AND LUTEINIZING HORMONE CONCENTRATIONS DURING THE OESTROUS CYCLE OF THE RAT
Brown-Grant, K., Exley, D., & Naftolin, F. N. (1970) · Journal of Endocrinology · doi:10.1677/joe.0.0480295 · Cited by 187 · see citing works
Eating and drinking cause increased dopamine release in the nucleus accumbens and ventral tegmental area in the rat: measurement by in vivo microdialysis
Yoshida, M., Yokoo, H., Mizoguchi, K., Kawahara, H., Tsuda, A., Nishikawa, T., & Tanaka, M. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90861-z · Cited by 179 · see citing works
The influence of estrogen on nigrostriatal dopamine activity
Becker, J. B., & Beer, M. E. (1986) · Behavioural Brain Research · doi:10.1016/0166-4328(86)90044-6 · Cited by 177 · see citing works
Evidence implicating descending fibers in self-stimulation of the medial forebrain bundle
Bielajew, C. H., & Shizgal, P. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-04-00919.1986 · Cited by 175 · see citing works
Pimozide and amphetamine have opposing effects on the reward summation function
Gallistel, C. R., & Karras, D. J. (1984) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(84)90104-7 · Cited by 154 · see citing works
Effects of Daily Cocaine and Morphine Treatment on Somatodendritic and Terminal Field Dopamine Release
Kalivas, P. W., & Duffy, P. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb03036.x · Cited by 140 · see citing works
Partial dopamine depletion of the prefrontal cortex leads to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli
Mitchell, J., & Gratton, A. P. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03609.1992 · Cited by 139 · see citing works
Self-citation
Estrous Cyclicity in Mammals
Feder, H. H. (1981) · Springer eBooks · doi:10.1007/978-1-4684-3875-8_10 · Cited by 138 · see citing works
PLASMA AND PITUITARY LUTEINIZING HORMONE AND PERIPHERAL PLASMA OESTRADIOL CONCENTRATIONS IN THE NORMAL OESTROUS CYCLE OF THE RAT AND AFTER EXPERIMENTAL MANIPULATION OF THE CYCLE
Naftolin, F. N., Brown-Grant, K., & Corker, C. S. (1972) · Journal of Endocrinology · doi:10.1677/joe.0.0530017 · Cited by 129 · see citing works
General Endocrinology.
(1966) · Annals of Internal Medicine · doi:10.7326/0003-4819-65-4-871_1 · Cited by 116 · see citing works
Does pimozide block the reinforcing effect of brain stimulation?
Gallistel, C. R., Boytim, M. J., Gomita, Y., & Klebanoff, L. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90360-4 · Cited by 113 · see citing works
PRE-OVULATORY PROGESTERONE, THE ADRENAL CORTEX AND THE 'CRITICAL PERIOD' FOR LUTEINIZING HORMONE RELEASE IN RATS
Feder, H. H., Brown-Grant, K., & CORKER, C. S. (1971) · Journal of Endocrinology · doi:10.1677/joe.0.0500029 · Cited by 112 · see citing works
Characterization of the striatal dopamine receptor supersensitivity produced by estrogen treatment of male rats
Hruska, R. E., Ludmer, L. M., & Silbergeld, E. K. (1980) · Neuropharmacology · doi:10.1016/0028-3908(80)90095-7 · Cited by 101 · see citing works
Effects of peripheral and central dopamine blockade on lateral hypothalamic self-stimulation: Evidence for both reward and motor deficits
Stellar, J. R. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90466-5 · Cited by 101 · see citing works
Temporal Interrelationships Between Plasma LH, Ovarian Secretion Rates and Peripheral Plasma Progestin Concentrations in the Rat: Effects of Nembutal and Exogenous Gonadotropins
Barraclough, C. A., COLLU, R., Massa, R., & Martini, L. (1971) · Endocrinology · doi:10.1210/endo-88-6-1437 · Cited by 98 · see citing works
Neuroleptic attenuation of intracranial self-stimulation: Reward or performance deficits?
Wise, R. A. (1978) · Life Sciences · doi:10.1016/0024-3205(78)90331-4 · Cited by 95 · see citing works
Bimodal Effect of Progesterone on in vitro Dopamine Function of the Rat Corpus striatum
Dluzen, D. E., & Ramirez, V. D. (2008) · Neuroendocrinology · doi:10.1159/000123971 · Cited by 85 · see citing works
Influence of gonadal hormones on social, sexual, emergence, and open field behaviour in the rat (Rattus norvegicus)
Quadagno, D. M., Shryne, J. E., Anderson, C., et al. (1972) · Animal Behaviour · doi:10.1016/s0003-3472(72)80145-3 · Cited by 80 · see citing works
A microcomputer-based method for physiologically interpretable measurement of the rewarding efficacy of brain stimulation
Campbell, K. A., Evans, G. J., & Gallistel, C. R. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90315-4 · Cited by 78 · see citing works
Estrogen potentiates the stereotypy induced by dopamine agonists in the rat
Chiodo, L. A., Caggiula, A. R., & Saller, C. F. (1981) · Life Sciences · doi:10.1016/0024-3205(81)90167-3 · Cited by 77 · see citing works
Dissociation of active from immobility components of sexual behavior in female rats by central 6-hydroxydopamine: Implications for CA involvement in sexual behavior and sensorimotor responsiveness
Caggiula, A. R., Herndon, J. G., Scanlon, R., Greenstone, D., Bradshaw, W. G., & Sharp, D. (1979) · Brain Research · doi:10.1016/0006-8993(79)90582-1 · Cited by 74 · see citing works
Time-dependent effects of estradiol and progesterone on the number of striatal dopaminergic D2-receptors
Fernández‐Ruíz, J., Amor, J. C., & Ramos, J. A. (1989) · Brain Research · doi:10.1016/0006-8993(89)91266-3 · Cited by 70 · see citing works
Decline of sexual behavior in castrated male rats: Effects of female precopulatory behavior
Madlafousek, J., Hlinak, Z., & Beran, J. (1976) · Hormones and Behavior · doi:10.1016/0018-506x(76)90051-9 · Cited by 64 · see citing works
Onset of the receptive and proceptive components of feminine sexual behavior in rats following the intravenous administration of progesterone
Glaser, J. H., Rubin, B. S., & Barfield, R. J. (1983) · Hormones and Behavior · doi:10.1016/0018-506x(83)90012-0 · Cited by 50 · see citing works
Effects of estrogen upon dopamine release from the corpus striatum of young and aged female rats
McDermott, J. L. (1993) · Brain Research · doi:10.1016/0006-8993(93)91578-g · Cited by 49 · see citing works
Importance of Female's Precopulatory Behaviour for the Primary Initiation of Male's Copulatory Behaviour in the Laboratory Rat
Madlafousek, J., & Hlinak, Z. (1983) · Behaviour · doi:10.1163/156853983x00381 · Cited by 38 · see citing works
Interpretation of Lesion Effects on Stimulant Self-Administration
Roberts, D. C. S., & Zito, K. A. (1987) · Springer eBooks · doi:10.1007/978-1-4612-4812-5_4 · Cited by 34 · see citing works
Estrous Cycle in the Rat: Effects on Self-Stimulation Behavior
Prescott, R. G. W. (1966) · Science · doi:10.1126/science.152.3723.796 · Cited by 34 · see citing works
Lack of correlation between naloxone-induced changes in sexual behavior and serum LH in male rats
McConnell, S. K., Baum, M. J., & Badger, T. M. (1981) · Hormones and Behavior · doi:10.1016/0018-506x(81)90032-5 · Cited by 33 · see citing works
Detailed analysis of estrous-related changes in wheel running and self-stimulation
Steiner, M. S., Katz, R. J., & Carroll, B. J. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90127-5 · Cited by 28 · see citing works
Effects of estrogen on self-stimulation behavior in ovariectomized rats
Meyerson, B. J., Wilkins, S. E., & Sawyer, C. H. (1969) · Physiology & Behavior · doi:10.1016/0031-9384(69)90177-2 · Cited by 8 · see citing works
Temporal aspects of ventromedial hypothalamic progesterone action in the facilitation of estrous behavior in the female rat.
Glaser, J. H., Etgen, A. M., & Barfield, R. J. (1987) · Behavioral Neuroscience · doi:10.1037/0735-7044.101.4.534 · Cited by 6 · see citing works
Temporal aspects of ventromedial hypothalamic progesterone action in the facilitation of estrous behavior in the female rat.
Glaser, J. H., Etgen, A. M., & Barfield, R. J. (1987) · Behavioral Neuroscience · doi:10.1037//0735-7044.101.4.534 · Cited by 5 · see citing works

Flagged first, then by citations

Sorted by citations

The brain reward circuitry in mood disorders
Russo, S. J., & Nestler, E. J. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3381 · Cited by 1,870 · see citing works
Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking
Smith, A. R., Chein, J., & Steinberg, L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.006 · Cited by 214 · see citing works
Reinforcing aspects of androgens
Wood, R. I. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.012 · Cited by 121 · see citing works
Reproductive steroids and ADHD symptoms across the menstrual cycle
Roberts, B., Eisenlohr-Moul, T., & Martel, M. M. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.11.015 · Cited by 77 · see citing works

Acupuncture Modulates Intracranial Self-Stimulation of the Medial Forebrain Bundle in Rats
Yoon, S. S., Yun, J., Lee, B. H., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147519 · Cited by 2 · see citing works
Comparisons of refractory periods for medial forebrain bundle fibers subserving stimulation-induced feeding and brain stimulation reward: a psychophysical study
Gratton, A. P., & Wise, R. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)91344-3 · Cited by 27 · see citing works
Tripelennamine: Enhancement of brain-stimulation reward
Unterwald, E. M., Kucharski, L. T., Williams, J. E. G., et al. (1984) · Life Sciences · doi:10.1016/0024-3205(84)90585-x · Cited by 24 · see citing works
The distribution of changes in local cerebral energy metabolism associated with brain stimulation reward to the medial forebrain bundle of the rat
Porrino, L. J., Huston-Lyons, D., Bain, G. T., et al. (1990) · Brain Research · doi:10.1016/0006-8993(90)90218-z · Cited by 52 · see citing works
Effect of some brain lesions on intracranial self-stimulation in the rat
Boyd, E., & Gardner, L. C. (1967) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1967.213.4.1044 · Cited by 56 · see citing works

Authors: Bless, E. P., McGinnis, K. A., Mitchell, A. L., Hartwell, A., & Mitchell, J. B.
Affiliations: Boston College (US)
Corresponding author: Bless, Elizabeth P.
Mitchell, John B.
ORCID: Bless, Elizabeth P.
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 1997-01
Volume: 82
Issue: 2
Pages: 235-244
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/s0166-4328(96)00129-5
OpenAlex: W2170549725
Cited by: 52
References: 52
Citations by year: 2026: 1 · 2025: 1 · 2024: 3 · 2023: 2 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 2 · 2017: 2 · 2016: 2 · 2015: 2 · 2013: 4 · 2012: 1
FWCI: 0.92
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords: sex steroids, estrogen, progesterone, brain stimulation reward, mesolimbic dopamine system, medial forebrain bundle, estrous cycle, estradiol replacement, ovariectomy, female rats, motor performance
MeSH terms: Animals, Brain, Conditioning, Operant, Dopamine, Estrogens, Estrus, Female, Medial Forebrain Bundle, Ovariectomy, Progesterone, Reward, Self Stimulation, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The effects of gonadal steroids on brain stimulation reward in female rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks