Effect of stress on the voluntary intake of a sweetened ethanol solution in pair-housed adolescent and adult rats
Abstract
BACKGROUND: Data regarding the effects of stressors on ethanol intake are mixed. Previous experiments reporting greater voluntary intake of ethanol in adolescent than adult rats have examined intake in isolate-housed animals. Given that the stress of isolate housing may differ ontogenetically as well as confound interpretation of other stressor effects, the present study examined stressor/ethanol interactions among pair-housed adolescent and adult rats. METHODS: Sprague-Dawley male rats were implanted with identification tags that allowed individual monitoring of home cage intake of water and either a 10% (v/v) ethanol solution containing 0.1% (w/v) saccharin or saccharin alone over a 14-day access period. Animals were given zero, one, or eight daily 15-min footshock sessions, with shock-induced freezing and pre-, post-, and recovery corticosterone levels determined on the first and last footshock exposure days. After the access period, withdrawal was assessed with a plus maze, and tolerance to ethanol-induced loss of righting reflex was examined. RESULTS: Nonstressed adolescents drank considerably more sweetened ethanol than did adults, with chronic stress suppressing this adolescent consumption. Ethanol access in adolescents disrupted within-session adaptation to footshock in terms of freezing behavior, although no such disruption was evident at either age when indexed hormonally. Despite relatively high ethanol intakes (up to 6 g/kg/day in the adolescents), no evidence for withdrawal-associated anxiogenesis emerged. Evidence for tolerance was mixed and, to the extent that it was present, was metabolic in nature. CONCLUSIONS: Previous reports of heightened voluntary ethanol intake among adolescent rats are not a function of isolate stress but are evident in pair-housed animals. Adolescents were more sensitive to ethanol/stress interactions than were adults, with the elevated ethanol intake of pair-housed adolescents selectively disrupted by chronic stress, a stress-induced disruption not evident in adults. Likewise, ethanol disrupted behavioral adaptation to the footshock stressor among adolescents but not adults.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Adolescent rats voluntarily ingest larger quantities of alcohol than adults.
“Adolescent rats voluntarily ingest larger quantities of alcohol than adults using a variety of access paradigms (25–28).”
From Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents (2018) · cites this paper as [25]
Cites
Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Self-citationAnxiety, defence and the elevated plus-maze.
Rodgers, R., & Dalvi, A. (1997) · Neuroscience and Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00058-9 · Cited by 1,028 · see citing works
Alcoholism: theory, problem and challenge. II. Reinforcement theory and the dynamics of alcoholism.
Conger, J. J. (1956) · PubMed · Cited by 810 · see citing works
II. Reinforcement Theory and the Dynamics of Alcoholism
Conger, J. J. (1956) · Quarterly Journal of Studies on Alcohol · doi:10.15288/qjsa.1956.17.296 · Cited by 617 · see citing works
Parallel circuits mediating distinct emotional coping reactions to different types of stress
Keay, K. A., & Bandler, R. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00049-5 · Cited by 512 · see citing works
Hall, F. S. (1998) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v12.i1-2.50 · Cited by 512 · see citing works
Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats
Gale, G. D., Anagnostaras, S., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., Wiltgen, B. J., & Fanselow, M. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4100-03.2004 · Cited by 427 · see citing works
Laviola, G., Adriani, W., Terranova, M. L., & Gerra, G. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00032-9 · Cited by 345 · see citing works
Differential Effects of Ethanol on Memory in Adolescent and Adult Rats
Markwiese, B. J., Acheson, S. K., Levin, E. D., Wilson, W. A., & Swartzwelder, H. S. (1998) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.1998.tb03668.x · Cited by 320 · see citing works
Lü, L., Shepard, J. D., Hall, F. S., & Shaham, Y. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00073-3 · Cited by 277 · see citing works
Stress and the developing limbic-hypothalamic-pituitary-adrenal axis
M. Vázquez, D. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00029-8 · Cited by 274 · see citing works
Differential Effects of Ethanol in Adolescent and Adult Rats
Little, P., Kuhn, C. M., Wilson, W. A., & Swartzwelder, H. S. (1996) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1996.tb01133.x · Cited by 240 · see citing works
Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats
Doremus‐Fitzwater, T. L., Brunell, S. C., Varlinskaya, E. I., & SPEAR, L. P. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00134-5 · Cited by 203 · see citing works
Self-citationInduction of dependence on ethanol by free-choice drinking in alcohol-preferring rats
Waller, M. B., McBride, W. J. H., Lumeng, L., et al. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90459-2 · Cited by 196 · see citing works
Age‐Dependent Inhibition of Long‐Term Potentiation by Ethanol in Immature Versus Mature Hippocampus
Swartzwelder, H. S., Wilson, W. A., & Tayyeb, M. I. (1995) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.1995.tb01011.x · Cited by 196 · see citing works
Hypothalamic-Pituitary-Adrenal Responses to Brief Social Separation
Hennessy, M. B. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00013-9 · Cited by 190 · see citing works
Sweetness Intensity and Pleasantness in Children, Adolescents, and Adults
de Graaf, C., & Zandstra, E. H. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00090-6 · Cited by 189 · see citing works
Devaud, L. L., Smith, F. D., Grayson, D. R., & Morrow, A. L. (1995) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)10544-0 · Cited by 184 · see citing works
INTERACTION OF ETHANOL AND STRESS: RESEARCH WITH EXPERIMENTAL ANIMALS—AN UPDATE
Pohorecky, L. A. (1990) · Alcohol and Alcoholism · doi:10.1093/oxfordjournals.alcalc.a045000 · Cited by 160 · see citing works
Dissociation Between Behavioral and Hormonal Responses to the Forced Swim Stress in Lactating Rats
Walker, C., Trottier, G., Rochford, J. M., & Lavallée, D. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00799.x · Cited by 159 · see citing works
Clément, Y. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00058-4 · Cited by 155 · see citing works
Rodgers, R. J., Johnson, N. J., Cole, J. C., et al. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02156-6 · Cited by 119 · see citing works
Maternal influences on ontogeny of suckling and feeding rhythms in the rat
Levin, R., & Stern, J. M. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077038 · Cited by 103 · see citing works
A New Assessment of the Ability of Oral Ethanol to Function as a Reinforcing Stimulus
Samson, H. H., Czachowski, C. L., & Slawecki, C. J. (2000) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2000.tb02054.x · Cited by 100 · see citing works
Greater Behavioral Effects of Stress in Immature as Compared to Mature Male Mice
Stone, E. A., & Quartermain, D. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00366-1 · Cited by 99 · see citing works
Acute and chronic stress effects on performance in a forced-swim task
Prince, C. R., & Anisman, H. (1984) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(84)90942-7 · Cited by 82 · see citing works
Stress-induced consumption of ethanol by rats
Nash, J. F., & Maickel, R. P. (1985) · Life Sciences · doi:10.1016/0024-3205(85)90546-6 · Cited by 80 · see citing works
Hashiguchi, H., Ye, S., Morris, M., et al. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00527-6 · Cited by 80 · see citing works
The Bidirectional Effects of Shock on Alcohol Preference in Rats
Volpicelli, J. R., Ulm, R. R., & Hopson, N. (1990) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1990.tb01837.x · Cited by 77 · see citing works
The effects of restraint stress on voluntary ethanol consumption in rats.
Lynch, W. J., Kushner, M. G., Rawleigh, J. M., Fiszdon, J. M., & Carroll, M. E. (1999) · Experimental and Clinical Psychopharmacology · doi:10.1037//1064-1297.7.4.318 · Cited by 76 · see citing works
Bertoglio, L. J., & Carobrez, A. P. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00958-9 · Cited by 74 · see citing works
Silveri, M. M., & SPEAR, L. P. (2002) · Alcoholism Clinical and Experimental Research · doi:10.1097/00000374-200204000-00003 · Cited by 68 · see citing works
Self-citationThe effects of restraint stress on voluntary ethanol consumption in rats.
Lynch, W. J., Kushner, M. G., Rawleigh, J. M., et al. (1999) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.7.4.318 · Cited by 65 · see citing works
Play behavior and stress responsivity in periadolescent offspring exposed prenatally to cocaine
Wood, R. D., Molina, V. A., Wagner, J. M., & SPEAR, L. P. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00120-l · Cited by 63 · see citing works
Self-citationSocial deprivation, housing density, and gregariousness in rats.
Latané, B., Cappell, H., & Joy, V. (1970) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0028742 · Cited by 60 · see citing works
Choi, S., & Kellogg, C. K. (1996) · Developmental Brain Research · doi:10.1016/s0165-3806(96)80005-8 · Cited by 59 · see citing works
Development of the circadian rhythm of body temperature in rats
Kittrell, E. M. W., & Satinoff, E. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90138-1 · Cited by 57 · see citing works
Influence of Age on Behavioural Response in the Light/Dark Paradigm
Hascoët, M., Colombel, M. C., & Bourin, M. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00333-3 · Cited by 45 · see citing works
Effects of continuous versus limited access to ethanol on ethanol self-administration
Files, F. J., Lewis, R. S., & Samson, H. H. (1994) · Alcohol · doi:10.1016/0741-8329(94)90079-5 · Cited by 37 · see citing works
Boyle, A. E., Smith, B. R., & Amit, Z. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90491-w · Cited by 31 · see citing works
Alcohol Self‐Administration in a Nonrestricted Access Situation with Alcohol‐Preferring (P) Rats
Files, F. J., Andrews, C. M., Samson, H. H., et al. (1992) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1992.tb00672.x · Cited by 28 · see citing works
RIVIER, C. L. (1995) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1995.tb01010.x · Cited by 24 · see citing works
Sprague, J. E., & Maickel, R. P. (1994) · Life Sciences · doi:10.1016/0024-3205(94)90043-4 · Cited by 20 · see citing works
Tolliver, G. A., & Samson, H. H. (1989) · Alcohol · doi:10.1016/0741-8329(89)90008-6 · Cited by 17 · see citing works
Development changes in sugar and starch taste preferences in young rats
Pérez, C., & Sclafani, A. J. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90252-y · Cited by 12 · see citing works
Effects of Ethanol on the Stress-Induced Expression of NGFI-A mRNA in the Rat Brain
Ueyama, T., Ohya, H., Yoshimura, R., & Senba, E. (1999) · Alcohol · doi:10.1016/s0741-8329(98)00081-0 · Cited by 10 · see citing works
Karanian, J. W., D'Souza, N. B., & Salem, N. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90185-2 · Cited by 10 · see citing works
Ethanol and nitrogen metabolism
Mezey, E. (1978) · Gastroenterology · doi:10.1016/0016-5085(78)90910-1 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.08.008 · Cited by 397 · see citing works
Self-citationFactors influencing elevated ethanol consumption in adolescent relative to adult rats
Doremus, T. L., Brunell, S. C., Rajendran, P., & Spear, L. P. (2005) · Alcoholism: Clinical & Experimental Research · doi:10.1097/01.alc.0000183007.65998.aa · Cited by 291 · see citing works
Self-citationAre adolescents more vulnerable to drug addiction than adults? Evidence from animal models
Schramm-Sapyta, N. L., Walker, Q. D., Caster, J. M., Levin, E. D., & Kuhn, C. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1585-5 · Cited by 215 · see citing works
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents
Logan, R. W., Hasler, B. P., Forbes, E. E., Franzen, P. L., Torregrossa, M. M., Huang, Y. H., Buysse, D. J., Clark, D. B., & McClung, C. A. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.11.035 · Cited by 194 · see citing works
The emergence of gonadal hormone influences on dopaminergic function during puberty
Kuhn, C., Johnson, M., Thomae, A., Luo, B., Simon, S. A., Zhou, G., & Walker, Q. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.10.015 · Cited by 113 · see citing works
Ethanol‐induced conditioned taste aversion in male Sprague‐Dawley rats: impact of age and stress
Anderson, R. I., Varlinskaya, E. I., & Spear, L. P. (2010) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01307.x · Cited by 96 · see citing works
Self-citationA psychobiological framework of the substrates that mediate nicotine use during adolescence
O'Dell, L. E. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.039 · Cited by 81 · see citing works
Chester, J. A., Barrenha, G. D., Hughes, M. L., & Keuneke, K. J. (2008) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00763.x · Cited by 54 · see citing works
Vetter-O’Hagen, C. S., & Spear, L. P. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01555.x · Cited by 55 · see citing works
Social interactions and 50kHz ultrasonic vocalizations in adolescent and adult rats
Willey, A. R., Varlinskaya, E. I., & Spear, L. P. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.03.025 · Cited by 52 · see citing works
Self-citationPerry, J. L., Anderson, M. M., Nelson, S. E., & Carroll, M. E. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.02.001 · Cited by 42 · see citing works
Adolescent and adult heart rate responses to self-administered ethanol
Ristuccia, R. C., & Spear, L. P. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00752.x · Cited by 35 · see citing works
Self-citationVarlinskaya, E. I., Truxell, E. M., & Spear, L. P. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.10.016 · Cited by 21 · see citing works
Self-citation
- Authors
- Brunell, S. C., & Spear, L. P.
- Affiliations
- Binghamton University (US)
- Corresponding author
- Spear, Linda P.
- ORCID
- Spear, Linda P.
- Venue
- Alcoholism Clinical and Experimental Research
- Publisher
- Wiley
- Published
- 2005-09
- Volume
- 29
- Issue
- 9
- Pages
- 1641-1653
- ISSN
- 0145-6008 (ISSN-L)
- OpenAlex
- W1977565766
- Cited by
- 128
- References
- 49
- Citations by year
- 2025: 1 · 2021: 1 · 2020: 4 · 2019: 5 · 2018: 6 · 2017: 3 · 2016: 7 · 2015: 1 · 2014: 6 · 2013: 9 · 2012: 7
- FWCI
- 4.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Alcoholism Clinical and Experimental Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Binghamton University
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
- Keywords
- ethanol consumption, stress, adolescence, pair housing, footshock, corticosterone, ethanol withdrawal, ethanol tolerance, saccharin, freezing behavior, ontogeny
- MeSH terms
- Age Factors, Alcohol Drinking, Animals, Body Temperature, Corticosterone, Freezing, Male, Saccharin, Stress, Psychological, Rats, Sprague-Dawley, Maze Learning, 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
