The DOI matches its Crossref record; 78 of the 78 references it cites were found in a registry or an index.
Opposite metabolic changes in the habenula and ventral tegmental area of a genetic model of helpless behavior
Abstract
Congenitally helpless rats have been selectively bred to display an immediate helpless response to stress in order to model hereditary brain differences that contribute to depression vulnerability. Differences in regional brain metabolism between congenitally helpless and non-helpless rats were investigated using quantitative cytochrome oxidase histochemistry. The results indicated that congenitally helpless rats had 64-71% elevated metabolism in the habenula and a 25% elevation in the related interpeduncular nucleus. In contrast, helpless rats had 28% reduced metabolism in the ventral tegmental area (VTA) and 14-16% reductions in the basal ganglia and basolateral and central amygdala. The opposite metabolic changes in the habenula and ventral tegmental area may be especially important for determining the congenitally helpless rat's global pattern of brain activity, which resembles the metabolic activity pattern produced by dopamine antagonism.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“The LHb is implicated in negative mood states in both animal and human research.”
From Deep brain stimulation for depression. (2022) · cites this paper as [41]
Citations
Cites
Psychopharmacology: The third generation of progress
O’Connell, R. A. (1988) · Comprehensive Psychiatry · doi:10.1016/0010-440x(88)90057-0 · Cited by 3,020
Psychopharmacology: The Third Generation of Progress.
(1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-108-3-509_2 · Cited by 2,021
Limbic-cortical dysregulation: a proposed model of depression
(1997) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/jnp.9.3.471 · Cited by 1,585
The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction.
Aggleton, J. P. (1992) · Wiley-Liss eBooks · Cited by 1,536
Neuroimaging studies of mood disorders
Drevets, W. C. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01020-9 · Cited by 1,334
The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction
Scheel-Krüger, J. (1993) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(93)90037-5 · Cited by 1,281
Cytochrome oxidase: an endogenous metabolic marker for neuronal activity
Wong-Riley, M. T. T. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90165-3 · Cited by 1,238
Drevets, W. C. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00203-8 · Cited by 1,146
Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems
EVERITT, B. J., PARKINSON, J. A., OLMSTEAD, M. C., ARROYO, M., ROBLEDO, P., & ROBBINS, T. W. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09280.x · Cited by 708
Swerdlow, N. R., & Koob, G. F. (1987) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00047488 · Cited by 674
Depression, intellectual impairment, and Parkinson disease
Mayeux, R. P., Stern, Y., Rosen, J. J., & Leventhal, J. (1981) · Neurology · doi:10.1212/wnl.31.6.645 · Cited by 571
Sutherland, R. J. (1982) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(82)90003-3 · Cited by 537
Videbech, P. (2000) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2000.101001011.x · Cited by 419
Christoph, G., Leonzio, R., & Wilcox, K. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-03-00613.1986 · Cited by 418
Physiological Evidence for Habenula as Major Link Between Forebrain and Midbrain Raphe
Wang, R. Y., & Aghajanian, G. K. (1977) · Science · doi:10.1126/science.194312 · Cited by 411
Zur Serotonin-Hypothese der Depression*
Lesch, K., & Beckmann, H. (1990) · Fortschritte der Neurologie · Psychiatrie · doi:10.1055/s-2007-1001206 · Cited by 392
Magnetic Resonance Imaging of the Caudate Nuclei in Depression: Preliminary Observations
Krishnan, K. R. R. (1992) · Archives of General Psychiatry · doi:10.1001/archpsyc.1992.01820070047007 · Cited by 365
Metabolic rate in the right amygdala predicts negative affect in depressed patients
Abercrombie, H. C., Schaefer, S. M., Larson, C. L., Oakes, T. R., Lindgren, K. A., Holden, J. E., Perlman, S. B., Turski, P. A., Krahn, D. D., Benca, R. M., et al. (1998) · Neuroreport · doi:10.1097/00001756-199810050-00028 · Cited by 316
Regional cerebral glucose utilization in patients with a range of severities of unipolar depression
Kimbrell, T. A., Ketter, T. A., George, M. S., Little, J. T., Benson, B. E., Willis, M. W., Herscovitch, P., & Post, R. M. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01216-1 · Cited by 303
Covariation of activity in habenula and dorsal raphe nuclei following tryptophan depletion
Morris, J. S., Smith, K. A., Cowen, P. J., Friston, K. J., & Dolan, R. J. (1999) · NeuroImage · doi:10.1006/nimg.1999.0455 · Cited by 288
Functional Magnetic Resonance Imaging of Brain Reward Circuitry in the Human
BREITER, H. C., & Rosen, B. R. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09287.x · Cited by 233
Caldecott-Hazard, S., Mazziotta, J. C., & Phelps, M. E. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-06-01951.1988 · Cited by 194
Amat, J., Sparks, P., Matus-Amat, P., Griggs, J., Watkins, L. R., & Maier, S. F. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02934-1 · Cited by 187
Dopaminergic abnormalities in amygdaloid nuclei in major depression: a postmortem study
Klimek, V., Schenck, J. E., Han, H., Stockmeier, C. A., & Ordway, G. A. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01383-5 · Cited by 181
Maswood, S., Barter, J. E., Watkins, L. R., & Maier, S. F. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01313-9 · Cited by 173
Nishikawa, T., Fage, D., & Scatton, B. (1986) · Brain Research · doi:10.1016/0006-8993(86)90347-1 · Cited by 166
Gonzalez-Lima, F., & Cada, A. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90550-9 · Cited by 163
Self-citationFrontostriatal deficits in unipolar major depression
Rogers, M. A., Bradshaw, J. L., Pantelis, C., & Phillips, J. G. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00126-9 · Cited by 150
Intellectual changes in patients with MPTP‐induced parkinsonism
Stern, Y., & Langston, J. W. (1985) · Neurology · doi:10.1212/wnl.35.10.1506 · Cited by 150
Kalén, P., Karlson, M., & Wiklund, L. (1985) · Brain Research · doi:10.1016/0006-8993(85)91244-2 · Cited by 148
Gonzalez-Lima, F., & Jones, D. (1994) · Brain Research · doi:10.1016/0006-8993(94)90836-2 · Cited by 145
Self-citationBrain Glucose Metabolism During Non—Rapid Eye Movement Sleep in Major Depression
Ho, A. P. (1996) · Archives of General Psychiatry · doi:10.1001/archpsyc.1996.01830070095014 · Cited by 131
Lisoprawski, A., Herve, D., Blanc, G., Glowinski, J., & Tassin, J. P. (1980) · Brain Research · doi:10.1016/0006-8993(80)90135-3 · Cited by 130
Prevention of learned helplessness: In vivo correlation with cortical serotonin
Petty, F., Kramer, G. L., & Wilson, L. B. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90163-a · Cited by 123
Gallistel, C. R., Gomita, Y., Yadin, E., & Campbell, K. J. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01246.1985 · Cited by 119
Metabolic Mapping of the Brain During Rewarding Self-Stimulation
Porrino, L. J., Esposito, R., Seeger, T., Crane, A. M., Pert, A., & Sokoloff, L. (1984) · Science · doi:10.1126/science.6710145 · Cited by 118
Cells of the rat lateral habenula respond to high-threshold somatosensory inputs
Benabid, A. L., & Jeaugey, L. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90393-5 · Cited by 94
Cytochrome Oxidase in Neuronal Metabolism and Alzheimer’s Disease
Gonzalez-Lima, F. (1998) · Springer eBooks · doi:10.1007/978-1-4757-9936-1 · Cited by 92
Self-citationHaun, F., Eckenrode, T. C., & Murray, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-08-03282.1992 · Cited by 91
Kozlowski, M. R., & Marshall, J. F. (1980) · Brain Research · doi:10.1016/0006-8993(80)90442-4 · Cited by 89
Valjakka, A., Vartiainen, J., Tuomisto, L. M., Tuomisto, J. T., Olkkonen, H., & Airaksinen, M. M. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00006-9 · Cited by 86
Quantitative histochemistry of cytochrome oxidase in rat brain
Gonzalez-Lima, F., & Garrosa, M. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90943-n · Cited by 83
Self-citationSelf-stimulation of the habenular complex in the rat.
Sutherland, R. J., & Nakajima, S. (1981) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077833 · Cited by 77
Ascending reticular activating system in the rat: A 2-deoxyglucose study
Gonzalez-Lima, F., & Scheich, H. (1985) · Brain Research · doi:10.1016/0006-8993(85)91190-4 · Cited by 76
Self-citationCytochrome Oxidase in Neuronal Metabolism and Alzheimer's Disease
Gonzalez-Lima, F. (2013) · Medical Entomology and Zoology · Cited by 74
Self-citationLee, E. H. Y., & Huang, S.-P. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90169-6 · Cited by 73
Relevance of the Habenular Complex to Neuropsychiatry: A Review and Hypothesis
Sandyk, R. (1991) · International Journal of Neuroscience · doi:10.3109/00207459108990738 · Cited by 70
Haloperidol and Cerebral Metabolism in the Conscious Rat: Relation to Pharmacokinetics
Pizzolato, G., Soncrant, T. T., & Rapoport, S. I. (1984) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1984.tb12792.x · Cited by 67
Congenital helpless rats as a genetic model for cortex metabolism in depression
Shumake, J., Poremba, A., Edwards, E., & Gonzalez-Lima, F. (2000) · Neuroreport · doi:10.1097/00001756-200011270-00040 · Cited by 65
Self-citationGenetic predisposition and the development of posttraumatic stress disorder in an animal model
King, J. A., Abend, S., & Edwards, E. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01071-x · Cited by 65
Self-citationNeurochemical and behavioral consequences of mild, uncontrollable shock: Effects of PCPA
Edwards, E., Johnson, J., Anderson, D. C., Turano, P., & Henn, F. A. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90018-3 · Cited by 58
Self-citationCada, A. M., Gonzalez-Lima, F., Rose, G. M., & Bennett, M. C. (1995) · Metabolic Brain Disease · doi:10.1007/bf02109361 · Cited by 58
Self-citationEarly Stress and Genetic Influences on Hypothalamic–Pituitary–Adrenal Axis Functioning in Adulthood
King, J. A., & Edwards, E. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1525 · Cited by 57
Self-citationKalén, P., Pritzel, M., Nieoullon, A. L., & Wiklund, L. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90225-9 · Cited by 57
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
Quantitative Histochemistry of Cytochrome Oxidase Activity
Gonzalez-Lima, F., & Cada, A. M. (1998) · Springer eBooks · doi:10.1007/978-1-4757-9936-1_2 · Cited by 53
Self-citationD1/D2 DOPAMINE RECEPTOR STIMULATION BY L-DOPA: A[14C]-2-DEOXYGLUCOSE AUTORADIOGRAPHIC STUDY
Trugman, J. M., JAMES, C. L., & Wooten, G. F. (1991) · Brain · doi:10.1093/brain/114.3.1429 · Cited by 50
Melancholia in rodents: neurobiology and pharmacology.
Henn, F. A., Johnson, J., Edwards, E., & Anderson, D. (1985) · PubMed · Cited by 49
Self-citationHammer, R. P., Pires, W. S., Markou, A., & Koob, G. F. (1993) · Synapse · doi:10.1002/syn.890140110 · Cited by 49
Dissociation of septo-hippocampal metabolism in the congenitally helpless rat
Shumake, J., Edwards, E., & Gonzalez-Lima, F. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00297-x · Cited by 48
Self-citationFirst and second order maternal behavior related afferents of the lateral habenula
Felton, T. M., Linton, L., Rosenblatt, J. S., & Morell, J. I. (1999) · Neuroreport · doi:10.1097/00001756-199903170-00039 · Cited by 48
(2001) · PubMed · Cited by 47
Hypermetabolism of paraventricular hypothalamus in the congenitally helpless rat
Shumake, J., Edwards, E., & Gonzalez-Lima, F. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)02142-5 · Cited by 41
Self-citationGenetic Studies in Affective Disorders
PAPOLOS, DEMITRI, F., LACHMAN, & HERBERT, M. (1995) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-199509000-00014 · Cited by 38
Habenular modulation of raphe indoleamine metabolism
Speciale, S. G., Neckers, L., & Wyatt, R. J. (1980) · Life Sciences · doi:10.1016/0024-3205(80)90506-8 · Cited by 35
Alterations in glucocorticoid inducible RNAs in the limbic system of learned helpless rats
Lachman, H. M., Papolos, D. F., Boyle, A., Sheftel, G., Juthani, M., Edwards, E., & Henn, F. A. (1993) · Brain Research · doi:10.1016/0006-8993(93)90862-h · Cited by 34
Self-citationGomita, Y., & Gallistel, C. R. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90369-0 · Cited by 34
Action of habenular efferents on ventral tegmental area neurons studied in vitro
Matsuda, Y., & Fujimura, K. (1992) · Brain Research Bulletin · doi:10.1016/0361-9230(92)90254-u · Cited by 33
Effects of methylenedioxymethamphetamine on local cerebral glucose utilization in the rat
Wilkerson, G., & London, E. D. (1989) · Neuropharmacology · doi:10.1016/0028-3908(89)90128-7 · Cited by 33
Effect size of efficacy measures comparing divalproex, lithium and placebo in acute mania
Bowden, C. L., Davis, J. M., Morris, D. D., Swann, A. C., Calabrese, J. R., Lambert, M., & Goodnick, P. J. (1997) · Depression and Anxiety · doi:10.1002/(sici)1520-6394(1997)6:1 · Cited by 31
Gonzalez-Lima, F., & Sadile, A. G. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00049-4 · Cited by 30
Self-citationLateral habenula and hippocampus: A complex interaction raphe cells-mediated
Ferraro, G., Montalbano, M. E., Sardo, P., & Grutta, V. L. (1997) · Journal of Neural Transmission · doi:10.1007/bf01291880 · Cited by 29
Habenula lesions attenuate lateral hypothalamic analgesia in the formalin test
Fuchs, P. N., & Cox, V. C. (1993) · Neuroreport · doi:10.1097/00001756-199302000-00001 · Cited by 26
Effect of some brain lesions on septal intracranial self-stimulation in the rat
Boyd, E., & Celso, M. (1970) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1970.219.3.734 · Cited by 19
Cytochrome Oxidase Atlas of Rat Brain
Gonzalez-Lima, F., & Cada, A. M. (1998) · Springer eBooks · doi:10.1007/978-1-4757-9936-1_10 · Cited by 16
Self-citationMelancholia as a Neurological Disorder
Austin, M., & Mitchell, P. (1996) · Cambridge University Press eBooks · doi:10.1017/cbo9780511759024.016 · Cited by 15
Dünner, D. L. (1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.6.948-a · Cited by 13
Effects of self-administered phencyclidine on regional uptake of 2-deoxy-d-[1-14C]glucose in brain
Weissman, A. D., Marquis, K. L., Moreton, J. E., & London, E. D. (1989) · Neuropharmacology · doi:10.1016/0028-3908(89)90136-6 · Cited by 10
Cited by
Sorted by citations
Ketamine blocks bursting in the lateral habenula to rapidly relieve depression
Yang, Y., Cui, Y., Sang, K., Dong, Y., Ni, Z., Ma, S., & Hu, H. (2018) · Nature · doi:10.1038/nature25509 · Cited by 1,036
The habenula: from stress evasion to value-based decision-making
Hikosaka, O. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2866 · Cited by 955
Sartorius, A., Kiening, K. L., Kirsch, P., von Gall, C. C., Haberkorn, U., Unterberg, A. W., Henn, F. A., & Meyer-Lindenberg, A. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.08.027 · Cited by 611
The neurobiology of depression and antidepressant action
Willner, P., Scheel-Krüger, J., & Belzung, C. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.12.007 · Cited by 519
Reward processing by the lateral habenula in normal and depressive behaviors
Proulx, C. D., Hikosaka, O., & Malinow, R. (2014) · Nature Neuroscience · doi:10.1038/nn.3779 · Cited by 461
Metadata
- Authors
- Shumake, J., Edwards, E., & Gonzalez-Lima, F.
- Affiliations
- The University of Texas at Austin (US)
- University of Maryland, Baltimore (US)
- Corresponding author
- Gonzalez-Lima, F.
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2003-02
- Volume
- 963
- Issue
- 1-2
- Pages
- 274-281
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W1999881677
- Cited by
- 232
- References
- 78
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 11 · 2023: 2 · 2022: 10 · 2021: 9 · 2020: 14 · 2019: 18 · 2018: 21 · 2017: 20 · 2016: 13 · 2015: 11 · 2014: 18 · 2013: 16 · 2012: 6
- FWCI
- 2.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (T32MH18837, T32MH018837)
- National Institute of Neurological Disorders and Stroke (R01NS037755, R01 NS-37755)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pharmacology (medical) › Treatment of Major Depression
- Keywords
- brain regional metabolism, habenula, ventral tegmental area, interpeduncular nucleus, amygdala, basal ganglia, depression vulnerability, stress response, dopamine antagonism, cytochrome oxidase histochemistry
- MeSH terms
- Animals, Basal Ganglia, Behavior, Animal, Electron Transport Complex IV, Histocytochemistry, Male, Phenotype, Stress, Psychological, Rats, Sprague-Dawley, Ventral Tegmental Area, Habenula, 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