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.
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The lateral habenula is implicated in negative mood states in both animal and human research.
“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]
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 · see citing works
Psychopharmacology: The Third Generation of Progress.
(1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-108-3-509_2 · Cited by 2,021 · see citing works
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 · see citing works
The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction.
Aggleton, J. P. (1992) · Wiley-Liss eBooks · Cited by 1,536 · see citing works
Neuroimaging studies of mood disorders
Drevets, W. C. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01020-9 · Cited by 1,313 · see citing works
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 1,277 · see citing works
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 · see citing works
Drevets, W. C. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00203-8 · Cited by 1,146 · see citing works
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 · see citing works
Swerdlow, N. R., & Koob, G. F. (1987) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00047488 · Cited by 674 · see citing works
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 · see citing works
Sutherland, R. J. (1982) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(82)90003-3 · Cited by 537 · see citing works
Videbech, P. (2000) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2000.101001011.x · Cited by 419 · see citing works
Christoph, G., Leonzio, R., & Wilcox, K. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-03-00613.1986 · Cited by 418 · see citing works
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 · see citing works
Zur Serotonin-Hypothese der Depression*
Lesch, K., & Beckmann, H. (1990) · Fortschritte der Neurologie · Psychiatrie · doi:10.1055/s-2007-1001206 · Cited by 392 · see citing works
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 · see citing works
Metabolic rate in the right amygdala predicts negative affect in depressed patients
Abercrombie, H., Schaefer, S., Larson, C., Oakes, T., Lindgren, K. A., Holden, J., Perlman, S. B., Turski, P., Krahn, D., Benca, R., et al. (1998) · NeuroReport · doi:10.1097/00001756-199810050-00028 · Cited by 345 · see citing works
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 300 · see citing works
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 · see citing works
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 231 · see citing works
Caldecott-Hazard, S., Mazziotta, J. C., & Phelps, M. E. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-06-01951.1988 · Cited by 194 · see citing works
Are SSRIs better than TCAs? Comparison of SSRIs and TCAs: A meta-analysis
Steffens, D. C., Krishnan, K. R., & Helms, M. J. (1997) · Depression and Anxiety · doi:10.1002/(sici)1520-6394(1997)6:1 · Cited by 194 · see citing works
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 · see citing works
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 176 · see citing works
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 · see citing works
Nishikawa, T., Fage, D., & Scatton, B. (1986) · Brain Research · doi:10.1016/0006-8993(86)90347-1 · Cited by 166 · see citing works
Gonzalez-Lima, F., & Cada, A. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90550-9 · Cited by 163 · see citing works
Self-citationIntellectual changes in patients with MPTP‐induced parkinsonism
Stern, Y., & Langston, J. W. (1985) · Neurology · doi:10.1212/wnl.35.10.1506 · Cited by 150 · see citing works
Kalén, P., Karlson, M., & Wiklund, L. (1985) · Brain Research · doi:10.1016/0006-8993(85)91244-2 · Cited by 148 · see citing works
Frontostriatal 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 147 · see citing works
Gonzalez-Lima, F., & Jones, D. (1994) · Brain Research · doi:10.1016/0006-8993(94)90836-2 · Cited by 145 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationHaun, F., Eckenrode, T. C., & Murray, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-08-03282.1992 · Cited by 91 · see citing works
Kozlowski, M. R., & Marshall, J. F. (1980) · Brain Research · doi:10.1016/0006-8993(80)90442-4 · Cited by 89 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationCytochrome Oxidase in Neuronal Metabolism and Alzheimer's Disease
Gonzalez-Lima, F. (2013) · Medical Entomology and Zoology · Cited by 74 · see citing works
Self-citationLee, E. H. Y., & Huang, S.-P. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90169-6 · Cited by 73 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationCada, A. M., Gonzalez-Lima, F., Rose, G. M., & Bennett, M. C. (1995) · Metabolic Brain Disease · doi:10.1007/bf02109361 · Cited by 58 · see citing works
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 · see citing works
Self-citationKalén, P., Pritzel, M., Nieoullon, A. L., & Wiklund, L. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90225-9 · Cited by 57 · 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
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 · see citing works
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 · see citing works
Melancholia in rodents: neurobiology and pharmacology.
Henn, F. A., Johnson, J., Edwards, E., & Anderson, D. (1985) · PubMed · Cited by 49 · see citing works
Self-citationHammer, R. P., Pires, W. S., Markou, A., & Koob, G. F. (1993) · Synapse · doi:10.1002/syn.890140110 · Cited by 49 · see citing works
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 · see citing works
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 · see citing works
(2001) · PubMed · Cited by 47 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationGomita, Y., & Gallistel, C. R. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90369-0 · Cited by 34 · see citing works
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 · see citing works
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 · see citing works
Gonzalez-Lima, F., & Sadile, A. G. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00049-4 · Cited by 30 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationMelancholia as a Neurological Disorder
Austin, M., & Mitchell, P. (1996) · Cambridge University Press eBooks · doi:10.1017/cbo9780511759024.016 · Cited by 15 · see citing works
Dünner, D. L. (1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.6.948-a · Cited by 13 · see citing works
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 · see citing works
Flagged first, then by citations
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 · see citing works
The habenula: from stress evasion to value-based decision-making
Hikosaka, O. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2866 · Cited by 955 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
βCaMKII in Lateral Habenula Mediates Core Symptoms of Depression
Li, K., Zhou, T., Liao, L., Yang, Z., Wong, C., Henn, F., Malinow, R., Yates, J. R., & Hu, H. (2013) · Science · doi:10.1126/science.1240729 · Cited by 411 · see citing works
Eisch, A. J., Bolaños, C. A., de Wit, J., Simonak, R. D., Pudiak, C. M., Barrot, M., Verhaagen, J., & Nestler, E. J. (2003) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.08.003 · Cited by 420 · see citing works
GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment
Shabel, S. J., Proulx, C. D., Piriz, J., & Malinow, R. (2014) · Science · doi:10.1126/science.1250469 · Cited by 369 · see citing works
Andrews, P. W., Bharwani, A., Lee, K. R., Fox, M., & Thomson, J. A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.018 · Cited by 281 · see citing works
Stress models of depression: forming genetically vulnerable strains
Henn, F. A., & Vollmayr, B. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.019 · Cited by 274 · see citing works
Lateral habenula in the pathophysiology of depression
Yang, Y., Wang, H., Hu, J., & Hu, H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.024 · Cited by 254 · see citing works
Neuronal Dynamics Regulating Brain and Behavioral State Transitions
Andalman, A. S., Burns, V. M., Lovett-Barron, M., Broxton, M. J., Poole, B., Yang, S., Grosenick, L., Lerner, T. N., Chen, R., Benster, T., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.037 · Cited by 246 · see citing works
Hu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253 · see citing works
Alcaro, A., & Panksepp, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.002 · Cited by 240 · see citing works
Yang, L.-M., Hu, B., Xia, Y.-H., Zhang, B.-L., & Zhao, H. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.022 · Cited by 236 · see citing works
Northoff, G., Wiebking, C., Feinberg, T., & Panksepp, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.007 · Cited by 222 · see citing works
McLaughlin, I., Dani, J. A., & Biasi, M. D. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14008 · Cited by 230 · see citing works
Deep brain stimulation for treatment-resistant depression: systematic review of clinical outcomes
Morishita, T., Fayad, S. M., Higuchi, M.-A., Nestor, K. A., & Foote, K. D. (2014) · Neurotherapeutics · doi:10.1007/s13311-014-0282-1 · Cited by 216 · see citing works
Dillon, D. G., Rosso, I. M., Pechtel, P., Killgore, W. D. S., Rauch, S. L., & Pizzagalli, D. A. (2014) · Depression and Anxiety · doi:10.1002/da.22202 · Cited by 209 · see citing works
Sustained antidepressant effect of ketamine through NMDAR trapping in the LHb
Ma, S., Chen, M., Jiang, Y., Xiang, X., Wang, S., Wu, Z., Li, S., Cui, Y., Wang, J., Zhu, Y., et al. (2023) · Nature · doi:10.1038/s41586-023-06624-1 · Cited by 213 · see citing works
Vadnie, C. A., & McClung, C. A. (2017) · Neural Plasticity · doi:10.1155/2017/1504507 · Cited by 199 · see citing works
The lateral habenula in addiction and depression: an anatomical, synaptic and behavioral overview
Lecca, S., Meye, F. J., & Mameli, M. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12480 · Cited by 196 · see citing works
Cerniauskas, I., Winterer, J., de Jong, J. W., Lukacsovich, D., Yang, H., Khan, F., Peck, J. R., Obayashi, S. K., Lilascharoen, V., Lim, B. K., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.005 · Cited by 187 · see citing works
Savitz, J. B., Nugent, A. C., Bogers, W., Roiser, J. P., Bain, E., Neumeister, A., Zarate, C. A., Manji, H. K., Cannon, D. M., Marrett, S., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.027 · Cited by 182 · see citing works
Ranft, K., Dobrowolny, H., Krell, D., Bielau, H., Bogerts, B., & Bernstein, H.-G. (2010) · Psychological Medicine · doi:10.1017/s0033291709990821 · Cited by 183 · see citing works
Lecca, S., Pelosi, A., Tchenio, A., Moutkine, I., Lujan, R., Hervé, D., & Mameli, M. (2016) · Nature Medicine · doi:10.1038/nm.4037 · Cited by 176 · see citing works
Deep brain stimulation for depression.
Figee, M., Riva-Posse, P., Choi, K. S., Bederson, L., Mayberg, H. S., & Kopell, B. H. (2022) · Neurotherapeutics · doi:10.1007/s13311-022-01270-3 · Cited by 175 · see citing works
Carlson, P. J., Diazgranados, N., Nugent, A. C., Ibrahim, L., Luckenbaugh, D. A., Brutsche, N., Herscovitch, P., Manji, H. K., Zarate, C. A., & Drevets, W. C. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.02.008 · Cited by 168 · see citing works
Translating the habenula-from rodents to humans
Boulos, L.-J., Darcq, E., & Kieffer, B. L. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.06.003 · Cited by 164 · see citing works
Learned helplessness: unique features and translational value of a cognitive depression model
Vollmayr, B., & Gass, P. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1654-2 · Cited by 155 · see citing works
Habenular and interpeduncularis nuclei: shared components in multiple-function networks.
Klemm, W. R. (2004) · PubMed · Cited by 153 · see citing works
Winter, C., Vollmayr, B., Djodari-Irani, A., Klein, J., & Sartorius, A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.07.034 · Cited by 145 · see citing works
The Lateral Habenula:No Longer Neglected
Geisler, S., & Trimble, M. (2008) · CNS Spectrums · doi:10.1017/s1092852900016710 · Cited by 149 · see citing works
Zhao, H., Zhang, B., Yang, S., & Rusak, B. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.016 · Cited by 147 · see citing works
Okamoto, H., Agetsuma, M., & Aizawa, H. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20913 · Cited by 142 · see citing works
Negative learning bias is associated with risk aversion in a genetic animal model of depression
Shabel, S. J., Murphy, R. T., & Malinow, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00001 · Cited by 148 · see citing works
Alcaro, A., Panksepp, J., Witczak, J., Hayes, D. J., & Northoff, G. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.11.023 · Cited by 144 · see citing works
Learning shapes the aversion and reward responses of lateral habenula neurons
Wang, D., Li, Y., Feng, Q., Guo, Q., Zhou, J., & Luo, M. (2017) · eLife · doi:10.7554/elife.23045 · Cited by 141 · see citing works
Brain Systems Underlying Susceptibility to Helplessness and Depression
Shumake, J., & Gonzalez-Lima, F. (2003) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582303259057 · Cited by 135 · see citing works
Self-citationGonçalves, L., Sego, C., & Metzger, M. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22787 · Cited by 134 · see citing works
Kim, U., & Lee, T. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08030.x · Cited by 133 · see citing works
The medial habenula: still neglected
Viswanath, H., Carter, A. Q., Baldwin, P. R., Molfese, D. L., & Salas, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00931 · Cited by 141 · see citing works
Sego, C., Gonçalves, L., Lima, L. B., Furigo, I. C., Donato, J., & Metzger, M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23533 · Cited by 126 · see citing works
The Effects of Tryptophan Depletion on Neural Responses to Emotional Words in Remitted Depression
Roiser, J. P., Levy, J., Fromm, S. J., Nugent, A. C., Talagala, S. L., Hasler, G., Henn, F. A., Sahakian, B. J., & Drevets, W. C. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.05.002 · Cited by 123 · see citing works
Neurobiological Mechanisms of Nicotine Reward and Aversion
Wills, L. P., Ables, J. L., Braunscheidel, K. M., Caligiuri, S. P. B., Elayouby, K. S., Fillinger, C., Ishikawa, M., Moen, J. K., & Kenny, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000299 · Cited by 132 · see citing works
Genetics and genomics of depression
Hamet, P., & Tremblay, J. (2005) · Metabolism · doi:10.1016/j.metabol.2005.01.006 · Cited by 110 · see citing works
Depression, Olfaction, and Quality of Life: A Mutual Relationship
Rochet, M., el-Hage, W., Richa, S., Kazour, F., & Atanasova, B. (2018) · Brain Science · doi:10.3390/brainsci8050080 · Cited by 104 · see citing works
Shumake, J., Barrett, D. W., & Gonzalez-Lima, F. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.016 · Cited by 107 · see citing works
Self-citationThe role of the habenula in the transition from reward to misery in substance use and mood disorders
Batalla, A., Homberg, J. R., Lipina, T. V., Sescousse, G., Luijten, M., Ivanova, S. А., Schellekens, A., & LOONEN, A. J. M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.019 · Cited by 100 · see citing works
Weiss, T., & Veh, R. W. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.047 · Cited by 100 · see citing works
Deep brain stimulation for psychiatric disorders: where we are now
Cleary, D. R., Ozpinar, A., Raslan, A. M. T., & Ko, A. L. (2015) · Neurosurgical FOCUS · doi:10.3171/2015.3.focus1546 · Cited by 99 · see citing works
Dysregulation of the Lateral Habenula in Major Depressive Disorder
Browne, C. A., Hammack, R. J., & Lucki, I. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00046 · Cited by 93 · see citing works
The habenula in psychiatric disorders: More than three decades of translational investigation
Fakhoury, M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.010 · Cited by 90 · see citing works
Striatal structure and function in mood disorders: a comprehensive review
Marchand, W. R., & Yurgelun‐Todd, D. (2010) · Bipolar Disorders · doi:10.1111/j.1399-5618.2010.00874.x · Cited by 91 · see citing works
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 91 · see citing works
Topographic commissural and descending projections of the habenula in the rat
Kim, U. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.21951 · Cited by 85 · see citing works
Mirrione, M. M., Schulz, D., Lapidus, K. A. B., Zhang, S., Goodman, W. K., & Henn, F. A. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00029 · Cited by 86 · see citing works
Role of the Lateral Habenula in Pain-Associated Depression
Li, Y., Wang, Y., Xuan, C., Li, Y., Piao, L., Li, J., & Zhao, H. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00031 · Cited by 85 · see citing works
The lateral habenula and the serotonergic system
Metzger, M., Bueno, D., & Lima, L. B. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.05.007 · Cited by 81 · see citing works
Shumake, J., Ilango, A., Scheich, H., Wetzel, W., & Ohl, F. W. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3604-09.2010 · Cited by 82 · see citing works
Self-citationBrain glucose metabolism in an animal model of depression
Detka, J., Kurek, A., Kucharczyk, M. W., Głombik, K., Basta‐Kaim, A., Kubera, M., Lasoń, W., & Budziszewska, B. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.046 · Cited by 86 · see citing works
Hyperactivation of the habenula as a link between depression and sleep disturbance
Aizawa, H., Cui, W., Tanaka, K., & Okamoto, H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00826 · Cited by 81 · see citing works
Lima, L. B., Bueno, D., Leite, F., Souza, S., Gonçalves, L., Furigo, I. C., Donato, J., & Metzger, M. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24217 · Cited by 80 · see citing works
GPR3 Receptor, a Novel Actor in the Emotional-Like Responses
Valverde, O., Célèrier, E., Baranyi, M., Vanderhaeghen, P., Maldonado, R. J., Sperlágh, B., Vassart, G., & Ledent, C. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004704 · Cited by 78 · see citing works
Elevation of p11 in lateral habenula mediates depression-like behavior
Seo, J.-S., Zhong, P., Liu, A., Yan, Z., & Greengard, P. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.96 · Cited by 77 · see citing works
Altered brain network modules induce helplessness in major depressive disorder
Peng, D., Shi, F., Shen, T., Peng, Z., Zhang, C., Liu, X., Qiu, M., Liu, J., Jiang, K., Fang, Y., et al. (2014) · Journal of Affective Disorders · doi:10.1016/j.jad.2014.05.061 · Cited by 76 · see citing works
Metzger, M., Souza, R., Lima, L. B., Bueno, D., Gonçalves, L., Sego, C., Donato, J., & Shammah‐Lagnado, S. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14647 · Cited by 77 · see citing works
Mällo, T., Matrov, D., Kõiv, K., & Harro, J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.041 · Cited by 74 · see citing works
Li, J., Kang, S., Fu, R., Wu, L., Wu, W., Liu, H., Gregor, D. M., Zuo, W., Bekker, A., & Ye, J.-H. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.08.035 · Cited by 73 · see citing works
Behavioral correlates of differences in neural metabolic capacity
Sakata, J. T., Crews, D., & Gonzalez-Lima, F. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.07.017 · Cited by 73 · see citing works
Self-citationZhang, S., Zhang, H., Ku, S. M., Juarez, B., Morel, C., Tzavaras, N., Montgomery, S. E., Hodes, G. E., Brancato, A., Russo, S. J., et al. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.02.021 · Cited by 70 · see citing works
Kanarik, M., O’Leary, A., Matrov, D., Kõiv, K., Sharp, T., Panksepp, J., & Harro, J. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2010.06.015 · Cited by 71 · see citing works
Habenular Kiss1 Neurons Modulate the Serotonergic System in the Brain of Zebrafish
Ogawa, S., Ng, K. W., Ramadasan, P. N., Nathan, F. M., & Parhar, I. S. (2012) · Endocrinology · doi:10.1210/en.2012-1062 · Cited by 66 · see citing works
Berger, A. L., Henricks, A. M., Lugo, J. M., Wright, H. R., Warrick, C. R., Sticht, M. A., Morena, M., Río, I. B., Laredo, S. A., Craft, R. M., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.04.018 · Cited by 66 · see citing works
Beyond depression: Toward a process‐based approach to research, diagnosis, and treatment.
Forgeard, M. J. C., Haigh, E. A. P., Beck, A. T., Davidson, R. J., Henn, F. A., Maier, S. F., Mayberg, H. S., & Seligman, M. E. P. (2011) · Clinical Psychology Science and Practice · doi:10.1111/j.1468-2850.2011.01259.x · Cited by 63 · see citing works
Why depression and pain often coexist and mutually reinforce: Role of the lateral habenula
Li, J., Li, Y., Zhang, B., Shen, X., & Zhao, H. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.08.010 · Cited by 63 · see citing works
An emerging role for the lateral habenula in aggressive behavior
Flanigan, M. E., Aleyasin, H., Takahashi, A., Golden, S. A., & Russo, S. J. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.05.003 · Cited by 61 · see citing works
Han, L., Zhang, L., Li, L., Sun, Y., Wang, Y., Chen, L., Guo, Y., Zhang, Y., Zhang, Q.-J., & Liu, J. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.01.024 · Cited by 62 · see citing works
Xu, C., Sun, Y., Cai, X., You, T., Zhao, H., Li, Y., & Zhao, H. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00238 · Cited by 62 · see citing works
Benarroch, E. E. (2015) · Neurology · doi:10.1212/wnl.0000000000001937 · Cited by 58 · see citing works
Harro, J. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.11.006 · Cited by 59 · see citing works
Kowski, A. B., Geisler, S., Krauss, M. I., & Veh, R. W. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21610 · Cited by 58 · see citing works
Functional integrity of the habenula is necessary for social play behaviour in rats
van Kerkhof, L. W. M., Damsteegt, R., Trezza, V., Voorn, P., & Vanderschuren, L. J. M. J. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12353 · Cited by 56 · see citing works
Brain differences in newborn rats predisposed to helpless and depressive behavior
Shumake, J., Conejo, N. M., González‐Pardo, H., & Gonzalez-Lima, F. (2004) · Brain Research · doi:10.1016/j.brainres.2004.10.015 · Cited by 57 · see citing works
Self-citationPuryear, C. B., Brooks, J. M., Tan, L. A., Smith, K. L., Li, Y., Cunningham, J. I., Todtenkopf, M. S., Dean, R. L., & Sánchez, C. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.007 · Cited by 56 · see citing works
Furman, D. J., & Gotlib, I. H. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw019 · Cited by 53 · see citing works
Millan, M. J., Brocco, M., Papp, M., Serres, F., Rochelle, C. D. L., Sharp, T., Péglion, J.-L., & Dekeyne, A. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.062463 · Cited by 53 · see citing works
Jeon, S. G., Yoo, A., Chun, D. W., Hong, S. B., Chung, H., Kim, J.-I., & Moon, M. (2020) · Aging and Disease · doi:10.14336/ad.2019.0718 · Cited by 55 · see citing works
The neurophysiology of ketamine: an integrative review
McMillan, R. L., & Muthukumaraswamy, S. D. (2020) · Reviews in the Neurosciences · doi:10.1515/revneuro-2019-0090 · Cited by 49 · see citing works
González‐Pardo, H., Conejo, N. M., Lana, G., & Arias, J. L. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.064 · Cited by 50 · see citing works
Classifying suicidal behavior with resting-state functional connectivity and structural neuroimaging
Gosnell, S. N., Fowler, J. C., & Salas, R. (2019) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.13029 · Cited by 49 · see citing works
Sourani, D., Eitan, R., Gordon, N., & Goelman, G. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08200.x · Cited by 51 · see citing works
A Sex-Specific Role of Type VII Adenylyl Cyclase in Depression
Hines, L. M., Hoffman, P. L., Bhave, S. V., Saba, L. M., Kaiser, A., Snell, L. D., Goncharov, I., Legault, L., Dongier, M., Grant, B. F., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1040-06.2006 · Cited by 50 · see citing works
5HT1B receptor-mediated pre-synaptic depression of excitatory inputs to the rat lateral habenula
Hwang, E.-K., & Chung, J.-M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.046 · Cited by 46 · see citing works
Zuo, W., Zhang, Y., Xie, G., Gregor, D. M., Bekker, A., & Ye, J.-H. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.10.012 · Cited by 45 · see citing works
Harro, J., Kanarik, M., Matrov, D., & Panksepp, J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.02.016 · Cited by 45 · see citing works
Luo, X., Zhang, B. L., Li, J. C., Yang, Y., Sun, Y., & Zhao, H. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.11.006 · Cited by 42 · see citing works
Wang, T., Zhang, L., Zhang, Q.-J., Wang, Y., Du, C., Sun, Y., Zhang, J., Lv, S.-X., Chen, L., & Liu, J. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.015 · Cited by 42 · see citing works
Deep Brain Stimulation of the Lateral Habenular Complex in Treatment-Resistant Depression
Schneider, T. M., Beynon, C., Sartorius, A., Unterberg, A. W., & Kiening, K. L. (2012) · Operative Neurosurgery · doi:10.1227/neu.0b013e318277a5aa · Cited by 40 · see citing works
Fear and Anxiety Regulation by Conserved Affective Circuits
Okamoto, H., & Aizawa, H. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.031 · Cited by 38 · see citing works
- 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 › 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
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