Lesions of the lateral habenula produce anxiolytic effects in a rat model of Parkinson’s disease

References

• Prediger RDS, Matheus FC, Schwarzbold ML, et al. Anxiety in Parkinson’s disease: a critical review of experimental and clinical studies. Neuropharmacology. 2012;62(1):115–124.
   PubMed Web of Science ®Google Scholar
• Schapira AHV, Chaudhuri KR, Jenner P. Non-motor features of Parkinson disease. Nat Rev Neurosci. 2017;18(7):435–450.
   PubMed Web of Science ®Google Scholar
• Eskow Jaunarajs KL, Dupre KB, Ostock CY, et al. Behavioral and neurochemical effects of chronic L-DOPA treatment on non-motor sequelae in the hemiparkinsonian rat. Behav Pharmacol. 2010;21(7):627–637.
   PubMed Web of Science ®Google Scholar
• Jungnickel J, Kalve I, Reimers L, et al. Topology of intrastriatal dopaminergic grafts determines functional and emotional outcome in neurotoxin-lesioned rats. Behav Brain Res. 2011;216(1):129–135.
   PubMed Web of Science ®Google Scholar
• Hui YP, Wang T, Han LN, et al. Anxiolytic effects of prelimbic 5-HT1A receptor activation in the hemiparkinsonian rat. Behav Brain Res. 2015;277:211–220.
   PubMed Web of Science ®Google Scholar
• Sun YN, Wang T, Wang Y, et al. Activation of 5-HT1A receptors in the medial subdivision of the central nucleus of the amygdala produces anxiolytic effects in a rat model of Parkinson’s disease. Neuropharmacology. 2015;95:181–191.
   PubMed Web of Science ®Google Scholar
• Sun YN, Yao L, Li LB, et al. Activation and blockade of basolateral amygdala 5-HT6 receptor produce anxiolytic-like behaviors in an experimental model of Parkinson’s disease. Neuropharmacology. 2018;137:275–285.
   PubMed Web of Science ®Google Scholar
• Kiss J, Csaki A, Bokor H, et al. Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [(3)H]D-aspartate labelling and immunocytochemistry. Neuroscience. 2002;111(3):671–691.
   PubMed Web of Science ®Google Scholar
• Zahm DS, Root DH. Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving. Pharmacol Biochem Behav. 2017;162:3–21.
   PubMed Web of Science ®Google Scholar
• Lecourtier L, Kelly PH. A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci Biobehav Rev. 2007;31(5):658–672.
   PubMed Web of Science ®Google Scholar
• Lecca S, Meye FJ, Mameli M. The lateral habenula in addiction and depression: an anatomical, synaptic and behavioral overview. Eur J Neurosci. 2014;39(7):1170–1178.
   PubMed Web of Science ®Google Scholar
• Pobbe RL, Jr ZH. Involvement of the lateral habenula in the regulation of generalized anxiety- and panic-related defensive responses in rats. Life Sci. 2008;82(25–26):1256–1261.
   PubMed Web of Science ®Google Scholar
• Dolzani SD, Baratta MV, Amat J, et al. Activation of a habenulo-raphe circuit is critical for the behavioral and neurochemical consequences of uncontrollable stress in the male rat. eNeuro. 2016;3(5):ENEURO.0229–16.2016.
   PubMed Web of Science ®Google Scholar
• Kang S, Li J, Zuo W, et al. Ethanol withdrawal drives anxiety-related behaviors by reducing m-type potassium channel activity in the lateral habenula. Neuropsychopharmacology. 2017;42(9):1813–1824.
   PubMed Web of Science ®Google Scholar
• Gill MJ, Ghee SM, Harper SM, et al. Inactivation of the lateral habenula reduces anxiogenic behavior and cocaine seeking under conditions of heightened stress. Pharmacol Biochem Behav. 2013;111:24–29.
   PubMed Web of Science ®Google Scholar
• Wang T, Zhang L, Zhang QJ, et al. Involvement of lateral habenula α1 subunit-containing GABAA receptor-mediated inhibitory transmission in the regulation of depression-related behaviors in experimental Parkinson’s disease. Neuropharmacology. 2017;116:399–411.
   PubMed Web of Science ®Google Scholar
• Zhang J, Lv SX, Tang GY, et al. Activation of calcium-impermeable GluR2-containing AMPA receptors in the lateral habenula produces antidepressant-like effects in a rodent model of Parkinson’s disease. Exp Neurol. 2019;322:113058.
   PubMed Web of Science ®Google Scholar
• Zhang J, Wang Y, Sun YN, et al. Blockade of calcium-permeable AMPA receptors in the lateral habenula produces increased antidepressant-like effects in unilateral 6-hydroxydopamine-lesioned rats compared to sham-lesioned rats. Neuropharmacology. 2019;157:107687.
   PubMed Web of Science ®Google Scholar
• Marsh L. Neuropsychiatric aspects of Parkinson’s disease. Psychosomatics. 2000;41(1):15–23.
   PubMed Web of Science ®Google Scholar
• Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 4th ed. New York: Academic Press; 2004.
   Google Scholar
• Sourani D, Eitan R, Gordon N, et al. The habenula couples the dopaminergic and the serotonergic systems: application to depression in Parkinson’s disease. Eur J Neurosci. 2012;36(6):2822–2829.
   PubMed Web of Science ®Google Scholar
• Belzung C, Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res. 2001;125(1–2):141–149.
   PubMed Web of Science ®Google Scholar
• Seibenhener ML, Wooten MC. Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp. 2015;96:e52434. DOI:https://doi.org/10.3791/52434
   PubMed Web of Science ®Google Scholar
• Carola V, D’Olimpio F, Brunamonti E, et al. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res. 2002;134(1–2):49–57.
   PubMed Web of Science ®Google Scholar
• Bourin M. Experimental anxiety model for anxiety disorders: relevance to drug discovery. Adv Exp Med Biol. 2020;1191:169–184.
   PubMed Web of Science ®Google Scholar
• Han LN, Zhang L, Li LB, et al. Activation of serotonin2C receptors in the lateral habenular nucleus increases the expression of depression-related behaviors in the hemiparkinsonian rat. Neuropharmacology. 2015;93:68–79.
   PubMed Web of Science ®Google Scholar
• Luo XF, Zhang BL, Li JC, et al. Lateral habenula as a link between dopaminergic and serotonergic systems contributes to depressive symptoms in Parkinson’s disease. Brain Res Bull. 2015;110:40–46.
   PubMed Web of Science ®Google Scholar
• Carvalho MM, Campos FL, Coimbra B, et al. Behavioral characterization of the 6-hydroxidopamine model of Parkinson’s disease and pharmacological rescuing of non-motor deficits. Mol Neurodegener. 2013;8(1):14.
   PubMed Web of Science ®Google Scholar
• Delaville C, Chetrit J, Abdallah K, et al. Emerging dysfunctions consequent to combined monoaminergic depletions in Parkinsonism. Neurobiol Dis. 2012;45(2):763–773.
   PubMed Web of Science ®Google Scholar
• Metzger M, Bueno D, Lima LB. The lateral habenula and the serotonergic system. Pharmacol Biochem Behav. 2017;162:22–28.
   PubMed Web of Science ®Google Scholar
• Petzel A, Bernard R, Poller WC, et al. Anterior and posterior parts of the rat ventral tegmental area and the rostromedial tegmental nucleus receive topographically distinct afferents from the lateral habenular complex. J Comp Neurol. 2017;525(10):2310–2327.
   PubMed Web of Science ®Google Scholar
• Jhou TC, Geisler S, Marinelli M, et al. The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol. 2009;513(6):566–596.
   PubMed Web of Science ®Google Scholar
• Christoph GR, Leonzio RJ, Wilcox KS. Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci. 1986;6(3):613–619.
   PubMed Web of Science ®Google Scholar
• Matsumoto M, Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature. 2007;447(7148):1111–1115.
   PubMed Web of Science ®Google Scholar
• Wang RY, Aghajanian GK. Physiological evidence for habenula as major link between forebrain and midbrain raphe. Science. 1977;197(4298):89–91. 1977.
   PubMed Web of Science ®Google Scholar
• Nestler EJ, Barrot M, DiLeone RJ, et al. Neurobiology of depression. Neuron. 2002;34(1):13–25.
   PubMed Web of Science ®Google Scholar
• Berton O, Nestler EJ. New approaches to antidepressant drug discovery: beyond monoamines. Nat Rev Neurosci. 2006;7(2):137–151.
   PubMed Web of Science ®Google Scholar
• Hale MW, Bouwknecht JA, Spiga F, et al. Exposure to high- and low-light conditions in an open-field test of anxiety increases c-Fos expression in specific subdivisions of the rat basolateral amygdaloid complex. Brain Res Bull. 2006;71(1–3):174–182.
   PubMed Web of Science ®Google Scholar
• Du CX, Guo Y, Zhang QJ, et al. Involvement of prelimbic 5-HT7 receptors in the regulation of anxiety-like behaviors in hemiparkinsonian rats. Neurological Res. 2018;40(10):847–855.
   PubMed Web of Science ®Google Scholar
• Liu KC, Guo Y, Zhang J, et al. Activation and blockade of dorsal hippocampal serotonin 6 receptors regulate anxiety-like behaviors in a unilateral 6-hydroxydopamine rat model of Parkinson’s disease. Neurological Res. 2019;41(9):791–801.
   PubMed Web of Science ®Google Scholar
• Benke T, Bösch S, Andree B. A study of emotional processing in Parkinson’s disease. Brain Cogn. 1998;38(1):36e52.
   Web of Science ®Google Scholar
• Tessitore A, Hariri AR, Fera F, et al. Dopamine modulates the response of the human amygdala: a study in Parkinson’s disease. J Neurosci. 2002;22(20):9099e9103.
   Web of Science ®Google Scholar