Research Article
Cellular, Behavioral, and Locomotor Effects of Oral Nicotine in Male Rats with Bilateral Lesions in the Ventrolateral Striatum Induced with 6-OHDA
Abstract
Objective: Parkinson's disease is a progressive neurodegenerative disease having a spectrum of non-motor to motor symptoms. Unrelated to motor symptoms of sensory, autonomic, and neuropsychiatric symptoms often appear early in the course of the disease. It is a remarkable observation that patients in the premotor phase can easily quit smoking without help. This study was intended to investigate the interrelation between nicotine and the partial loss of dopaminergic innervation in the ventrolateral striatum induced by 6-OHDA.
Methods: We used an experimental premotor parkinsonism model. The oral nicotine preference of rats was investigated with the two-bottle free choice method. The behaviors related to locomotor activity and emotional state were evaluated with a locomotor activity test, elevated plus maze, and forced swimming test. Histopathological evaluation was performed in the striatum by staining techniques using hematoxylin+eosin (H&E) and immunohistochemistry markers (caspase-3, and MAP-2).
Results: Bilateral 6-OHDA lesions did not lead to a significant alteration in the total locomotor activity or nicotine preference. Nicotine increased horizontal but decreased vertical movements in addition to increasing anxiolytic but also depressive effects in the OHDA lesion group. The number of apoptotic cells was significantly lower in the lesion group receiving nicotine compared to those not receiving nicotine.
Conclusion: Our experimental study points to the role of oral nicotine in male rats with bilateral striatal 6-OHDA lesions in the ventrolateral striatum. Further studies are needed to understand the relationship between loss of dopaminergic innervation in the striatum and nicotine consumption.
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References
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- Tolosa E, Compta Y, Gaig C. The premotor phase of Parkinson’s disease. Parkinsonism and Related Disorders 2007; 13:2-7
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- Rowell PP, Hurst HE, Marlowe C, Bennett BD. Oral administration of nicotine: its uptake and distribution after chronic administration to mice. J Pharmacol Methods1983; 9:249–261
- Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 5th ed, p 205. San Diego: Academic Press 2005.
- Armario A. The forced swim test: Historical, conceptual and methodological considerations and its relationship with individual behavioral traits. Neuroscience & Biobehavioral Reviews. 2021; 128:74-86. DOI:10.1016/j.neubiorev. 2021.06.014
- Konstantinidou AE, Givalos N, Gakiopoulou H, Korkolopoulou P, Kotsiakis X, Boviatsis E, Agrogiannis G, Mahera H, Patsouris E. Caspase-3 immunohistochemical expression is a marker of apoptosis, increased grade and early recurrence in intracranial meningiomas. Apoptosis 2007;12(4):695-705. DOI: 10.1007/s10495-006-0001
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- Dickson PR, Lang CG, Hinton SC, Kelley AG. Oral stereotypy induced by amphetamine microinjection into striatum: an anatomical mapping study Neuroscience 1994;61(1):81-91. DOI: 10.1016/0306-4522(94)90062-0.
- Pisa M. Motor somatotopy in the striatum of rat: manipulation, biting and gait. Behav Brain Res.1988; 27(1):21-35. DOI: 10.1016/0166-4328(88)90106-4.
- Graham DL, Stanwood GD. Handbook of Developmental Neurotoxicology. 2nd ed. Behavioral Phenotyping in Developmental Neurotoxicology-Simple Approaches Using Unconditioned Behaviours in Rodents; 2018.
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- Ksir C. Acute and chronic nicotine effects on measures of activity in rats: A multivariate analysis, Psychopharmacology1994;115(1-2):105-109. DOI: 10.1007/BF02244758
- Redolat R, Pérez-Martínez A, Carrasco MA, Mesa P. Individual differences in novelty-seeking and behavioral responses to nicotine: a review of animal studies, Curr Drug Abuse Rev.2009; 2(3):230-242. DOI: 10.2174/1874473710902030230.
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- Wexler Y, Benjamini Y, Golani I. Vertical exploration and dimensional modularity in mice. R Soc Open Sci.2018; 5(3):180069. DOI: 10.1098/rsos.180069.
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- Balleine BW, O'Doherty JP. Human and rodent homologies in action control: corticostriatal determinants of -goal-directed and habitual action. Neuropsychopharmacology 2010; 35(1):48-69. DOI: 10.1038/npp.2009.131.
- Anyan J, Amir S. Too depressed to swim or too afraid to stop? A reinterpretation of the forced swim test as a measure of anxiety-like behavior. Neuropsychopharmacology 2018; 43(5):931-933. DOI: 10.1038/npp.2017.260.
- Costa G, Abin-Carriquiry JA, Dajas F. Nicotine prevents striatal dopamine loss produced by 6-hydroxydopamine lesion in the substantia nigra. Brain Res. 2001; 888: 336 – 334
- Parain K, Marchand V, Dumery B, Hirsch E. Nicotine, but not cotinine, partially protects dopaminergic neurons against MPTP-induced degeneration in mice. Brain Res; 2001; 890: 347 – 350. DOI: 10.1016/s0006-8993(00)03198-x. PMID: 11164803.
- Takeuchi H, Yanagida T, Inden M, Takata K, Kitamura Y, Yamakawa K, Sawada H, Izumi Y, Yamamoto N, Kihara T, Uemura K, Inoue H, Taniguchi T, Akaike A, Takahashi R, Shimohama S. Nicotinic receptor stimulation protects nigral dopaminergic neurons in rotenone-induced Parkinson's disease models. J Neurosci Res. 2009;87(2):576-85. DOI: 10.1002/jnr.21869. PMID: 18803299
- Smith Y, Villalba R. Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov Disord. 2008;23 (3):534-47. DOI: 10.1002/mds.22027.
- Witzig VS, Komnig D, Falkenburger BH. Changes in Striatal Medium Spiny Neuron Morphology Resulting from Dopamine Depletion Are Reversible. Cells 2020;9(11):2441. DOI: 10.3390/cells9112441.
- DeGiosio RA, Grubisha MJ, MacDonald ML, McKinney BC, Camacho CJ, Sweet RA. More than a marker: potential pathogenic functions of MAP2. Front Mol Neurosci. 2022:16; 15:974890. DOI: 10.3389/fnmol.2022.974890.
- Durieux PF, Schiffmann SN, de Kerchove d'Exaerde A. Targeting neuronal populations of the striatum. Front Neuroanat. 2011: 15;5: 40. DOI: 10.3389/fnana.2011.00040.
Year 2023,
Volume: 13 Issue: 3, 615 - 622, 11.09.2023
Abstract
Keywords
Project Number
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References
- Cheng HC, Ulane CM, Burke RE. Clinical progression in Parkinson’s disease and the neurobiology of axons. Ann Neurol. 2010; 67: 715-725. DOI: 10.1002/ana.21995
- Tolosa E, Compta Y, Gaig C. The premotor phase of Parkinson’s disease. Parkinsonism and Related Disorders 2007; 13:2-7
- Moccia M, Erro R, Picillo M, Vassallo E, Vitale C, Longo K, Amboni M, Santangelo G, Palladino R, Nardone A, Triassi M, Barone P, Pellecchia MT. Quitting smoking: An early non-motor feature of Parkinson's disease. Parkinsonism and Related Disorders 2015; 21:216-220.
- Postuma RB, Aarsland D, Barone P, Burn DJ, Hawkes CH, Oertel W, ZiemssenT. Identifying prodromal Parkinson's disease: Pre-motor disorders in Parkinson's disease. Mov. Disord. Offic. J. Mov. Dis.Soc. 2012; 27:617–626.
- Tanner CM. Advances in environmental epidemiology. Mov Disord. 2010;25(1): 58–62
- Chuang YH, Paula KC, Sinsheimerb JS, Bronsteinc JM, Bordelonc YM, Ritza B. Genetic variants in nicotinic receptors and smoking cessation in Parkinson's disease. Parkinsonism and Related Disorders.2019; 62:57–61
- Quik M, Wonnacott S. {alpha}6{beta}2* and {alpha}4{beta}2* Nicotinic acetylcholine receptors as drug targets for Parkinson’s disease. Pharmacol Rev. 2011; 63:938–966.
- Zhang D, McGregor M, Bordia T, et al. α7 nicotinic receptor agonists reduce levodopa-induced dyskinesias with severe nigrostriatal damage. Mov Disord. 2015;30(14):1901–1911.
- Rowell PP, Hurst HE, Marlowe C, Bennett BD. Oral administration of nicotine: its uptake and distribution after chronic administration to mice. J Pharmacol Methods1983; 9:249–261
- Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 5th ed, p 205. San Diego: Academic Press 2005.
- Armario A. The forced swim test: Historical, conceptual and methodological considerations and its relationship with individual behavioral traits. Neuroscience & Biobehavioral Reviews. 2021; 128:74-86. DOI:10.1016/j.neubiorev. 2021.06.014
- Konstantinidou AE, Givalos N, Gakiopoulou H, Korkolopoulou P, Kotsiakis X, Boviatsis E, Agrogiannis G, Mahera H, Patsouris E. Caspase-3 immunohistochemical expression is a marker of apoptosis, increased grade and early recurrence in intracranial meningiomas. Apoptosis 2007;12(4):695-705. DOI: 10.1007/s10495-006-0001
- Lindner MD, Cain CK, Plone MA, Frydel BR, Blaney TJ, Emerich DF, Hoane MR. Incomplete nigrostriatal dopaminergic cell loss and partial reductions in striatal dopamine produce akinesia, rigidity, tremor and cognitive deficits in middle-aged rats. Behav Brain Res. 1999;102(1-2):1-16. DOI: 10.1016/s0166-4328(98)00160-0. PMID: 10403011.
- Dickson PR, Lang CG, Hinton SC, Kelley AG. Oral stereotypy induced by amphetamine microinjection into striatum: an anatomical mapping study Neuroscience 1994;61(1):81-91. DOI: 10.1016/0306-4522(94)90062-0.
- Pisa M. Motor somatotopy in the striatum of rat: manipulation, biting and gait. Behav Brain Res.1988; 27(1):21-35. DOI: 10.1016/0166-4328(88)90106-4.
- Graham DL, Stanwood GD. Handbook of Developmental Neurotoxicology. 2nd ed. Behavioral Phenotyping in Developmental Neurotoxicology-Simple Approaches Using Unconditioned Behaviours in Rodents; 2018.
- Jandová K, Marešová D, Pokorný J. Fast and delayed locomotor response to acute high-dose nicotine administration in adult male rats. Physiol Res.2013;62(1): 81-88. DOI: 10.33549/physiolres.932610.
- Ksir C. Acute and chronic nicotine effects on measures of activity in rats: A multivariate analysis, Psychopharmacology1994;115(1-2):105-109. DOI: 10.1007/BF02244758
- Redolat R, Pérez-Martínez A, Carrasco MA, Mesa P. Individual differences in novelty-seeking and behavioral responses to nicotine: a review of animal studies, Curr Drug Abuse Rev.2009; 2(3):230-242. DOI: 10.2174/1874473710902030230.
- Khwaja M, McCormack A, McIntosh JM, Di Monte AD, Quik M. Nicotine partially protects against paraquat-induced nigrostriatal damage in mice; link to alpha 6beta2* nAChRs. J Neurochem.2007;100: 180 – 190.
- Wexler Y, Benjamini Y, Golani I. Vertical exploration and dimensional modularity in mice. R Soc Open Sci.2018; 5(3):180069. DOI: 10.1098/rsos.180069.
- Iguchi Y, Kosugi S, Nishikawa H, Lin Z, Minabe Y, Toda S. Repeated exposure of adult rats to transient oxidative stress induces various long-lasting alterations in cognitive and behavioral functions. PLoS One 2014;9(12): e114024. DOI: 10.1371/journal.pone.0114024
- Balleine BW, O'Doherty JP. Human and rodent homologies in action control: corticostriatal determinants of -goal-directed and habitual action. Neuropsychopharmacology 2010; 35(1):48-69. DOI: 10.1038/npp.2009.131.
- Anyan J, Amir S. Too depressed to swim or too afraid to stop? A reinterpretation of the forced swim test as a measure of anxiety-like behavior. Neuropsychopharmacology 2018; 43(5):931-933. DOI: 10.1038/npp.2017.260.
- Costa G, Abin-Carriquiry JA, Dajas F. Nicotine prevents striatal dopamine loss produced by 6-hydroxydopamine lesion in the substantia nigra. Brain Res. 2001; 888: 336 – 334
- Parain K, Marchand V, Dumery B, Hirsch E. Nicotine, but not cotinine, partially protects dopaminergic neurons against MPTP-induced degeneration in mice. Brain Res; 2001; 890: 347 – 350. DOI: 10.1016/s0006-8993(00)03198-x. PMID: 11164803.
- Takeuchi H, Yanagida T, Inden M, Takata K, Kitamura Y, Yamakawa K, Sawada H, Izumi Y, Yamamoto N, Kihara T, Uemura K, Inoue H, Taniguchi T, Akaike A, Takahashi R, Shimohama S. Nicotinic receptor stimulation protects nigral dopaminergic neurons in rotenone-induced Parkinson's disease models. J Neurosci Res. 2009;87(2):576-85. DOI: 10.1002/jnr.21869. PMID: 18803299
- Smith Y, Villalba R. Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov Disord. 2008;23 (3):534-47. DOI: 10.1002/mds.22027.
- Witzig VS, Komnig D, Falkenburger BH. Changes in Striatal Medium Spiny Neuron Morphology Resulting from Dopamine Depletion Are Reversible. Cells 2020;9(11):2441. DOI: 10.3390/cells9112441.
- DeGiosio RA, Grubisha MJ, MacDonald ML, McKinney BC, Camacho CJ, Sweet RA. More than a marker: potential pathogenic functions of MAP2. Front Mol Neurosci. 2022:16; 15:974890. DOI: 10.3389/fnmol.2022.974890.
- Durieux PF, Schiffmann SN, de Kerchove d'Exaerde A. Targeting neuronal populations of the striatum. Front Neuroanat. 2011: 15;5: 40. DOI: 10.3389/fnana.2011.00040.
There are 31 citations in total.
Details
| Primary Language | English |
|---|---|
| Subjects | Central Nervous System, Neurology and Neuromuscular Diseases |
| Journal Section | Articles |
| Authors | |
| Project Number | No |
| Publication Date | September 11, 2023 |
| Submission Date | August 26, 2022 |
| Published in Issue | Year 2023 Volume: 13 Issue: 3 |
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