Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2014

Open Access 01-12-2014 | Research article

Acupuncture stimulation improves scopolamine-induced cognitive impairment via activation of cholinergic system and regulation of BDNF and CREB expressions in rats

Authors: Bombi Lee, Bongjun Sur, Jaegul Shim, Dae-Hyun Hahm, Hyejung Lee

Published in: BMC Complementary Medicine and Therapies | Issue 1/2014

Login to get access

Abstract

Background

Acupuncture is an alternative therapy that is widely used to treat various neurodegenerative diseases and effectively improve cognitive and memory impairment. The aim of this study was to examine whether acupuncture stimulation at the Baihui (GV20) acupoint improves memory defects caused by scopolamine (SCO) administration in rats. We also investigated the effects of acupuncture stimulation at GV20 on the cholinergic system as well as the expression of brain-derived neurotrophic factor (BDNF) and cAMP-response element-binding protein (CREB) in the hippocampus.

Methods

SCO (2 mg/kg, i.p.) was administered to male rats once daily for 14 days. Acupuncture stimulation at GV20 was performed for 5 min before SCO injection. After inducing cognitive impairment via SCO administration, we conducted a passive avoidance test (PAT) and the Morris water maze (MWM) test to assess behavior.

Results

Acupuncture stimulation at GV20 improved memory impairment as measured by the PAT and reduced the escape latency for finding the platform in the MWM test. Acupuncture stimulation at GV20 significantly alleviated memory-associated decreases in the levels of choline acetyltransferase (ChAT), BDNF and CREB proteins in the hippocampus. Additionally, acupuncture stimulation at GV20 significantly restored the expression of choline transporter 1 (CHT1), vesicular acetylcholine transporter (VAChT), BDNF and CREB mRNA in the hippocampus. These results demonstrate that acupuncture stimulation at GV20 exerts significant neuroprotective effects against SCO-induced neuronal impairment and memory dysfunction in rats.

Conclusions

These findings suggest that acupuncture stimulation at GV20 might be useful in various neurodegenerative diseases to improve cognitive functioning via stimulating cholinergic enzyme activities and regulating BDNF and CREB expression in the brain.
Appendix
Available only for authorised users
Literature
1.
go back to reference Scarpini E, Scheltens P, Feldman H: Treatment of Alzheimer’s disease: current status and new perspectives. Lancet Neurol. 2003, 2 (9): 539-547. 10.1016/S1474-4422(03)00502-7.CrossRefPubMed Scarpini E, Scheltens P, Feldman H: Treatment of Alzheimer’s disease: current status and new perspectives. Lancet Neurol. 2003, 2 (9): 539-547. 10.1016/S1474-4422(03)00502-7.CrossRefPubMed
3.
go back to reference Drever BD, Anderson WG, Johnson H, O’Callaghan M, Seo S, Choi DY, Riedel G, Platt B: Memantine acts as a cholinergic stimulant in the mouse hippocampus. J Alzheimers Dis. 2007, 12 (4): 319-333.PubMed Drever BD, Anderson WG, Johnson H, O’Callaghan M, Seo S, Choi DY, Riedel G, Platt B: Memantine acts as a cholinergic stimulant in the mouse hippocampus. J Alzheimers Dis. 2007, 12 (4): 319-333.PubMed
4.
go back to reference Lanctôt KL, Rajaram RD, Herrmann N: Therapy for Alzheimer’s disease: how effective are current treatments?. Ther Adv Neurol Disord. 2009, 2 (3): 163-180. 10.1177/1756285609102724.CrossRefPubMedPubMedCentral Lanctôt KL, Rajaram RD, Herrmann N: Therapy for Alzheimer’s disease: how effective are current treatments?. Ther Adv Neurol Disord. 2009, 2 (3): 163-180. 10.1177/1756285609102724.CrossRefPubMedPubMedCentral
5.
go back to reference Lahiri DK, Farlow MR, Sambamurti K, Greig NH, Giacobini E, Schneider LS: A critical analysis of new molecular targets and strategies for drug developments in Alzheimer’s disease. Curr Drug Targets. 2003, 4 (2): 97-112. 10.2174/1389450033346957. ReviewCrossRefPubMed Lahiri DK, Farlow MR, Sambamurti K, Greig NH, Giacobini E, Schneider LS: A critical analysis of new molecular targets and strategies for drug developments in Alzheimer’s disease. Curr Drug Targets. 2003, 4 (2): 97-112. 10.2174/1389450033346957. ReviewCrossRefPubMed
6.
go back to reference Lee B, Sur B, Shim I, Lee H, Hahm DH: Phellodendron amurense and Its Major Alkaloid Compound, Berberine Ameliorates Scopolamine-Induced Neuronal Impairment and Memory Dysfunction in Rats. Korean J Physiol Pharmacol. 2012, 16 (2): 79-89. 10.4196/kjpp.2012.16.2.79.CrossRefPubMedPubMedCentral Lee B, Sur B, Shim I, Lee H, Hahm DH: Phellodendron amurense and Its Major Alkaloid Compound, Berberine Ameliorates Scopolamine-Induced Neuronal Impairment and Memory Dysfunction in Rats. Korean J Physiol Pharmacol. 2012, 16 (2): 79-89. 10.4196/kjpp.2012.16.2.79.CrossRefPubMedPubMedCentral
7.
go back to reference Ahmed T, Gilani AH: Inhibitory effect of curcuminoids on acetylcholinesterase activity and attenuation of scopolamine-induced amnesia may explain medicinal use of turmeric in Alzheimer's disease. Pharmacol Biochem Behav. 2009, 91 (4): 554-559. 10.1016/j.pbb.2008.09.010.CrossRefPubMed Ahmed T, Gilani AH: Inhibitory effect of curcuminoids on acetylcholinesterase activity and attenuation of scopolamine-induced amnesia may explain medicinal use of turmeric in Alzheimer's disease. Pharmacol Biochem Behav. 2009, 91 (4): 554-559. 10.1016/j.pbb.2008.09.010.CrossRefPubMed
8.
go back to reference Uchida S, Endo S, Akita K, Ohta T, Fukuda S: The cyanine Dye NK-4 improves scopolamine-induced memory impairments in mice. Biol Pharm Bull. 2012, 35 (10): 1831-1835. 10.1248/bpb.b12-00370.CrossRefPubMed Uchida S, Endo S, Akita K, Ohta T, Fukuda S: The cyanine Dye NK-4 improves scopolamine-induced memory impairments in mice. Biol Pharm Bull. 2012, 35 (10): 1831-1835. 10.1248/bpb.b12-00370.CrossRefPubMed
9.
go back to reference Hong SW, Yang JH, Joh EH, Kim HJ, Kim DH: Gypenoside TN-2 ameliorates scopolamine-induced learning deficit in mice. J Ethnopharmacol. 2011, 134 (3): 1010-1013. 10.1016/j.jep.2011.02.002.CrossRefPubMed Hong SW, Yang JH, Joh EH, Kim HJ, Kim DH: Gypenoside TN-2 ameliorates scopolamine-induced learning deficit in mice. J Ethnopharmacol. 2011, 134 (3): 1010-1013. 10.1016/j.jep.2011.02.002.CrossRefPubMed
10.
go back to reference Willians CM, El Mohsen MA, Vauzour D, Rendeiro C, Butler LT, Ellis JA, Whiteman M, Spencer JP: Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med. 2008, 45 (3): 295-305. 10.1016/j.freeradbiomed.2008.04.008.CrossRef Willians CM, El Mohsen MA, Vauzour D, Rendeiro C, Butler LT, Ellis JA, Whiteman M, Spencer JP: Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med. 2008, 45 (3): 295-305. 10.1016/j.freeradbiomed.2008.04.008.CrossRef
11.
go back to reference Xu J, Rong S, Xie B, Sun Z, Deng Q, Wu H, Bao W, Wang D, Yao P, Huang F, Liu L: Memory impairment in cognitively impaired aged rats associated with decreased hippocampal CREB phosphorylation: reversal by procyanidins extracted from the lotus seedpod. J Gerontol A Biol Sci Med Sci. 2010, 65 (9): 933-940.CrossRefPubMed Xu J, Rong S, Xie B, Sun Z, Deng Q, Wu H, Bao W, Wang D, Yao P, Huang F, Liu L: Memory impairment in cognitively impaired aged rats associated with decreased hippocampal CREB phosphorylation: reversal by procyanidins extracted from the lotus seedpod. J Gerontol A Biol Sci Med Sci. 2010, 65 (9): 933-940.CrossRefPubMed
12.
go back to reference Tyler WJ, Alonso M, Bramham CR, Pozzo-miller LD: From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem. 2002, 9 (5): 224-237. 10.1101/lm.51202. ReveiwCrossRefPubMedPubMedCentral Tyler WJ, Alonso M, Bramham CR, Pozzo-miller LD: From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem. 2002, 9 (5): 224-237. 10.1101/lm.51202. ReveiwCrossRefPubMedPubMedCentral
13.
go back to reference Kim EJ, Jung IH, Van Le TK, Jeong JJ, Kim NJ, Kim DH: Ginsenosides Rg5 and Rh3 protect scopolamine-induced memory deficits in mice. J Ethnopharmacol. 2013, 146 (1): 294-299. 10.1016/j.jep.2012.12.047.CrossRefPubMed Kim EJ, Jung IH, Van Le TK, Jeong JJ, Kim NJ, Kim DH: Ginsenosides Rg5 and Rh3 protect scopolamine-induced memory deficits in mice. J Ethnopharmacol. 2013, 146 (1): 294-299. 10.1016/j.jep.2012.12.047.CrossRefPubMed
14.
go back to reference Bekinschtein P, Cammarota M, Katche C, Slipczuk L, Rossato JI, Goldin A, Izquierdo I, Medina JH: BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A. 2008, 105 (7): 2711-2716. 10.1073/pnas.0711863105.CrossRefPubMedPubMedCentral Bekinschtein P, Cammarota M, Katche C, Slipczuk L, Rossato JI, Goldin A, Izquierdo I, Medina JH: BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A. 2008, 105 (7): 2711-2716. 10.1073/pnas.0711863105.CrossRefPubMedPubMedCentral
15.
go back to reference Kotani S, Yamauchi T, Teramoto T, Ogura H: Donepezil, an acetylcholinesterase inhibitor, enhances adult hippocampal neurogenesis. Chem Biol Interact. 2008, 175 (1–3): 227-230.CrossRefPubMed Kotani S, Yamauchi T, Teramoto T, Ogura H: Donepezil, an acetylcholinesterase inhibitor, enhances adult hippocampal neurogenesis. Chem Biol Interact. 2008, 175 (1–3): 227-230.CrossRefPubMed
16.
go back to reference Kotani S, Yamauchi T, Teramoto T, Ogura H: Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience. 2004, 142 (2): 505-514.CrossRef Kotani S, Yamauchi T, Teramoto T, Ogura H: Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience. 2004, 142 (2): 505-514.CrossRef
17.
go back to reference He X, Yan T, Chen R, Ran D: Acute effects of electro-acupuncture (EA) on hippocampal long term potentiation (LTP) of perforant path-dentate gyrus granule cells synapse related to memory. Acupunct Electrother Res. 2012, 37 (2–3): 89-101.CrossRefPubMed He X, Yan T, Chen R, Ran D: Acute effects of electro-acupuncture (EA) on hippocampal long term potentiation (LTP) of perforant path-dentate gyrus granule cells synapse related to memory. Acupunct Electrother Res. 2012, 37 (2–3): 89-101.CrossRefPubMed
18.
go back to reference Lee JD, Jang MH, Kim EH, Kim CJ: Acupuncture decreases neuropeptide Y expression in the hypothalamus of rats with Streptozotocin-induced diabetes. Acupunct Electrother Res. 2004, 29 (1–2): 73-82.CrossRefPubMed Lee JD, Jang MH, Kim EH, Kim CJ: Acupuncture decreases neuropeptide Y expression in the hypothalamus of rats with Streptozotocin-induced diabetes. Acupunct Electrother Res. 2004, 29 (1–2): 73-82.CrossRefPubMed
19.
go back to reference Zhu Y, Zeng Y: Electroacupuncture protected pyramidal cells in hippocampal CA1 region of vascular dementia rats by inhibiting the expression of p53 and Noxa. CNS Neurosci Ther. 2011, 17 (6): 599-604. 10.1111/j.1755-5949.2010.00192.x.CrossRefPubMed Zhu Y, Zeng Y: Electroacupuncture protected pyramidal cells in hippocampal CA1 region of vascular dementia rats by inhibiting the expression of p53 and Noxa. CNS Neurosci Ther. 2011, 17 (6): 599-604. 10.1111/j.1755-5949.2010.00192.x.CrossRefPubMed
20.
go back to reference Chunag CM, Hsieh CL, Li TC, Lin JG: Acupuncture stimulation at Baihui acupoint reduced cerebral infarct and increased dopamine levels in chronic cerebral hypoterfusion and ischemia-reperfusion injured Sprague–Dawley rats. Am J Chin Med. 2007, 35 (5): 779-791. 10.1142/S0192415X07005260.CrossRef Chunag CM, Hsieh CL, Li TC, Lin JG: Acupuncture stimulation at Baihui acupoint reduced cerebral infarct and increased dopamine levels in chronic cerebral hypoterfusion and ischemia-reperfusion injured Sprague–Dawley rats. Am J Chin Med. 2007, 35 (5): 779-791. 10.1142/S0192415X07005260.CrossRef
21.
go back to reference Shen EY, Chen FJ, Chen YY, Lin MF: Locating the Acupoint Baihui (GV20) Beneath the Cerebral Cortex with MRI Reconstructed 3D Neuroimages. Evid Based Complement Alternat Med. 2011, 362494- Shen EY, Chen FJ, Chen YY, Lin MF: Locating the Acupoint Baihui (GV20) Beneath the Cerebral Cortex with MRI Reconstructed 3D Neuroimages. Evid Based Complement Alternat Med. 2011, 362494-
22.
go back to reference Lee MS, Shin BS, Ernst E: Acupuncture for Alzheimer's disease: a systematic review. Int J Clin Pract. 2009, 63 (6): 874-879. 10.1111/j.1742-1241.2009.02043.x.CrossRefPubMed Lee MS, Shin BS, Ernst E: Acupuncture for Alzheimer's disease: a systematic review. Int J Clin Pract. 2009, 63 (6): 874-879. 10.1111/j.1742-1241.2009.02043.x.CrossRefPubMed
23.
go back to reference Zhou F, Guo J, Cheng J, Wu G, Xia Y: Electroacupuncture increased cerebral blood flow and reduced ischemia brain injury: dependence on stimulation intensity and frequency. J Appl Physiol. 2011, 111 (6): 1877-1887. 10.1152/japplphysiol.00313.2011.CrossRefPubMedPubMedCentral Zhou F, Guo J, Cheng J, Wu G, Xia Y: Electroacupuncture increased cerebral blood flow and reduced ischemia brain injury: dependence on stimulation intensity and frequency. J Appl Physiol. 2011, 111 (6): 1877-1887. 10.1152/japplphysiol.00313.2011.CrossRefPubMedPubMedCentral
24.
go back to reference Lee B, Sur BJ, Kwon S, Jung E, Shim I, Lee H, Hahm DH: Acupuncture stimulation alleviates corticosterone-induced impairments of spatial memory and cholinergic neurons in rats. Evid Based Complement Alternat Med. 2012, 2012: 670536-PubMed Lee B, Sur BJ, Kwon S, Jung E, Shim I, Lee H, Hahm DH: Acupuncture stimulation alleviates corticosterone-induced impairments of spatial memory and cholinergic neurons in rats. Evid Based Complement Alternat Med. 2012, 2012: 670536-PubMed
25.
go back to reference Fang Z, Ning J, Xiong C, Shulin Y: Effects of electroacupuncture at head points on the function of cerebral motor areas in stroke patients: A PET study. Evid Based Complement Alternat Med. 2012, 2012: 902413-PubMedPubMedCentral Fang Z, Ning J, Xiong C, Shulin Y: Effects of electroacupuncture at head points on the function of cerebral motor areas in stroke patients: A PET study. Evid Based Complement Alternat Med. 2012, 2012: 902413-PubMedPubMedCentral
26.
go back to reference Wang Q, Wang F, Li X, Yang Q, Li X, Xu N, Huang Y, Zhang Q, Gou X, Chen S, Xiong L: Electroacupuncture pretreatment attenuates cerebral ischemic injury through α7 nicotinic acetylcholine receptor-mediated inhibition of high-mobility group box 1 release in rats. J Neuroinflammation. 2012, 26 (9): 24-36.CrossRef Wang Q, Wang F, Li X, Yang Q, Li X, Xu N, Huang Y, Zhang Q, Gou X, Chen S, Xiong L: Electroacupuncture pretreatment attenuates cerebral ischemic injury through α7 nicotinic acetylcholine receptor-mediated inhibition of high-mobility group box 1 release in rats. J Neuroinflammation. 2012, 26 (9): 24-36.CrossRef
27.
go back to reference Youn D, Na C: Hepatoprotective effects of elector-acupuncture at Taechung (LR3) and Yangji (TE4) on experimental liver injury in rats. Korean J Acupunct. 2006, 23 (2): 167-176. Youn D, Na C: Hepatoprotective effects of elector-acupuncture at Taechung (LR3) and Yangji (TE4) on experimental liver injury in rats. Korean J Acupunct. 2006, 23 (2): 167-176.
28.
go back to reference Zhao RJ, Yoon SS, Lee BH, Kwon YK, Kim KJ, Shim I, Choi KH, Kim MR, Golden GT, Yang CH: Acupuncture normalizes the release of accumbal dopamine during the withdrawal period and after the ethanol challenge in chronic ethanol-treated rats. Neurosci Lett. 2006, 395 (1): 28-32. 10.1016/j.neulet.2005.10.043.CrossRefPubMed Zhao RJ, Yoon SS, Lee BH, Kwon YK, Kim KJ, Shim I, Choi KH, Kim MR, Golden GT, Yang CH: Acupuncture normalizes the release of accumbal dopamine during the withdrawal period and after the ethanol challenge in chronic ethanol-treated rats. Neurosci Lett. 2006, 395 (1): 28-32. 10.1016/j.neulet.2005.10.043.CrossRefPubMed
29.
go back to reference Paxinos G, Watson C: The rat brain in stereotaxic coordinates. 1986, New York, USA: Academic Press, 54-85. 3 Paxinos G, Watson C: The rat brain in stereotaxic coordinates. 1986, New York, USA: Academic Press, 54-85. 3
30.
go back to reference Sun Z, Jia J, Gong X, Jia Y, Deng J, Wang X, Wang X: Inhibition of glutamate and acetylcholine release in behavioral improvement induced by electroacupuncture in parkinsonian rats. Neurosci Lett. 2012, 520 (1): 32-37. 10.1016/j.neulet.2012.05.021.CrossRefPubMed Sun Z, Jia J, Gong X, Jia Y, Deng J, Wang X, Wang X: Inhibition of glutamate and acetylcholine release in behavioral improvement induced by electroacupuncture in parkinsonian rats. Neurosci Lett. 2012, 520 (1): 32-37. 10.1016/j.neulet.2012.05.021.CrossRefPubMed
31.
go back to reference Lin YW, Hsieh CL: Electroacupuncture at Baihui acupoint (GV20) reverses behavior deficit and long-term potentiation through N-methyl-d-aspartate and transient receptor potential vanilloid subtype 1 receptors in middle cerebral artery occlusion rats. J Integr Neurosci. 2010, 9 (3): 269-282. 10.1142/S0219635210002433.CrossRefPubMed Lin YW, Hsieh CL: Electroacupuncture at Baihui acupoint (GV20) reverses behavior deficit and long-term potentiation through N-methyl-d-aspartate and transient receptor potential vanilloid subtype 1 receptors in middle cerebral artery occlusion rats. J Integr Neurosci. 2010, 9 (3): 269-282. 10.1142/S0219635210002433.CrossRefPubMed
32.
go back to reference Satoh H: Acute effects of acupuncture treatment with baihui (GV20) on human arterial stiffness andwave reflection. J Acupunct Meridian Stud. 2009, 2 (2): 130-134. 10.1016/S2005-2901(09)60045-5.CrossRefPubMed Satoh H: Acute effects of acupuncture treatment with baihui (GV20) on human arterial stiffness andwave reflection. J Acupunct Meridian Stud. 2009, 2 (2): 130-134. 10.1016/S2005-2901(09)60045-5.CrossRefPubMed
33.
go back to reference Hwang IK, Chung JY, Yoo DY, Yi SS, Youn HY, Seong JK, Yoon YS: Effects of electroacupuncture at Zusanli and Baihui on brain-derived neurotrophic factor and cyclic AMP response element-binding protein in the hippocampal dentate gyrus. J Vet Med Sci. 2010, 72 (11): 1431-1436. 10.1292/jvms.09-0527.CrossRefPubMed Hwang IK, Chung JY, Yoo DY, Yi SS, Youn HY, Seong JK, Yoon YS: Effects of electroacupuncture at Zusanli and Baihui on brain-derived neurotrophic factor and cyclic AMP response element-binding protein in the hippocampal dentate gyrus. J Vet Med Sci. 2010, 72 (11): 1431-1436. 10.1292/jvms.09-0527.CrossRefPubMed
34.
go back to reference Liu SY, Hsieh CL, Wei TS, Liu PT, Chang YJ, Li TC: Acupuncture stimulation improves balance function in stroke patients: a single-blinded controlled, randomized study. Am J Chin Med. 2009, 37 (3): 483-494. 10.1142/S0192415X09006990.CrossRefPubMed Liu SY, Hsieh CL, Wei TS, Liu PT, Chang YJ, Li TC: Acupuncture stimulation improves balance function in stroke patients: a single-blinded controlled, randomized study. Am J Chin Med. 2009, 37 (3): 483-494. 10.1142/S0192415X09006990.CrossRefPubMed
35.
go back to reference Yu J, Liu C, Zhang X, Han J: Acupuncture improved cognitive impairment caused by multi-infarct dementia in rats. Physiol Behav. 2005, 86 (4): 434-441. 10.1016/j.physbeh.2005.07.015.CrossRefPubMed Yu J, Liu C, Zhang X, Han J: Acupuncture improved cognitive impairment caused by multi-infarct dementia in rats. Physiol Behav. 2005, 86 (4): 434-441. 10.1016/j.physbeh.2005.07.015.CrossRefPubMed
36.
go back to reference Kim JH, Choi KH, Jang YJ, Bae SS, Shin BC, Choi BT, Shin HK: Electroacupuncture Acutely Improves Cerebral Blood Flow and Attenuates Moderate Ischemic Injury via an Endothelial Mechanism in Mice. PLoS One. 2013, 8 (2): e56736-10.1371/journal.pone.0056736.CrossRefPubMedPubMedCentral Kim JH, Choi KH, Jang YJ, Bae SS, Shin BC, Choi BT, Shin HK: Electroacupuncture Acutely Improves Cerebral Blood Flow and Attenuates Moderate Ischemic Injury via an Endothelial Mechanism in Mice. PLoS One. 2013, 8 (2): e56736-10.1371/journal.pone.0056736.CrossRefPubMedPubMedCentral
37.
go back to reference Prado MA, Reis RA, Prado VF, de Mello MC, Gomez MV, de Mello FG: Regulation of acetylcholine synthesis and storage. Neurochem Int. 2002, 41 (5): 291-299. 10.1016/S0197-0186(02)00044-X. ReviewCrossRefPubMed Prado MA, Reis RA, Prado VF, de Mello MC, Gomez MV, de Mello FG: Regulation of acetylcholine synthesis and storage. Neurochem Int. 2002, 41 (5): 291-299. 10.1016/S0197-0186(02)00044-X. ReviewCrossRefPubMed
38.
go back to reference Klinkenberg I, Blokland A: The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev. 2010, 34 (8): 1307-1350. 10.1016/j.neubiorev.2010.04.001.CrossRefPubMed Klinkenberg I, Blokland A: The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev. 2010, 34 (8): 1307-1350. 10.1016/j.neubiorev.2010.04.001.CrossRefPubMed
39.
go back to reference Doguc DK, Delibas N, Vural H, Altuntas I, Sutcu R, Sonmez Y: Effects of chronic scopolamine administration on spatial working memory and hippocampal receptors related to learning. Behav Pharmacol. 2012, 23 (8): 762-770. 10.1097/FBP.0b013e32835a38af.CrossRefPubMed Doguc DK, Delibas N, Vural H, Altuntas I, Sutcu R, Sonmez Y: Effects of chronic scopolamine administration on spatial working memory and hippocampal receptors related to learning. Behav Pharmacol. 2012, 23 (8): 762-770. 10.1097/FBP.0b013e32835a38af.CrossRefPubMed
40.
go back to reference Khakpai F, Nasehi M, Haeri-Rohani A, Eidi A, Zarrindast MR: Scopolamine induced memory impairment; possible involvement of NMDA receptor mechanisms of dorsal hippocampus and/or septum. Behav Brain Res. 2012, 213 (1): 1-10.CrossRef Khakpai F, Nasehi M, Haeri-Rohani A, Eidi A, Zarrindast MR: Scopolamine induced memory impairment; possible involvement of NMDA receptor mechanisms of dorsal hippocampus and/or septum. Behav Brain Res. 2012, 213 (1): 1-10.CrossRef
41.
go back to reference Giacobini E: Long term stabilizing effect of cholinesterase inhibitors in the therapy of Alzheimer’s disease. J Neural Transm Suppl. 2002, 62: 181-187. 10.1007/978-3-7091-6139-5_17.CrossRefPubMed Giacobini E: Long term stabilizing effect of cholinesterase inhibitors in the therapy of Alzheimer’s disease. J Neural Transm Suppl. 2002, 62: 181-187. 10.1007/978-3-7091-6139-5_17.CrossRefPubMed
42.
go back to reference Hut RA, Van der Zee EA: The cholinergic system, circadian rhythmicity, and time memory. Behav Brain Res. 2011, 221 (2): 466-480. 10.1016/j.bbr.2010.11.039.CrossRefPubMed Hut RA, Van der Zee EA: The cholinergic system, circadian rhythmicity, and time memory. Behav Brain Res. 2011, 221 (2): 466-480. 10.1016/j.bbr.2010.11.039.CrossRefPubMed
43.
go back to reference White KG, Ruske AC: Memory deficits in Alzheimer’s disease: the encoding hypothesis and cholinergic function. Psychon Bull Rev. 2002, 9 (3): 426-437. 10.3758/BF03196301. ReviewCrossRefPubMed White KG, Ruske AC: Memory deficits in Alzheimer’s disease: the encoding hypothesis and cholinergic function. Psychon Bull Rev. 2002, 9 (3): 426-437. 10.3758/BF03196301. ReviewCrossRefPubMed
44.
go back to reference Lee B, Sur BJ, Han JJ, Shim I, Her S, Lee HJ, Hahm DH: Krill phosphatidylserine improves learning and memory in Morris water maze in aged rats. Prog Neuropsychopharmacol Biol Psychiatry. 2010, 34 (6): 1085-1093. 10.1016/j.pnpbp.2010.05.031.CrossRefPubMed Lee B, Sur BJ, Han JJ, Shim I, Her S, Lee HJ, Hahm DH: Krill phosphatidylserine improves learning and memory in Morris water maze in aged rats. Prog Neuropsychopharmacol Biol Psychiatry. 2010, 34 (6): 1085-1093. 10.1016/j.pnpbp.2010.05.031.CrossRefPubMed
45.
go back to reference Sarter M, Parikh V: Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci. 2005, 6 (1): 48-56. 10.1038/nrn1588.CrossRefPubMed Sarter M, Parikh V: Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci. 2005, 6 (1): 48-56. 10.1038/nrn1588.CrossRefPubMed
46.
go back to reference Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD: Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci. 2003, 23 (30): 9697-9709.PubMed Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman CJ, Yi H, Levey AI, Blakely RD: Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J Neurosci. 2003, 23 (30): 9697-9709.PubMed
47.
go back to reference De Jaeger X, Cammarota M, Prado MA, Izquierdo I, Prado VF, Pereira GS: Decreased acetylcholine release delays the consolidation of object recognition memory. Behav Brain Res. 2013, 1 (238): 62-68.CrossRef De Jaeger X, Cammarota M, Prado MA, Izquierdo I, Prado VF, Pereira GS: Decreased acetylcholine release delays the consolidation of object recognition memory. Behav Brain Res. 2013, 1 (238): 62-68.CrossRef
48.
go back to reference Nagy PM, Aubert I: Overexpression of the vesicular acetylcholine transporter increased acetylcholine release in the hippocampus. Neuroscience. 2012, 30 (218): 1-11.CrossRef Nagy PM, Aubert I: Overexpression of the vesicular acetylcholine transporter increased acetylcholine release in the hippocampus. Neuroscience. 2012, 30 (218): 1-11.CrossRef
49.
go back to reference Sase A, Khan D, Höger H, Lubec G: Intraperitoneal injection of saline modulates hippocampal brain receptor complex levels but does not impair performance in the Morris Water Maze. Amino Acids. 2012, 43 (2): 783-792. 10.1007/s00726-011-1130-9.CrossRefPubMed Sase A, Khan D, Höger H, Lubec G: Intraperitoneal injection of saline modulates hippocampal brain receptor complex levels but does not impair performance in the Morris Water Maze. Amino Acids. 2012, 43 (2): 783-792. 10.1007/s00726-011-1130-9.CrossRefPubMed
50.
go back to reference Veeraragavan S, Bui N, Perkins JR, Yuva-Paylor LA, Carpenter RL, Paylor R: Modulation of behavioral phenotypes by a muscarinic M1 antagonist in a mouse model of fragile X syndrome. Psychopharmacology (Berl). 2011, 217 (1): 143-151. 10.1007/s00213-011-2276-6.CrossRef Veeraragavan S, Bui N, Perkins JR, Yuva-Paylor LA, Carpenter RL, Paylor R: Modulation of behavioral phenotypes by a muscarinic M1 antagonist in a mouse model of fragile X syndrome. Psychopharmacology (Berl). 2011, 217 (1): 143-151. 10.1007/s00213-011-2276-6.CrossRef
51.
go back to reference Parfitt GM, Campos RC, Barbosa AK, Koth AP, Barros DM: Participation of hippocampal cholinergic system in memory persistence for inhibitory avoidance in rats. Neurobiol Learn Mem. 2012, 97 (2): 183-188. 10.1016/j.nlm.2011.12.001.CrossRefPubMed Parfitt GM, Campos RC, Barbosa AK, Koth AP, Barros DM: Participation of hippocampal cholinergic system in memory persistence for inhibitory avoidance in rats. Neurobiol Learn Mem. 2012, 97 (2): 183-188. 10.1016/j.nlm.2011.12.001.CrossRefPubMed
52.
go back to reference Vaynman S, Ying Z, Gomez-Pinilla F: Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience. 2003, 122 (3): 647-657. 10.1016/j.neuroscience.2003.08.001.CrossRefPubMed Vaynman S, Ying Z, Gomez-Pinilla F: Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience. 2003, 122 (3): 647-657. 10.1016/j.neuroscience.2003.08.001.CrossRefPubMed
53.
go back to reference Kida S, Josselyn SAV, de Ortiz SP, Kogan JH, Chevere I, Masushige S: CREB required for the stability of new and reactivated fear memories. Nat Neurosci. 2002, 5 (4): 348-355. 10.1038/nn819.CrossRefPubMed Kida S, Josselyn SAV, de Ortiz SP, Kogan JH, Chevere I, Masushige S: CREB required for the stability of new and reactivated fear memories. Nat Neurosci. 2002, 5 (4): 348-355. 10.1038/nn819.CrossRefPubMed
54.
go back to reference Guzowski JF, McGaugh JL: Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc Natl Acad Sci U S A. 1997, 94 (1): 2693-2698.CrossRefPubMedPubMedCentral Guzowski JF, McGaugh JL: Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc Natl Acad Sci U S A. 1997, 94 (1): 2693-2698.CrossRefPubMedPubMedCentral
55.
go back to reference Feng S, Wang Q, Wang H, Peng Y, Wang L, Lu Y, Shi T, Xiong L: Electroacupuncture pretreatment ameliorates hypergravity-induced impairment of learning and memory and apoptosis of hippocampal neurons in rats. Neurosci Lett. 2010, 478 (3): 150-155. 10.1016/j.neulet.2010.05.006.CrossRefPubMed Feng S, Wang Q, Wang H, Peng Y, Wang L, Lu Y, Shi T, Xiong L: Electroacupuncture pretreatment ameliorates hypergravity-induced impairment of learning and memory and apoptosis of hippocampal neurons in rats. Neurosci Lett. 2010, 478 (3): 150-155. 10.1016/j.neulet.2010.05.006.CrossRefPubMed
56.
go back to reference Liu R, Li JZ, Song JK, Zhou D, Huang C, Bai XY, Xie T, Zhang X, Li YJ, Wu CX, Zhang L, Li L, Zhang TT, Du GH: Pinocembrin improves cognition and protects the neurovascular unit in Alzheimer related deficits. Neurobiol Aging. 2014, 35 (6): 1275-1285. 10.1016/j.neurobiolaging.2013.12.031.CrossRefPubMed Liu R, Li JZ, Song JK, Zhou D, Huang C, Bai XY, Xie T, Zhang X, Li YJ, Wu CX, Zhang L, Li L, Zhang TT, Du GH: Pinocembrin improves cognition and protects the neurovascular unit in Alzheimer related deficits. Neurobiol Aging. 2014, 35 (6): 1275-1285. 10.1016/j.neurobiolaging.2013.12.031.CrossRefPubMed
57.
go back to reference Kim MW, Chung YC, Jung HC, Park MS, Han YM, Chung YA, Maeng LS, Park SI, Lim J, Im WS, Chung JY, Kim M, Mook I, Kim M: Electroacupuncture enhances motor recovery performance with brain-derived neurotrophic factor expression in rats with cerebral infarction. Acupunct Med. 2012, 30 (3): 222-226. 10.1136/acupmed-2011-010126.CrossRefPubMed Kim MW, Chung YC, Jung HC, Park MS, Han YM, Chung YA, Maeng LS, Park SI, Lim J, Im WS, Chung JY, Kim M, Mook I, Kim M: Electroacupuncture enhances motor recovery performance with brain-derived neurotrophic factor expression in rats with cerebral infarction. Acupunct Med. 2012, 30 (3): 222-226. 10.1136/acupmed-2011-010126.CrossRefPubMed
58.
go back to reference Zhou Y, Jin J: Effect of acupuncture given at the HT 7, ST 36, ST 40 and KI 3 acupoints on various parts of the brains of Alzheimer’ s disease patients. Acupunct Electrother Res. 2008, 33 (1–2): 9-17.CrossRefPubMed Zhou Y, Jin J: Effect of acupuncture given at the HT 7, ST 36, ST 40 and KI 3 acupoints on various parts of the brains of Alzheimer’ s disease patients. Acupunct Electrother Res. 2008, 33 (1–2): 9-17.CrossRefPubMed
59.
go back to reference Wang T, Liu CZ, Yu JC, Jiang W, Han JX: Acupuncture protected cerebral multi-infarction rats from memory impairment by regulating the expression of apoptosis related genes Bcl-2 and Bax in hippocampus. Physiol Behav. 2009, 96 (1): 155-161. 10.1016/j.physbeh.2008.09.024.CrossRefPubMed Wang T, Liu CZ, Yu JC, Jiang W, Han JX: Acupuncture protected cerebral multi-infarction rats from memory impairment by regulating the expression of apoptosis related genes Bcl-2 and Bax in hippocampus. Physiol Behav. 2009, 96 (1): 155-161. 10.1016/j.physbeh.2008.09.024.CrossRefPubMed
60.
go back to reference Chang KH, Bai SJ, Lee H, Lee BH: Effects of acupuncture stimulation at different acupoints on formalin-induced pain in rats. Korean J Physiol Pharmacol. 2014, 18 (2): 121-127. 10.4196/kjpp.2014.18.2.121.CrossRefPubMedPubMedCentral Chang KH, Bai SJ, Lee H, Lee BH: Effects of acupuncture stimulation at different acupoints on formalin-induced pain in rats. Korean J Physiol Pharmacol. 2014, 18 (2): 121-127. 10.4196/kjpp.2014.18.2.121.CrossRefPubMedPubMedCentral
61.
go back to reference Lee BH, Lim SC, Jeon HJ, Kim JS, Lee YK, Lee HJ, In S, Kim HY, Yoon SS, Yang CH: Acupuncture suppresses reinstatement of morphine-seeking behavior induced by a complex cue in rats. Neurosci Lett. 2012, 26 (548): 126-131. Lee BH, Lim SC, Jeon HJ, Kim JS, Lee YK, Lee HJ, In S, Kim HY, Yoon SS, Yang CH: Acupuncture suppresses reinstatement of morphine-seeking behavior induced by a complex cue in rats. Neurosci Lett. 2012, 26 (548): 126-131.
Metadata
Title
Acupuncture stimulation improves scopolamine-induced cognitive impairment via activation of cholinergic system and regulation of BDNF and CREB expressions in rats
Authors
Bombi Lee
Bongjun Sur
Jaegul Shim
Dae-Hyun Hahm
Hyejung Lee
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2014
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/1472-6882-14-338

Other articles of this Issue 1/2014

BMC Complementary Medicine and Therapies 1/2014 Go to the issue