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The Effect of Nucleus Basalis Magnocellularis Deep Brain Lee et al. BMC Neurology (2016) 16:6 DOI 10.1186/s12883-016-0529-z RESEARCH ARTICLE Open Access The effect of nucleus basalis magnocellularis deep brain stimulation on memory function in a rat model of dementia Ji Eun Lee1†, Da Un Jeong1†, Jihyeon Lee1, Won Seok Chang2 and Jin Woo Chang1,2* Abstract Background: Deep brain stimulation has recently been considered a potential therapy in improving memory function. It has been shown that a change of neurotransmitters has an effect on memory function. However, much about the exact underlying neural mechanism is not yet completely understood. We therefore examined changes in neurotransmitter systems and spatial memory caused by stimulation of nucleus basalis magnocellularis in a rat model of dementia. Methods: We divided rats into four groups: Normal, Lesion, Implantation, and Stimulation. We used 192 IgG-saporin for degeneration of basal forebrain cholinergic neuron related with learning and memory and it was injected into all rats except for the normal group. An electrode was ipsilaterally inserted in the nucleus basalis magnocellularis of all rats of the implantation and stimulation group, and the stimulation group received the electrical stimulation. Features were verified by the Morris water maze, immunochemistry and western blotting. Results: AllgroupsshowedsimilarperformancesduringMorriswater maze training. During the probe trial, performance of the lesion and implantation group decreased. However, the stimulation group showed an equivalent performance to the normal group. In the lesion and implantation group, expression of glutamate acid decarboxylase65&67 decreased in the medial prefrontal cortex and expression of glutamate transporters increased in the medial prefrontal cortex and hippocampus. However, expression of the stimulation group showed similar levels as the normal group. Conclusion: The results suggest that nucleus basalis magnocellularis stimulation enhances consolidation and retrieval of visuospatial memory related to changes of glutamate acid decarboxylase65&67 and glutamate transporter. Keywords: Nucleus basalis magnocellularis, Deep brain stimulation, Spatial memory, Medial prefrontal cortex, Hippocampus Background decrease of cholinergic projections could be an important Alzheimer’s disease (AD) is a progressive and irreversible factor characterizing the cognitive decline and functional neurodegenerative disease accompanied by decline of impairment that characterizes this disorder [2–4]. memory and cognitive function [1]. Degeneration of cho- As an effective surgical treatment, deep brain stimu- linergic basal forebrain neurons is one of the common fea- lation (DBS) has demonstrated its efficacy for the treat- tures of AD [2]. It has been reported that degeneration of ment of a variety of movement disorders [5]. Recently, basal forebrain cholinergic neurons (BFCN) and the there is growing evidence from laboratory and clinical trials that electrical stimulation at memory associated * Correspondence: [email protected] † structures enhances cognitive functions, and DBS has Equal contributors increasingly been considered as a potential therapy be- 1Brain Korea 21 Plus Project for Medical Science & Brain Research Institute, Yonsei University College of Medicine, Seoul, Korea cause of its recent effects in improving memory function 2Department of Neurosurgery, Severance Hospital, Yonsei University College of Medicine, Seoul 120-752, Republic of Korea © 2016 Lee et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Lee et al. BMC Neurology (2016) 16:6 Page 2 of 9 [6, 7]. However, there is currently limited evidence at best of Yonsei University and Institute of Laboratory Anima that DBS improves memory functioning in humans. Resources commission on Life Sciences National Research Stimulation of the entorhinal region in patients with de- Council, USA. This study received approval of Institu- mentia could improve patient’s spatial memory perform- tional Animal Care and Use Committee (IACUC number: ance [8]. In addition, electrical stimulation of the fornix 2014-0206). Every effort was made to minimize animal affects hippocampus-dependent memory [9]. Although suffering and to reduce the number of rats used. Twenty- DBS is being evaluated as a promising therapy for dis- five male Sprague–Dawley rats were used that weighed eases related to memory impairment, much about the 190 − 210 g (6 week old) at the beginning of the studies. underlying exact neural mechanism of DBS is not yet They were housed in clear plastic cages in a temperature- completely understood. Therefore, studies are needed and humidity-controlled room with a 12-h light/12-h dark to characterize not only the effective regions and stimu- cycle. Rats were randomly assigned to one of four experi- lation parameters for DBS causing memory improve- mental groups before surgery. The normal group (n =6) ment, but also the mechanisms connecting memory underwent no surgical procedures. The lesion group enhancement and changes of the neural circuit caused (n = 7) had intraventricular administration of 192 IgG- by stimulation. saporin. The implantation group (n =7) and stimula- In this study, we used 192 IgG-saporin for degener- tion group (n = 5) had intraventricular administration ation of BFCN to make a memory impaired rat model of 192 IgG-saporin and implantation of an electrode in mimicking cholinergic denervation of AD. Composed the NBM. The stimulation group had unilateral elec- of a monoclonal antibody, 192 IgG-sapoin, has a low af- trical stimulation. finity for the rat nerve growth factor receptor p75 lo- cated on cholinergic cell bodies of the basal forebrain. And it contains a ribosomal inactivating protein called Administration of 192 IgG-saporin saporin [10–12]. Therefore, 192 IgG-saporin injection Rats in the three experimental groups, but not the nor- to the intraventricular cause selective degeneration of mal group, were anesthetized with a mixture of ketamine BFCN closely related with spatial learning and memory (75 mg/kg), acepromazine (0.75 mg/kg), and xylazine [13, 14]. (4 mg/kg), and secured in a stereotaxic frame. Eight mi- Nucleus basalis magnocellularis (NBM) in the basal croliters (0.63 μg/μl) of 192 IgG-saporin (Chemicon, forebrain has mostly cholinergic neurons, and also it has a Temecula, CA, USA) were bilaterally injected into the few of noncholinergic neurons such as GABAergic and lateral ventricle following coordinates relating to Bregma glutamatergic [15]. It has mainly projections to the neo- (AP - 0.8 mm, ML ± 1.2 mm, DV - 3.4 mm). The solu- cortex, amygdala, and thalamus [16, 17]. Substantial evi- tions were delivered at a rate of 1 μl/min and diffused dence suggests that the NBM plays an important role in for 5 min after each injection. neural activities such as learning and memory [11, 16, 18]. NBM lesions by ibotanic acid resulted in deficits in the ac- Electrode implantation quisition of spatial memory tasks, and produced a pro- Right after the administration of 192 IgG-saporin, an found selective disturbance in recent memory [19, 20]. electrode (SNEX-100, contact diameter 0.1 mm, shaft Meanwhile, a research on a two-way active avoidance task diameter 0.25 mm, impedance 0.7–1.5 MΩ;DavidKopf (a test of associative memory) suggests the stimulation of Instruments, Tujunga, CA, USA) was inserted into the NBM can improve the acquisition memory [21, 22]. Espe- right NBM following coordinates relating to Bregma cially, the high frequency stimulation by regulating neuro- (AP -1.32 mm, ML + 2.8 mm, DV -7.4 mm) of the rats transmitters improves memory function. A study suggests in the implantation and stimulation group. Dental ce- that high frequency stimulation in the dorsal striatum is ment (Long Dental Manufacturing, Wheeling, IL, USA) effects on response learning and on GABA levels [23]. was used to firmly fix the electrode in place to the skull And also, NBM stimulation in patients with Parkinson- surface. dementia syndrome caused improvement of cognitive function [7]. In the present study, we examined whether Electrical stimulation unilateral electrical stimulation of the NBM improves The stimuli were bipolar and electrical stimuli (120 Hz, memory in a rat model that mimicking the basal forebrain 90 μs, 1 V) delivered via a Grass A-300 pulsemaster cholinergic deficits of AD. (Grass Instrument, Quincy, MA, USA). Stimulation pa- rameters were monitored in real time at the beginning Methods and end of stimulation using an oscilloscope (HDS Animals 1022 M, Owon, Korea). Rats were unilaterally stimulated All experiments were conducted according to the guide- daily beginning one week after surgery until the start of lines of the Institutional Animal Care and Use Committee behavioral testing (1 h per day, 1 week in total). Lee et al. BMC Neurology (2016) 16:6 Page 3 of 9 Morris water maze (MWM) Acetylcholinesterase (AChE) assay The MWM test began 2 weeks after surgery. The test Three out of six rats from the normal group, four out consisted of 5 consecutive
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