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Implications for Learning and Memory The Journal of Neuroscience, May 15, 2000, 20(10):3900–3908 Cholinergic Excitation of Septohippocampal GABA But Not Cholinergic Neurons: Implications for Learning and Memory Min Wu,1 Marya Shanabrough,2 Csaba Leranth,2,3 and Meenakshi Alreja1,3 Departments of 1Psychiatry, 2Obstetrics and Gynecology, and 3Neurobiology, Yale University School of Medicine and the Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut 06508 The medial septum/diagonal band (MSDB), which gives rise to linergic neurons in rat brain slices, we have found that musca- the septohippocampal pathway, is a critical locus for the mne- rinic agonists do not excite septohippocampal cholinergic neu- monic effects of muscarinic drugs. Infusion of muscarinic cho- rons, instead they inhibit a subpopulation of cholinergic linergic agonists into the MSDB enhance learning and memory neurons. In contrast, unlabeled neurons, confirmed to be non- processes both in young and aged rats and produce a contin- cholinergic, septohippocampal GABA-type neurons using ret- uous theta rhythm in the hippocampus. Intraseptal muscarinic rograde marking and double-labeling techniques, are pro- agonists also alleviate the amnesic syndrome produced by foundly excited by muscarine. Thus, the cognition-enhancing systemic administration of muscarinic receptor antagonists. It effects of muscarinic drugs in the MSDB cannot be attributed to has been presumed, but not proven, that the cellular mecha- an increase in hippocampal ACh release. Instead, disinhibitory nisms underlying the effects of muscarinic agonists in the mechanisms, caused by increased impulse flow in the septo- MSDB involve an excitation of septohippocampal cholinergic hippocampal GABAergic pathway, may underlie the cognition- neurons and a subsequent increase in acetylcholine (ACh) re- enhancing effects of muscarinic agonists. lease in the hippocampus. Using a novel fluorescent labeling Key words: theta rhythm; 192IgG; p75 receptor; neurotro- technique to selectively visualize live septohippocampal cho- phin; acetylcholine; memory; cognition; disinhibition Basic and clinical studies have long recognized the importance of systemic scopolamine-induced amnesia, suggesting that the cholinergic mechanisms in cognitive functioning (Givens and MSDB is a critical locus for the mnemonic effects of muscarinic Sarter, 1997), and drugs that increase synaptic acetylcholine levels drugs (Givens and Olton, 1995). are currently the most used for the treatment of cognitive deficits In general, it is assumed that improvements in SH pathway- associated with CNS disorders such as Alzheimer’s disease, al- related learning and memory tasks occurs as a result of an beit, with limited effectiveness (Benzi and Moretti, 1998). The increase in hippocampal ACh release (Monmaur and Breton, septohippocampal (SH) pathway, which originates in the medial 1991; Givens and Olton, 1994, 1995; Apartis et al., 1998; Bland septum/diagonal band (MSDB) and shows progressive degener- and Oddie, 1998; Dickinson-Anson et al., 1998). As such, it has ation in Alzheimer’s disease (Whitehouse et al., 1982), has spe- been presumed that the memory-enhancing effects of intraseptal- cifically been implicated in cognitive mechanisms. Lesions of the muscarinic agonists occur because of increased firing of SH fimbria-fornix, which conveys SH cholinergic (Lewis and Shute, cholinergic neurons (Markowska et al., 1995; Givens and Sarter, 1967) and GABAergic fibers to the hippocampus (Kohler et al., 1997). These assumptions have been based on earlier studies that 1984; Freund, 1989), interfere both with learning and memory reported a muscarinic receptor-mediated increase in firing of SH tasks and with generation of the theta rhythm in rats (Brito and neurons (Dutar et al., 1983; Lamour et al., 1984), which lead to Brito, 1990). These deficits can be attenuated by grafting ACh- the hypothesis that ACh, via muscarinic receptors, has a positive producing cells to the hippocampus (Dunnett et al., 1982; feedback effect on SH cholinergic neurons (Dutar et al., 1983; Dickinson-Anson et al., 1998). Lamour et al., 1984; Segal, 1986). However, the SH neurons Cholinergic mechanisms operating within the MSDB are also recorded from in these studies were presumed but not proven to critical for learning and memory. Thus, infusions of muscarinic be cholinergic. A small sample of cholinergic-type MSDB neu- agonists directly into the MSDB elicit continuous hippocampal rons (n ϭ 3), classified using electrophysiological characteristics, theta (Monmaur and Breton, 1991; Lawson and Bland, 1993) and were found to be inhibited by muscarine (Serafin et al., 1996). facilitate learning and memory-related behaviors both in young Additional effects of muscarine, such as a block of late afterhy- (Givens and Olton, 1990) and aged rats (Markowska et al., 1995). perpolarization (Sim and Griffith, 1991) and decrease in gluta- Intraseptal infusions of muscarinic agonists can also alleviate mate transmission (Sim and Griffith, 1996) have also been re- ported in unidentified basal forebrain neurons. Effects of Received Nov. 29, 1999; revised March 2, 2000; accepted March 6, 2000. muscarinic agonists on identified septohippocampal cholinergic This work was supported by National Alliance for Research on Schizophrenia and neurons have not been investigated. Depression and National Institutes of Health Grants DA09797 to M.A. and NS26068 to C.L. We thank N. Margiotta for technical help and Leslie Rosello for help in In the present study, we used a novel fluorescent marker, manuscript preparation. Cy3–192IgG, to selectively label live rat SH cholinergic neurons Correspondence should be addressed to Dr. Meenakshi Alreja, Department of and studied their response to cholinergic drugs using extracellular Psychiatry, CMHC 335A, Yale University School of Medicine, 34 Park Street, New Haven, CT 06508. E-mail: [email protected]. and whole-cell recordings in brain slices. Cy3–192IgG is prepared Copyright © 2000 Society for Neuroscience 0270-6474/00/203900-09$15.00/0 by conjugating the inert fluorochrome, Cy3, with an antibody Wu et al. • Acetylcholine and the Septohippocampal Pathway J. Neurosci., May 15, 2000, 20(10):3900–3908 3901 against the p75 neurotrophin receptor. When injected intraven- contrast imaging (IR-DIC) (Dodt and Zieglgansberger, 1990; Stuart et tricularly, Cy3–192IgG retrogradely labels only p75 receptor- al., 1993) was performed to visualize neurons for extracellular or patch- clamp recording using an Olympus Optical BX-50 microscope equipped expressing neurons (Hartig et al., 1998), which in the MSDB are witha60ϫ water immersion objective (numerical aperture, 0.9; Olym- exclusively cholinergic (Batchelor et al., 1989; Sobreviela et al., pus). Images were detected with a CCD-300-RC camera (DAGE-MTI, 1994). The goal of this study was to determine whether identified Michigan City, IN) and displayed on a standard black and white video SH cholinergic neurons are excited by their own neurotransmitter monitor (DAGE-MTI, HR 120). The images were transferred to the via muscarinic receptors. hard disk of a personal computer using an LG-3 scientific frame grabber (Scion Image, Frederick, MD) and processed further with Adobe Pho- toshop. Cy3–192IgG-labeled and rhodamine-labeled neurons were visu- MATERIALS AND METHODS alized using the appropriate fluorescence filters, as was Lucifer yellow. A neuron viewed with infrared optics was considered to be the same as that Retrograde labeling of septohippocampal neurons. Young adult male viewed with fluorescence optics when the infrared image and the fluo- Sprague Dawley albino rats (14- to 21-d-old) were anesthetized using the rescent image of the neuron had the same position and orientation with following cocktail: ketamine, 75 mg/kg; xylazine, 4 mg/kg, and the two imaging systems. acepromazine, 0.075 mg/kg. Retrograde labeling of septohippocampal Electrophysiology recordings. The image of the cells in the slice was neurons (SHNs) was performed by pressure injecting 50–100 nl of displayed on a video monitor, and glass pipettes used for electrophysio- rhodamine-labeled fluorescent latex microspheres (Lumafluor, Naples, logical recordings were visually advanced through the slice to the surface FL) at several sites within the hippocampus of 14- to 21-d-old rats using of the cell from which recordings were made. Extracellular recordings a glass micropipette (40–50 ␮m tip diameter). Rhodamine microspheres ⍀ ␮ were performed with glass micropipettes filled with 2 M NaCl (5–10 M ). (0.02–0.2 m diameter) show little diffusion and consequently produce Whole-cell patch-clamp recordings were performed using previously small, sharply defined injection sites. Once transported back to neuronal described methods (Alreja and Liu, 1996). In brief, low-resistance (2.5– somata, the label persists for at least 10 weeks in vivo and 1 year after 3.5 M⍀) patch pipettes were filled with a solution containing (in mM): K fixation. Microspheres have been reported to possess no obvious cyto- methylsulfonate/KCl, 120; HEPES, 10; BAPTA K , 5; sucrose, 20; toxicity or phototoxicity, as assessed by intracellular recording and stain- 4 CaCl2, 2.38; MgCl2,1;K2ATP, 1 and GTP, 0.1, pH 7.32–7.35. All ing of retrogradely labeled cells in brain slice preparation (Katz et al., recordings were made using an Axoclamp-2B amplifier (Axon Instru- 1984). The stereotaxic coordinates were: anteroposterior, Ϫ2.8, Ϫ1.4, Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ ments, Foster City, CA) in the bridge mode; the output signal was filtered 2.8;
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