An immunocytochemical study of choline acetyltransferase- containing neurons and axon terminals in normal and partially deafferented hippocampal formation

Matthews, Dee Ann; Salvaterra, Paul M.; Crawford, G. D.; Houser, Carolyn R.; Vaughn, James E.

doi:10.1016/0006-8993(87)91044-4

Cited by 120 publications

(51 citation statements)

References 38 publications

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“…Although there are intrinsic hippocampal cholinergic neurons (Matthews et al, 1987), they provide only a very small part of the normal cholinergic innervation of the hippocampus and are unlikely to account for the responses observed here. Previous attempts to elicit cholinergic responses in hippocampal neurons in vitro have demonstrated that trains of stimulation can activate a slow EPSP mediated by muscarinic receptors in CA1 pyramidal neurons (Cole and Nicoll, 1983;Madison et al, 1987) but did not detect a nicotinic component to the responses.…”

Section: Discussionmentioning

confidence: 66%

“…The relatively low frequency of the sEPSCs is expected because presumably they occur in an action potential-independent manner, i.e., via the terminals of the severed axons of cholinergic cell bodies located in the medial septum. Alternatively, it is possible that the spontaneous events arise from the action potential-dependent activity of the sparse cholinergic neurons in hippocampus (Matthews et al, 1987). In that event the low level of internal cholinergic circuitry also might explain the low frequency with which the spontaneous events were observed.…”

Section: Discussionmentioning

confidence: 99%

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Synaptic Potentials Mediated via α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors in Rat Hippocampal Interneurons

et al. 1998

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Exogenous application of acetylcholine elicits inward currents in hippocampal interneurons that are mediated via ␣-bungarotoxin-sensitive nicotinic acetylcholine receptors, but synaptic responses mediated via such receptors have never been reported in mammalian brain. In the present study, EPSCs were evoked in hippocampal interneurons in rat brain slices by electrical stimulation and were recorded by using whole-cell voltage-clamp techniques. Nicotinic EPSCs were isolated pharmacologically, using antagonists to block other known types of ligand-gated ion channels, and then were tested with either ␣-bungarotoxin or methyllycaconitine, which are selective antagonists for nicotinic acetylcholine receptors that contain the ␣7 receptor subunit. Each antagonist proved highly effective at reducing the remaining synaptic current. Evoked ␣7-mediated nicotinic EPSCs also were desensitized by superfusion with 1 M nicotine, had extrapolated reversal potentials near 0 mV, and showed strong inward rectification at positive potentials. In several interneurons, methyllycaconitine-sensitive spontaneous EPSCs also were observed that exhibited a biphasic decay rate very similar to that of the ␣7-mediated evoked response. These studies provide the first demonstration of a functional cholinergic synapse in the mammalian brain, in which the primary postsynaptic receptors are ␣-bungarotoxin-sensitive nicotinic acetylcholine receptors.

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Section: Discussionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Synaptic Potentials Mediated via α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors in Rat Hippocampal Interneurons

et al. 1998

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“…They reported that PACAP-38 was more potent than PACAP-27 in stimulating the release of ACh (Masuo et al 1993). This release of ACh was highly calcium dependent, suggesting that PACAP-38 works via a presynaptic mechanism (Matthews et al 1987;Margiotta and Pardi 1995). PACAP-38, acting through type-I receptors, enhances the ACh sensitivity of ciliary ganglionic neurons by a cAMPdependent mechanism (Matthews et al 1987).…”

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confidence: 99%

“…PACAP-38, acting through type-I receptors, enhances the ACh sensitivity of ciliary ganglionic neurons by a cAMPdependent mechanism (Matthews et al 1987). The hippocampus receives abundant extrinsic cholinergic innervation from the medial septal area (Frotscher and Léranth 1985;Matthews et al 1987), and the septohippocampal choliner-gic pathway has been suggested to have an important role in learning and memory (Valentino and Dingledine 1981;Krnjevic and Ropert 1982;Hepler et. al.…”

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confidence: 99%

PACAP-38 Enhances Excitatory Synaptic Transmission in the Rat Hippocampal CA1 Region

Roberto¹,

Brunelli²

2000

Learn. Mem.

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Specific receptors for pituitary adenylate cyclase-activating polypeptide (PACAP), a novel peptide with neuroregulatory and neurotrophic functions, have been identified recently in different brain regions, including the hippocampus. In this study, we examined the effects of PACAP-38 on the excitatory postsynaptic field potentials (fEPSPs) evoked at the Schaffer collateral-CA1 synapses. Brief bath application of PACAP-38 (0.05 nM) induced a long-lasting facilitation of the basal transmission. Enhancement of this response was occluded in part by previous high-frequency-induced long-term potentiation (LTP). PACAP-38 did not significantly alter the paired-pulse facilitation (PPF). PACAP-38 has been shown to have a presynaptic effect on the septohippocampal cholinergic terminals, which results in an increase in basal acetylcholine (ACh) release. To assess whether the PACAP-38 enhancement of CA1 synapses was related to the activation of the cholinergic system we examined the effect of this peptide in the presence of atropine, a muscarinic receptor antagonist. The enhancement of the fEPSPs by PACAP-38 was blocked by bath application of atropine. These results show that PACAP-38 induces facilitation of hippocampal synaptic transmission through activation of the cholinergic system via the muscarinic receptors.Pituitary adenylate cyclase-activating polypeptide (PACAP) is a new member of a neuropeptide family that includes vasoactive intestinal peptide (VIP), glucagon, secretin, and growth hormone, and whose members are thought to play an important role in neuronal function (Miyata et al. 1989; Arimura 1998). PACAP has been isolated from the ovine hypothalamus on the basis of its ability to stimulate adenylate cyclase in rat anterior pituitary cells (Miyata et al. 1989) and it is present in the central nervous system (CNS) and in a variety of peripheral tissues (Masuo et al. 1992;Arimura and Shioda 1995;Shioda et al. 1997). Two distinct forms of this neuropeptide, PACAP-38 and PACAP-27, with 38 or 27 amino acids, respectively, have been characterized (Arimura and Shioda 1995). PACAP-38 and PACAP-27 possess similar biological activity (Miyata et al. 1990). PACAP-38 is the prevailing form in mammalian tissues (Arimura 1992). The amino-acid sequence of PACAP-38 is well-preserved in different species and is identical in sheep, rats, and humans (Arimura 1992). Two types of high-affinity PACAP receptors have been identified: The PACAP type-I receptor (PACAPRI), which specifically binds PACAP-38 and PACAP-27 with higher affinity than it binds VIP; and the PACAP type-II receptor (PACAPRII), which has high homology with the VIP receptor and binds PACAP-38, PACAP-27, and VIP with the same high affinity (Arimura 1992;Sokolov and Kleschevnikov 1995). PACAPRI is mainly distributed in the CNS, including the septum, hippocampus, cerebellar cortex, amygdala, nucleus accumbens, hypothalamus, and the entorhinal cortices (Masuo et al. 1992(Masuo et al. ,1993 and it is positively coupled to adenylate cyclase and phospholipase C, whereas PACA...

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“…Key Words: Au toradiography-2-Deoxyglucose-G1ucose utilization Ibotenic acid-Plasticity-Septohippocampal pathway. Leninth, 1985;Matthews et a!., 1987). Studies em ploying acetylcholinesterase (AChE) histochemis try or ChAT immunocytochemistry for the identifi cation of septal cholinergic neurons in combination with retrograde tracing have provided evidence that only � 50% of the neurons of the medial septum/ diagonal band complex (MSDB) are cholinergic (Mesulam et a!., 1983;Baisden et a!., 1984;Rye et a!., 1984;Amaral and Kurz, 1985;Wainer et a!., 1985) .…”

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confidence: 99%

Plasticity in the Rat Hippocampal Formation following Ibotenic Acid Lesion of the Septal Region: A Quantitative [¹⁴C]Deoxyglucose and Acetylcholinesterase Study

Schulz

Wree

Schleicher

et al. 1992

J Cereb Blood Flow Metab

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Summary:The local cerebral glucose utilization was measured in the hippocampal formation 3, 21, and 90 days after bilateral lesions of the medial septal nucleus and the nucleus of the diagonal band of Broca by multiple ibotenic acid injections. The CMRgl c was determined in hippocampal areas and layers and various limbic and vi sual regions by quantitative e4C]2-deoxyglucose autora diography using a computerized image-processing sys tem. Three days after lesion, CMRgl c was significantly decreased in 26 of the 38 structures examined. The most pronounced reductions were found in CA2 and CA3, the subiculum, and the parasubiculum. The CMRglc values of the 21-and 90-day postlesion groups did not differ signif icantly from control data when univariate statistics were used. However, by means of a factor analysis and subse quently a discriminant analysis as a multivariate test for group differences, significant lesion-induced CMRg 1c changes could be detected between the control group, the 3-day group, and the 90-day group. The 21-day group didThe anatomy of the cholinergic septohippocam pal pathway has been intensively investigated using tracer techniques (Swanson and Cowan, 1979; Crutcher et a!., 198 1;Chandler and Crutcher, 1983) and, more recently, monoclonal antibodies to choline acetyltransferase (ChAT) (Frotscher and 1007 not differ significantly from the controls. The data indi cate that 90 days after lesion of the medial septum! diagonal band complex (MSDB), a considerable recovery of the mean CMRgl c was found in the hippocampal region, although a normal level was not reached. In a parallel series, processing of sections for acetylcholinesterase (AChE) histochemistry revealed a severe destruction of AChE-positive fibers in the hippocampus at 3 days after lesion and a conspicuous recovery in the amount of stain able fibers and their staining intensity at 21 days postle sion. In the 90-day group, the AChE fibers recovered even further but did not reach the values of unlesioned sham-operated controls. The present study indicates that sprouting of surviving cholinergic afferents might be an important morphological substrate for CMRglc recovery in the hippocampus after MSDB lesion.

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An immunocytochemical study of choline acetyltransferase- containing neurons and axon terminals in normal and partially deafferented hippocampal formation

Cited by 120 publications

References 38 publications

Synaptic Potentials Mediated via α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors in Rat Hippocampal Interneurons

Synaptic Potentials Mediated via α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors in Rat Hippocampal Interneurons

PACAP-38 Enhances Excitatory Synaptic Transmission in the Rat Hippocampal CA1 Region

Plasticity in the Rat Hippocampal Formation following Ibotenic Acid Lesion of the Septal Region: A Quantitative [¹⁴C]Deoxyglucose and Acetylcholinesterase Study

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An immunocytochemical study of choline acetyltransferase- containing neurons and axon terminals in normal and partially deafferented hippocampal formation

Cited by 120 publications

References 38 publications

Synaptic Potentials Mediated via α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors in Rat Hippocampal Interneurons

Synaptic Potentials Mediated via α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors in Rat Hippocampal Interneurons

PACAP-38 Enhances Excitatory Synaptic Transmission in the Rat Hippocampal CA1 Region

Plasticity in the Rat Hippocampal Formation following Ibotenic Acid Lesion of the Septal Region: A Quantitative [14C]Deoxyglucose and Acetylcholinesterase Study

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Plasticity in the Rat Hippocampal Formation following Ibotenic Acid Lesion of the Septal Region: A Quantitative [¹⁴C]Deoxyglucose and Acetylcholinesterase Study