Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells

Benardo, Larry S.; Prince, David A.

doi:10.1016/0006-8993(82)90067-1

Cited by 222 publications

(133 citation statements)

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“…ACh is known to evoke multiple effects in hippocampal neurons and the cholinergic influences on the evoked responses are strongly dependent on the sites of application (Bernardo and Prince 1982;Cherubini et al 1982;Frotscher and Léranth 1985;Madison et al 1987;Benson et al 1988;Chen and Tonegawa 1997). Several lines of evidence show that the cholinergic system plays a role in facilitating plastic changes at Schaffer collateral-commissural-CA1 synapses in accordance with the well-known memory-facilitating action of ACh (Markram and Segal 1990;Auerbach and Segal 1994).…”

Section: Pacap-38 Enhances Ca1 Synaptic Transmissionmentioning

confidence: 85%

“…The molecular mechanism of this long-lasting facilitation of EPSPs is still under debate. One possibility is that LTPm is correlated with an increase in postsynaptic excitability (Krnjevic et al 1981;Bernardo and Prince 1982;Krnjevic and Ropert 1982;Madison et al 1987;Benson et al 1988) associated with an increase in membrane resistance that is mediated by a selective inactivation of the K + channel (Madison et al 1987;Markram and Segal 1990). Alternatively, LTPm could be attributable to an increase in the Ca 2+ component of the N-methyl-D-aspartate (NMDA) response or by the activation of second messenger systems, which regulate intracellular Ca 2+ , which, in turn, modifies the NMDA response (Madison et al 1987;Auerbach and Segal 1994;Markram and Segal 1990;Cormier et al 1993;Huang and Malenka 1993).…”

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confidence: 99%

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

Roberto¹,

Brunelli²

2000

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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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Section: Pacap-38 Enhances Ca1 Synaptic Transmissionmentioning

confidence: 85%

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confidence: 99%

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

Roberto¹,

Brunelli²

2000

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“…PACAP-38 enhances in a dose-dependent manner the spontaneous release of ACh from the septal cholinergic fibers in the dorsal hippocampus (Masuo et al 1993) and ACh evokes multiple, concentration-dependent, effects on evoked responses at CA1 synapses (Bernardo and Prince 1982;Madison et al 1987). Specifically, ACh can induce a long-lasting muscarinic enhancement of EPSPs (Krnjevic et al 1981;Marchi and Raitieri 1989;Blitzer et al 1990;Markram and Segal 1990;Auerbach and Segal 1994) as well as a suppression of the CA1 responses evoked by stimulation of Schaffer collateral-commissural fibers (Krnjevic et al 1981;Krnjevic and Report 1982;Sheridan and Sutor 1990;Auerbach and Segal 1996).…”

Section: Discussionmentioning

confidence: 99%

Differential Effects of PACAP-38 on Synaptic Responses in Rat Hippocampal CA1 Region

Roberto

Scuri²,

Brunelli³

2001

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Pituitary adenylate cyclase-activating polypeptide (PACAP-38) is a member of the vasointestinal polypeptide (VIP)/secretin/glucagon family of neuropeptides for which neuroregulatory functions have been postulated. PACAP-38 receptors are expressed in different brain regions, including hippocampus. In this study, we examined the dose-dependent effects of PACAP-38 on the excitatory postsynaptic field potential (fEPSP) evoked at the Schaffer collateral-CA1 synapse in rat hippocampal slices. Bath application of low dose (0.05 nM) of PACAP-38 induced long-lasting facilitation of the fEPSP. This enhancement was blocked by the cholinergic receptor antagonist atropine and partially by the NMDA receptor antagonist 2-amino-5-phosphonovalerate (APV) and therefore, shares a common mechanism with LTP. In contrast, a high dose (1 µM) of PACAP-38 induced a persistent depression of the fEPSP that was not blocked by antagonists of cholinergic receptors (i.e., atropine and mecamylamine), adenosine receptors (i.e., DCPCX), or glutamatergic NMDA receptors (APV). Intermediate doses (0.1-0.5 µM) of PACAP-38 produced an initial decrease of the fEPSP followed by an enhancement. This decrease was not blocked by atropine whereas the facilitation was. These results show that PACAP-38 modulates CA1 synaptic transmission in a dose-dependent manner and that the peptide interacts with cholinergic and glutamatergic systems.Pituitary adenylate cyclase-activating polypeptide (PACAP-38) is a 38-amino acid peptide that was first isolated from ovine hypothalamus for its ability to stimulate adenylyl cyclase in rat anterior pituitary cells (Arimura 1992). PACAP-38 exhibits high sequence identity with vasoactive intestinal peptide (VIP), distinguishing PACAP-38 as a member of the VIP-secretin-glucagon family of peptides. The aminoacid sequence of PACAP-38 has been remarkably conserved during evolution, suggesting that PACAP-38 regulates important physiological functions (Arimura 1992;Masuo et al. 1993). Two receptors for PACAP-38 have been identified: type I receptors, which are positively coupled to adenylyl cyclase and phospholipase C, and type II receptors, which have only been linked to adenylyl cyclase (Spengler et al. 1993). PACAP-38 receptors are mainly distributed in the central nervous system including the hippocampus (Masuo et al. 1992(Masuo et al. , 1993.PACAP-38 modulates synaptic activity in several neuronal regions. For example, PACAP-38 enhances in a dosedependent manner the spontaneous release of acetylcholine (ACh) from septal cholinergic fibers in the dorsal hippocampus (Masuo et al. 1993). An excitatory action of PACAP-38 on glutamatergic N-methyl-D-aspartate (NMDA) receptors has also been reported in cortical neurons (Martin et al. 1995;Stella and Magistretti 1996;Liu and Madsen 1997) and in sympathetic preganglionic neurons of neonatal rat (Lai et al. 1997;Wu and Dun 1997). In addition, a high concentration of PACAP-38 (1-3 µM) induces a long-lasting depression of the field excitatory postsynaptic potential (fEPSP) at hippocampal ...

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“…Acetylcholine causes similar physiological effects in most cortical structures, including direct depolarization of neurons Benardo & Prince, 1982;Madison & Nicoll, 1984) and enhancement of long-term potentiation (Blitzer, Gil, & Landau, 1990;Brocher, Artola, & Singer, 1992;Patil, Linster, Lubenov, & Hasselmo, 1998). Experimental data in a number of different regions also shows that acetylcholine strongly suppresses excitatory glutamatergic synaptic transmission via presynaptic inhibition at intrinsic, recurrent synapses in cortical structures (Dutar & Nicoll, 1988;Gil, Connors, & Amitai, 1997;Hasselmo, Schnell, & Barkai, 1995;Hounsgaard, 1978;Hsieh, Cruikshank, & Metherate, 2000;Linster, Wyble, & Hasselmo, 1999;Williams & Constanti, 1988).…”

Section: Introductionmentioning

confidence: 89%

Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

Linster

Maloney

Patil

et al. 2003

Neurobiology of Learning and Memory

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Computational modeling assists in analyzing the specific functional role of the cellular effects of acetylcholine within cortical structures. In particular, acetylcholine may regulate the dynamics of encoding and retrieval of information by regulating the magnitude of synaptic transmission at excitatory recurrent connections. Many abstract models of associative memory function ignore the influence of changes in synaptic strength during the storage process and apply the effect of these changes only during a socalled recall-phase. Efforts to ensure stable activity with more realistic, continuous updating of the synaptic strength during the storage process have shown that the memory capacity of a realistic cortical network can be greatly enhanced if cholinergic modulation blocks transmission at synaptic connections of the association fibers during the learning process. We here present experimental data from an olfactory cortex brain slice preparation showing that previously potentiated fibers show significantly greater suppression (presynaptic inhibition) by the cholinergic agonist carbachol than unpotentiated fibers. We conclude that low suppression of non-potentiated fibers during the learning process ensures the formation of self-organized representations in the neural network while the higher suppression of previously potentiated fibers minimizes interference between overlapping patterns. We show in a computational model of olfactory cortex, that, together, these two phenomena reduce the overlap between patterns that are stored within the same neural network structure. These results further demonstrate the contribution of acetylcholine to mechanisms of cortical plasticity. The results are consistent with the extensive evidence supporting a role for acetylcholine in encoding of new memories and enhancement of response to salient sensory stimuli.

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Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells

Cited by 222 publications

References 36 publications

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

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

Differential Effects of PACAP-38 on Synaptic Responses in Rat Hippocampal CA1 Region

Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

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