The actions of motilin, luteinizing hormone releasing hormone, cholecystokinin, somatostatin, vasoactive intestinal peptide, and other peptides on rat cerebral cortical neurons

Phillis, John W.; Kirkpatrick, J. R.

doi:10.1139/y80-102

Cited by 239 publications

(23 citation statements)

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“…The localization of CCK in synaptic vesicle fractions of brain homogenates (4), its release from in vitro preparations in a calcium-dependent manner (4), and its excitatory effect on hippocampal (5) and cortical neurons (6) are consistent with the suggestion that the peptide functions as a neurotransmitter in the cortex and elsewhere. However, CCK has yet to be localized at the fine structural level in the cerebral cortex.…”

supporting

confidence: 66%

Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels.

Hendry¹,

Jones²,

Beinfeld³

1983

Proc. Natl. Acad. Sci. U.S.A.

135

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Neurons displaying cholecystokinin-like immunoreactivity (CCK neurons) in rat and monkey cerebral cortex were examined by light and electron microscopic immunocytochemistry. CCK neurons were found to be mainly bipolar cells present in all layers and in all areas of the rat cerebral cortex. CCK neurons were also found in all regions examined in monkey cortex (preand post-central gyri and superior parietal lobule). The somata and the dendritic processes of CCK neurons receive relatively few synapses but both symmetric and asymmetric axosomatic and axodendritic synapses were found. The majority of axon terminals displaying CCK-like immunoreactivity formed symmetric synapses, most frequently with the somata and proximal dendrites of pyramidal and nonpyramidal neurons. The somata and processes of CCK neurons were also found to establish very close nonsynaptic associations with blood vessels and with other neurons, suggesting possible roles for the peptide in the maintenance of neuronal excitability and cerebral blood flow.The octapeptide cholecystokinin (CCK) is one of several neuropeptides that has been identified in the mammalian cerebral cortex (1-3). The localization of CCK in synaptic vesicle fractions of brain homogenates (4), its release from in vitro preparations in a calcium-dependent manner (4), and its excitatory effect on hippocampal (5) and cortical neurons (6) are consistent with the suggestion that the peptide functions as a neurotransmitter in the cortex and elsewhere. However, CCK has yet to be localized at the fine structural level in the cerebral cortex. Cortical neurons displaying CCK-like immunoreactivity have been identified light microscopically in the rat (7,8) but the nature of their pre-and post-synaptic relationships with other neurons are unknown. In the present study, we have used a well-characterized antiserum against CCK-8 (9) to examine the distribution, morphology, and synaptology of neurons that have CCK-like immunoreactivity (CCK neurons) in the cerebral cortex of both rats and monkeys. We show that, in addition to having many of the characteristics of typical local circuit neurons, CCK neurons in the cortex have unusual nonsynaptic relationships with other neurons and with blood vessels. MATERIALS AND METHODSTwo cynomolgus monkeys (Macaca fascicularis; Hazelton Research Primates, Reston, VA) and eight Wistar rats (bred in our colony)-were used. One monkey and three rats received intraventricular injections of colchicine (10 ug/,41; 110 /.l for the monkey, 10 or 15 /ul for the rats) and were allowed to survive for 2 days. All animals were perfused through the heart with 4% paraformaldehyde/0. 1% glutaraldehyde in 0.1 M phosphate buffer (pH 7.4). The rat brains and blocks of monkey brains including the pre-and post-central gyri and the superior parietal lobule were sectioned with either a Vibratome or a freezing microtome at 40-50 ,um. After several washes in 0.1 M phosphate buffer, the sections were incubated overnight in primary antiserum at dilutions of 1:1,000, 1:250, or...

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supporting

confidence: 66%

Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels.

Hendry¹,

Jones²,

Beinfeld³

1983

Proc. Natl. Acad. Sci. U.S.A.

135

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“…Neurotensin has been shown to affect the excitability of single neurones in NTLIcontaining tissues such as ganglion cells in the retina (Dick & Miller, 1981), cerebral cortical neurones (Phillis & Kirkpatrick, 1980), preoptic/anterior hypothalamic (PAOH) neurones (Baldino et al 1985), neurones of the arcuate nucleus (Herbison, Hubbard & Sirett, 1986), substantia nigra (Pinnock, 1985), locus coeruleus (Young, Uhl & Kuhar, 1978), spinal cord (Suzue, Yanaihara & Otsuka, 1981;Stanzione & Zieglgansberger, 1983), and myenteric plexus (Williams, Katayama & North, 1979). No data have been reported concerning the functional role and membrane effects of this putative transmitter in prevertebral ganglia.…”

Section: Discussionmentioning

confidence: 99%

The electrophysiological effects of neurotensin on neurones of guinea‐pig prevertebral sympathetic ganglia.

Stapelfeldt

Szurszewski

1989

The Journal of Physiology

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SUMMARY1. The membrane effects of neurotensin on neurones of guinea-pig prevertebral ganglia were investigated by means of intracellular recording techniques in vitro.2. Neurotensin (2-5 ,UM) applied by superfusion caused depolarizing responses in fifty-seven of seventy-four neurones tested in the inferior mesenteric ganglion and thirty-seven of forty-seven neurones tested in the coeliac plexus. The remaining neurones tested showed no membrane response.3. Responses to neurotensin could be discriminated into two different types of membrane depolarizations on the basis of their different time courses and pharmacological characteristics: a steady-state type of depolarization and a transient type of depolarization. Seven of fifty-seven responsive neurones tested in the inferior mesenteric ganglion and ten of thirty-seven responsive neurones tested in the coeliac plexus responded to neurotensin with a depolarization which was maintained constant as long as neurotensin was superfused over the preparation (steady-state type). Forty-eight of fifty-seven responsive neurones tested in the inferior mesenteric ganglion and twenty of thirty-seven responsive neurones tested in the coeliac plexus responded with a transient depolarization which was followed by a repolarization in the maintained presence of neurotensin (transient type). A combination of both types of responses was observed in two neurones tested in the inferior mesenteric ganglion and in seven neurones tested in the coeliac plexus.4. Steady-state type responses were characterized by a slowly developing membrane depolarization which reached a plateau and lasted throughout the presence of neurotensin. Amplitude and time course of this response were not altered in a solution containing hexamethonium (10 ram) and atropine (10 tM) or by a solution low in calcium (1 mM) and high in magnesium (15 mM).5. Transient type depolarizations evoked by neurotensin were faster in reaching their maximum and were followed by a repolarization during the maintained presence of neurotensin. Responses similar in time course and amplitude were obtained in solutions containing hexamethonium (10-100 /tM) and atropine (10 /IM).However, transient responses were abolished in a solution low in calcium (1 mM) and high in magnesium (15 mM) and were markedly attenuated in ganglia treated with capsaicin (3 /tM). 7. Both types of depolarizations were observed when the C-terminal hexapeptide fragment neurotensin 8-13 was used.8. It was concluded that neurotensin caused an increase in excitability in a large portion of prevertebral sympathetic neurones of guinea-pigs by interaction with receptors specific for the C-terminal, bioactive portion of the molecule. The response of the large majority of neurones was mediated through Ca2+-dependent release of a non-cholinergic excitatory transmitter from capsaicin-sensitive nerve terminals.

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“…Whether these cholinergic cells also display neuropeptide-like or GluDCase immunoreactivity is now worth exploring. The weight of available evidence indicates that CCK and SRIF are released from axon'terminals in a calcium-dependent manner (27,28), and they act as excitatory agents in the mammalian cerebral cortex (29)(30)(31). There is little information available on NPY.…”

Section: Discussionmentioning

confidence: 99%

Neuropeptide-containing neurons of the cerebral cortex are also GABAergic.

Hendry

Jones

DeFelipe

et al. 1984

Proc. Natl. Acad. Sci. U.S.A.

402

149

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Neurons in the cat and monkey cerebral cortex were stained immunocytochemically for glutamic acid decarboxylase (GluDCase; L-glutamate 1-carboxy-lyase, EC 4.1. GluDCase was co-localized with CCK, SRIF, or NPY not only in cell somata, but also in small punctate structures, which are likely to be axon terminals. From the data gained in previous electron microscopic studies, we postulate that neurons displaying GluDCase-and CCK-like immunoreactivity are a class separate from those displaying GluDCase-and SRIF-like immunoreactivity. NPY, however, is co-localized with SRIF immunoreactivity. These results imply that classes of cortical interneuron contain a conventional neurotransmitter (y-aminobutyric acid) and a neuromodulator (one of the peptides).

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The actions of motilin, luteinizing hormone releasing hormone, cholecystokinin, somatostatin, vasoactive intestinal peptide, and other peptides on rat cerebral cortical neurons

Cited by 239 publications

References 0 publications

Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels.

Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels.

The electrophysiological effects of neurotensin on neurones of guinea‐pig prevertebral sympathetic ganglia.

Neuropeptide-containing neurons of the cerebral cortex are also GABAergic.

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