Somatostatin Augments the M-Current in Hippocampal Neurons

Moore, Scott D.; Madamba, Samuel G.; Joëls, Marian; Siggins, George R.

doi:10.1126/science.2892268

Cited by 199 publications

(140 citation statements)

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“…2A,B; n = 3; see below); and (2) the magnitude, kinetics, and voltage dependence of the relaxations appear similar to those of the M-current reported previously for CA1 pyramidal neurons ( Fig. 2A; Halliwell and Adams, 1982;Moore et al, 1988a).…”

Section: Resultssupporting

confidence: 84%

“…2, 3), using commands of -5 to -25 mV. Several lines of evidence suggest, as we reported previously for CA1 pyramidal neurons (Moore et al, 1988a), that the inward relaxations represent I,: (1) the relaxations are suppressed (leaving only a "rectangular" ohmic current response) by the muscarinic agonist carbachol (20-40 PM; n = 7; Fig. 2.4) or by 1 mM Ba2-+-( Fig.…”

Section: Resultssupporting

confidence: 60%

“…Our CA3 voltage-clamn studies were done at 30-32°C.to slow down I,,, kinetics. These temperatures do not appear to alter agonist actions on I,: in a previous study, somatostatin superfusion at 35-37°C elicited the same augmenting effect on I, as at lower temperatures (Moore et al, 1988a).…”

Section: Methodsmentioning

confidence: 63%

“…We used standard intracellular recording techniques in the rat hippocampal slice, prepared as described previously (Moore et al, 1988a(Moore et al, , 1990Schweitzer et al, 1993). In brief, we cut transverse hippocampal slices (taken from male Sprague-Dawley rats of 100-l 70 gm body weight) of 350-400 urn thickness on a brain McIllwain slicer and incibated them in gassed(95% 02, 5% COz) artificial cerebrospinal fluid (ACSF) of the following composition (mM): NaCI, 130; KCl, 3.5; NaH,PO,, 1.25; MgSO,.7H,O, 1.5; CaQ, 2.0; NaHCO,, 24; glucose, 10.…”

Section: Methodsmentioning

confidence: 99%

“…A preliminary currentclamp study (Pacheco et al, 1983) in fact found evidence for such voltage-dependent dynorphin effects in CA3 pyramidal neurons. Other peptides like somatostatin can alter voltagedependent conductances such as the M-current (I, ;Brown, 1988;Jacquin et al, 1988;Moore et al, 1988a). I, is a noninactivating K+ conductance seen at slightly depolarized membrane potentials.…”

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confidence: 99%

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Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro

et al. 1994

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Opioid peptides, and especially the dynorphins, have been localized to several circuits in the CA3 hippocampal region, yet electrophysiological studies often find mixed effects of opiates on the excitability of CA3 neurons. Reasoning that these mixed effects might involve voltage-dependent actions, we tested the effect of several opiates on CA3 pyramidal neurons using single-electrode voltage-clamp recording in a slice preparation of rat hippocampus. In most CA3 neurons, the voltage-dependent K+ current known as the M-current (IM) was uniquely sensitive to the opioid peptides, with the direction of response dependent upon the opiate type and concentration. Thus, an opiate selective for kappa receptors, U-50,488H, significantly augmented IM. The kappa-selective agonists dynorphin A and dynorphin B, which exist in mossy fiber afferents to CA3 pyramidal neurons, also markedly augmented IM at low concentrations (20–100 nM). By contrast, dynorphin A at higher concentrations (1–1.5 microM) often reduced IM. Similarly, several opiates [e.g., D-Ala2,D-Leu5-enkephalin: (DADL), [D- Pen2,5]-enkephalin (DPDPE)] known to act on the delta receptor subtypes reduced the M-current, with partial reversal of this effect by naloxone. Neither the selective mu-receptor agonist [D-Ala2, NMe-Phe4, Gly-ol]-enkephalin (DAMGO) nor the nonopioid fragment of dynorphin, des- Tyr-dynorphin, consistently altered IM. These opiate effects on IM were accompanied by changes in conductance and holding current consistent with their respective effects on IM. Dynorphin A did not measurably affect the Q-current, a conductance known to contribute to inward rectification in hippocampal pyramidal neurons. The opiate effects on IM were not altered by pretreatment with Cs+ (which blocks IQ) or Ca2+ channel blockers. The opposing effects of the dynorphins (both A and B) and DADL on IM were antagonized by naloxone (1–3 microM), and the dynorphin-induced augmentations of IM were usually reversed by the kappa receptor antagonist norbinaltorphimine. These results suggest that the opiates can have opposing effects on the same voltage- dependent K+ channel type (the M channel) in the rat CA3 pyramidal neuron, with the direction of the response depending on which receptor subtype is activated. These data not only help explain the mixed effects of opiates seen in other studies, but also suggest a potential postsynaptic function for the endogenous opiates contained in the CA3 mossy fibers.

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Section: Resultssupporting

confidence: 84%

Section: Resultssupporting

confidence: 60%

Section: Methodsmentioning

confidence: 63%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro

et al. 1994

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Immunohistochemical characterization of substance P receptor (NK₁R)‐expressing interneurons in the entorhinal cortex

Wolansky

Pagliardini

Greer

et al. 2007

J of Comparative Neurology

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It has been reported that application of substance P (SP) to the medial portion of the entorhinal cortex (EC) induces a powerful antiepileptic effect (Maubach et al. [1998] Neuroscience 83:1047-1062). This effect is presumably mediated via inhibitory interneurons expressing the neurokinin-1 receptor (NK(1)R), but the existence of NK(1)R-expressing inhibitory interneurons in the EC has not yet been reported. The present immunohistochemical study was performed in the rat to examine the existence and distribution of NK(1)R-expressing neurons in the EC as well as any co-expression of other neurotransmitters/neuromodulators known to be associated with inhibitory interneurons: gamma-aminobutyric acid (GABA), parvalbumin (PARV), calretinin (CT), calbindin (CB), somatostatin (SST), and neuropeptide Y (NPY). Our results indicated that NK(1)R-positive neurons were distributed rather sparsely (especially in the medial EC), primarily in layers II, V, and VI. The results of our double-immunohistochemical staining indicated that the vast majority of NK(1)R-expressing neurons also expressed GABA, SST, and NPY. In addition, CT was co-expressed in a weakly stained subgroup of NK(1)R-expressing neurons, and CB was co-expressed very rarely in the lateral EC, but not in the medial EC. In contrast, SP-immunopositive axons with fine varicosities were distributed diffusely throughout all layers of the EC, appearing to radiate from the angular bundle. SP may be released in a paracrine manner to activate a group of NK(1)R-expressing entorhinal neurons that co-express GABA, SST, and NPY, exerting a profound inhibitory influence on synchronized network activity in the EC.

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Ultrastructural analysis of somatostatin‐immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey

Lima

Morrison

1989

J of Comparative Neurology

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Somatostatin-containing neurons and terminals have been analyzed in monkey temporal and occipital cortex by using light and electron microscopic immunohistochemistry. An antibody against Somatostatin-28, that was shown previously preferentially to label fibers (Morrison et al.: Brain Research 262:344-351, 1983), was utilized. As expected, few cell bodies were labeled. At the electron microscopic level, labeled cells presented a characteristic asymmetric position of the nucleus and very few symmetric or asymmetric synapses on the somatic surface. In all areas examined, somatostatin fibers formed a dense plexus in the most superficial layers (I-upper III). The density of labeled fibers in intermediate (deep III-IV) and deep layers (V-VI) varied considerably among areas. The synaptic relationships of the immunoreactive fibers were analyzed and postsynaptic targets quantified in V1, V2, and the superior and inferior temporal gyrus (STG and ITG, respectively). The synapses formed by somatostatin-labeled boutons were of the symmetric type (type II) and the primary postsynaptic targets were dendritic shafts. No regional differences were found in the distribution of the postsynaptic targets in layers I-upper III. The pattern of synapses in the deep layers was examined in STG. The frequency and distribution of postsynaptic targets was similar to the superficial layers of STG and the other temporal and occipital regions. In intermediate layers of the temporal cortex areas there was an increase in the proportion of synapses on dendritic spines. In a correlated light and electron microscopic analysis we examined synapses made by radial fibers in these regions and found that although the main targets are distal dendritic shafts, almost 40% of synapses were on dendritic spines. We suggest that the radial fibers may originate from a specialized interneuron, previously described as the double bouquet cell, and that this particular subset of somatostatin-containing double bouquet cells is likely to exhibit a very high degree of regional heterogeneity with a preference for association cortices with extensive corticocortical convergence.

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Somatostatin Augments the M-Current in Hippocampal Neurons

Cited by 199 publications

References 37 publications

Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro

Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro

Immunohistochemical characterization of substance P receptor (NK₁R)‐expressing interneurons in the entorhinal cortex

Ultrastructural analysis of somatostatin‐immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey

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Somatostatin Augments the M-Current in Hippocampal Neurons

Cited by 199 publications

References 37 publications

Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro

Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro

Immunohistochemical characterization of substance P receptor (NK1R)‐expressing interneurons in the entorhinal cortex

Ultrastructural analysis of somatostatin‐immunoreactive neurons and synapses in the temporal and occipital cortex of the macaque monkey

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Immunohistochemical characterization of substance P receptor (NK₁R)‐expressing interneurons in the entorhinal cortex