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PubMed1998

Synaptic responsiveness of interneurons of the cat lateral amygdaloid nucleus.

Previous work in our laboratory has revealed that the excitability of lateral amygdaloid projection neurons is tightly regulated by GABA-mediated inhibitory postsynaptic potentials and intrinsic conductances that can be activated by synaptic inputs. Here, we studied the synaptic responsiveness of lateral amygdaloid interneurons recorded intracellularly in vivo, in the cat, to investigate their role in regulating the activity of projection cells. Interneurons were identified morphologically by their aspiny dendritic trees and physiologically by their ability to generate high frequency, non-adapting spike trains in response to depolarizing current pulses. Cortical shocks of increasing intensity generated opposite response profiles in interneurons and projection cells, with interneurons becoming progressively more excited and projection cells more inhibited. These cortically-evoked response profiles paralleled the activity of interneurons and projection cells in relation to spontaneous electroencephalographic events of differing amplitudes. Only at the lowest intensities were predominantly excitatory responses elicited in both cell types. As a result, only a narrow range of low stimulus intensities could trigger spikes in projection cells. In both cell types, the initial cortically-evoked excitatory postsynaptic potential was followed by a hyperpolarization, which was of markedly lower amplitude and duration in interneurons. In interneurons, the hyperpolarization reversed at approximately -72 mV with potassium acetate pipettes and approximately -55 mV with potassium chloride pipettes, suggesting that this inhibitory postsynaptic potential is primarily mediated by a chloride conductance. In light of previous findings indicating that inhibition in the lateral amygdaloid nucleus arises mostly from local inhibitory neurons, these results suggest that interneurons are synaptically coupled via GABAA receptors. Moreover, the opposite response profiles of interneurons and projection cells to cortical shocks indicate that interneurons play a critical role in regulating the activity of projection cells. The cellular interactions evidenced in the present study suggest that the lateral amygdaloid nucleus is endowed with an inhibitory gating mechanism that regulates information flow through the amygdala.

Amygdala↗
PubMed2003

Interneurons are the source and the targets of the first synapses formed in the rat developing hippocampal circuit.

In hippocampal CA1 pyramidal neurons, GABAergic synapses are established before glutamatergic synapses. GABAergic interneurons should therefore develop and acquire synapses at an earlier stage to provide the source for GABAergic synapses. We now report that this is indeed the case. At birth and in utero, when nearly all pyramidal neurons are not yet functional, most interneurons have already either GABAergic only or GABAergic and glutamatergic postsynaptic currents. At birth, the morphological maturation of interneurons parallels their individual functional responses. In addition, the formation of functional interneurons types appears to be a sequential process. Interneurons that innervate other interneurons acquire GABA(A) synapses before peridendritic interneurons, but also before perisomatic interneurons that are not yet functional at birth. Therefore, interneurons are the source and the targets of the first synapses formed in the developing circuit. Since GABA was shown to be excitatory in utero, interneurons provide all the excitatory drive at a time when the principal cells are silent. They could therefore play a central role in the formation of the cortical circuit at early developmental stages.

Animals↗
PubMed2004

Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex.

In the primate neocortex, little is known about the possible associations between functional subclasses of GABA neurons, their morphological properties and calcium-binding protein (CaBP) content. We used whole-cell current clamp recordings, combined with intracellular labeling and fluorescence immunohistochemistry, to determine these relationships for interneurons in layers 2-3 of monkey prefrontal cortex (PFC). Eighty-one interneurons were included in the analysis. Thirty-eight of these cells showed immunoreactivity for one of the three CaBPs tested. Co-localization of more than one CaBP was not observed in any of the interneurons examined. Interneurons with different CaBPs formed distinct populations with specific physiological membrane properties and morphological features. Parvalbumin (PV)-positive cells had the physiological properties characteristic of fast-spiking interneurons (FS) and the morphology of basket or chandelier neurons. Most calretinin (CR)-containing cells had the physiological properties ascribed to non-fast-spiking cells (non-FS) and a vertically oriented axonal morphology, similar to that of double bouquet cells. Calbindin (CB)-positive interneurons also had non-FS properties and included cells with double bouquet morphology or with a characteristic dense web of axonal collaterals in layer 1. Classification of the interneurons based on cluster analysis of multiple electrophysiological properties suggested the existence of at least two distinct groups of interneurons. The first group contained mainly PV-positive FS cells and the second group consisted predominantly of CR- and CB-positive non-FS interneurons. These findings may help to illuminate the functional roles of different groups of interneurons in primate PFC circuitry.

Action Potentials↗
PubMed2000

Differential control of GABA release at synapses from distinct interneurons in rat hippocampus.

1. Paired recordings from monosynaptically connected CA3 interneurons and pyramidal cells of rat hippocampal slice cultures were used to compare the modulation of GABA release at synapses from distinct interneurons. 2. The group II metabotropic glutamate receptor (mGluR) agonist (2S,2'R,3'R)-2-(2',3'-dicarboxylcyclopropyl) glycine (DCG-IV, 5 muM) reduced the amplitude of IPSPs originating from stratum radiatum but not stratum oriens interneurons. In contrast, the GABAB receptor agonist (-)baclofen (10 muM) reduced the amplitude of unitary IPSPs elicited by all interneurons. 3. IPSPs mediated by stratum oriens interneurons were unaffected by the N-type calcium channel blocker omega-conotoxin MVIIA (1 muM) but were suppressed by the P/Q-type blocker omega-agatoxin IVA (200 nM). In contrast, IPSPs mediated by stratum radiatum interneurons were abolished by omega-conotoxin MVIIA. 4. Transmission dynamics were different at synapses from the two groups of interneurons. IPSPs mediated by stratum oriens interneurons showed marked paired-pulse depression (PPD) at intervals of 50 400 ms. IPSPs mediated by stratum radiatum interneurons showed paired-pulse facilitation (PPF) at 50 ms and PPD at longer intervals. 5. The amplitude of unitary IPSPs from all interneurons was unaffected by the GABAB receptor antagonist CGP52432 (2 muM) as was PPD at both 50 and 400 ms intervals. However, CGP52432 did reduce PPD of extracellularly evoked IPSPs. 6. Our results show that two groups of inhibitory synapses impinging onto CA3 pyramidal cells can be distinguished according to their dynamic and modulatory properties.

Animals↗
PubMed2005

Mechanisms of target-cell specific short-term plasticity at Schaffer collateral synapses onto interneurones versus pyramidal cells in juvenile rats.

Although it is presynaptic, short-term plasticity has been shown at some synapses to depend upon the postsynaptic cell type. Previous studies have reported conflicting results as to whether Schaffer collateral axons have target-cell specific short-term plasticity. Here we investigate in detail the short-term dynamics of Schaffer collateral excitatory synapses onto CA1 stratum radiatum interneurones versus pyramidal cells in acute hippocampal slices from juvenile rats. In response to three stimulus protocols that invoke different forms of short-term plasticity, we find differences in some but not all forms of presynaptic short-term plasticity, and heterogeneity in the short term plasticity of synapses onto interneurones. Excitatory synapses onto the majority of interneurones had less paired-pulse facilitation than synapses onto pyramidal cells across a range of interpulse intervals (20-200 ms). Unlike synapses onto pyramidal cells, synapses onto most interneurones had very little facilitation in response to short high-frequency trains of five pulses at 5, 10 and 20 Hz, and depressed during trains at 50 Hz. However, the amount of high-frequency depression was not different between synapses onto pyramidal cells versus the majority of interneurones at steady state during 2-10 Hz trains. In addition, a small subset of interneurones (approximately 15%) had paired-pulse depression rather than paired-pulse facilitation, showed only depression in response to the high-frequency five pulse trains, and had more steady-state high-frequency depression than synapses onto pyramidal cells or the majority of interneurones. To investigate possible mechanisms for these differences in short-term plasticity, we developed a mechanistic mathematical model of neurotransmitter release that explicitly explores the contributions to different forms of short-term plasticity of the readily releasable vesicle pool size, release probability per vesicle, calcium-dependent facilitation, synapse inactivation following release, and calcium-dependent recovery from inactivation. Our model fits the responses of each of the three cell groups to the three different stimulus protocols with only two parameters that differ with cell group. The model predicts that the differences in short-term plasticity between synapses onto CA1 pyramidal cells and stratum radiatum interneurones are due to a higher initial release probability per vesicle and larger readily releasable vesicle pool size at synapses onto interneurones, resulting in a higher initial release probability. By measuring the rate of block of NMDA receptors by the open channel blocker MK-801, we confirmed that the initial release probability is greater at synapses onto interneurones versus pyramidal cells. This provides a mechanism by which both the initial strength and the short-term dynamics of Schaffer collateral excitatory synapses are regulated by their postsynaptic target cell.

Action Potentials↗
PubMed2002

Cholinergic and nitrergic interneurones in the myenteric plexus of the human colon.

BACKGROUND: Myenteric interneurones are involved in the reflexes that control the motility of the human colon. AIMS: The distribution of choline acetyltransferase (ChAT) and nitric oxide synthase (NOS) immunoreactivity in myenteric interneurones was investigated in this study. METHODS: DiI (1,1'- didodecyl 3,3,3',3'-indocarbocyanine perchlorate) was applied to the myenteric plexus of the human colon followed by organotypic culture. Retrogradely labelled neurones, with projections longer than motor neurones (>10 mm), were studied to exclude motor neurone populations. ChAT and NOS immunoreactivity was then determined in the interneurones. RESULTS: We found that 90% of interneurones projecting orally contained ChAT and none contained NOS. Ninety five per cent of descending interneurones were labelled with ChAT and/or NOS antisera; 46% contained NOS immunoreactivity alone, 20% contained ChAT immunoreactivity alone, and 29% contained both ChAT and NOS. Anally directed interneurones had significantly longer projections than orally projecting interneurones. CONCLUSIONS: Nearly all interneurones contain either NOS or ChAT immunoreactivity. Orally projecting interneurones are of two types: 90% contain ChAT alone and the remainder contain immunoreactivity for neither ChAT nor NOS. There are three main types of anally projecting interneurones: the largest, which contains NOS but not ChAT, and the two smaller classes which contain ChAT and NOS, and CHAT alone.

Aged↗
PubMed2006

Reduced excitatory drive in interneurons in an animal model of cortical dysplasia.

Cortical dysplasia (CD) is strongly associated with epilepsy. Enhanced excitability in dysplastic neuronal networks is believed to contribute to epileptogenesis, but the underlying mechanisms for the hyperexcitability are poorly understood. Cortical GABAergic interneurons provide the principal inhibition in the neuronal networks by forming inhibitory synapses on excitatory neurons. The aim of the present study was to determine if the function of interneurons in CD is compromised. In a rat model of CD, in utero irradiation, we studied spontaneous and miniature excitatory postsynaptic currents (sEPSCs and mEPSCs) in cortical interneurons using whole cell recording techniques. Two types of interneurons, type I and type II, were identified based on their distinctive spike patterns and short-term synaptic plasticity. We found that the frequencies of sEPSCs and mEPSCs were significantly decreased in both types of interneurons in CD. However, the amplitude and kinetics of sEPSCs and mEPSCs were not different. Five-pulse, 20-Hz stimulation produced short-term depression in type I interneurons in both CD and control tissue. Type II interneurons showed a robust short-term facilitation in both CD and control tissue. Morphological analysis of biocytin-filled neurons revealed that dendritic trees of both types of interneurons were not altered in CD. Our results demonstrate that the excitatory drive, namely sEPSCs and mEPSCs, in two main types of interneuron is largely attenuated in CD, probably due to a reduction in the number of excitatory synapses on both types of interneurons in CD.

Animals↗
PubMed1977

Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat.

1. Two groups of interneurons that are involved in the organization of the lateral geniculate nucleus (LGN) are described. The cell bodies of one group lie within the LGN; these units are referred to as intrageniculate. The cell bodies of the other group are found immediately above the LGN at its border with the perigeniculate nucleus; these units are referred to as perigeniculate. 2. Intrageniculate interneurons have center-surround receptive fields that resemble those of relay (principal) cells. They can be subdivided into brisk or sluggish and sustained or transient categories. They are stimulated transsynaptically from the visual cortex and have a characteristic variation in the latency of their spike response to such stimulation both at threshold and for suprathreshold stimuli. The pathway for this stimulation appears to be via cortical efferents to the LGN. Intrageniculate interneurons receive direct, monosynaptic retinal inputs, as determined by recording simultaneously from such interneurons and from the ganglion cells which provide excitatory input to them. Similar to relay cells, they are shown to have one or two major ganglion cell inputs. 3. Perigeniculate interneurons are generally binocularly innervated and give on-off responses to small spot stimuli throughout their receptive field. They respond well to rapid movement of large targets. They respond to electrical stimulation of the retina with a spike latency that falls between that of brisk transient and brisk sustained relay cells. This latency is one synaptic delay longer than that of brisk transient relay cell activation and suggests that they are excited by axon collaterals of these relay cells. Electrical stimulation of the visual cortex is also consistent with this model; the latency of the response of perigeniculate interneurons is approximately one synaptic delay longer than the latency of the response of brisk transient relay cells. 4. The interneuronal pathways described are consistent with proposed circuits that subserve the generation of IPSPs that arise in response to optic nerve and visual cortical stimulation. We now show that such inhibition has feed-forward (intrageniculate) and feed-back (perigeniculate) components that are mediated by two different classes of geniculate interneurons. It is suggested that the intrageniculate interneurons are involved in precise, spatially organized inhibition and that the perigeniculate interneurons are part of a more general, diffuse inhibitory system that modulates LGN excitability.

Animals↗
PubMed1979

Graded synaptic interactions between local premotor interneurons of the locust.

1. Graded synaptic interactions are revealed between pairs of nonspiking, local interneurons in the metathroracic ganglion of the locust. These interneurons drive motor neurons innervating muscles of a hindleg. 2. All the interactions found between the interneurons are inhibitory and one way. Synaptic transmission is effected by the graded release of chemical transmitter. Some of the connections are apparently direct. One local interneuron can, therefore, exert a graded control over the membrane potential of another local interneuron. 3. There are inhibitory connections between local interneurons that excite the same motor neuron, between local interneurons that excite antagonistic motor neurons, and between local interneurons that excite motor neurons to muscles moving different joints of a hindleg. 4. Other pairs of interneurons, which are not connected, may be driven by common synaptic inputs. Their outputs add together at the level of the motor neurons to produce effects that are greater than the sum of their individual effects. 5. It is proposed that graded interactions between these local interneurons are an essential element in the generation of motor patterns.

Electrophysiology↗
PubMed1985

Interactions of pattern-generating interneurons controlling feeding in Lymnaea stagnalis.

Intracellular recordings were made from rhythm-generating interneurons in the Lymnaea feeding system. The feeding pattern is a three-phase rhythm of interneuronal activity (N1, N2, N3) corresponding to protraction, rasp, and swallow. We describe the firing pattern and anatomy of the premotor interneurons, each of which fires a predominant burst in only one phase of the feeding rhythm. The rhythm can be driven by steady depolarization of N1 cells. The phase of the rhythm is reset by brief stimulation of N2 or N3 interneurons. N1 neurons excite the N2 interneurons, and these in turn inhibit the N1 cells. This recurrent inhibitory pathway can account for the switch from the N1 phase of the feeding cycles to the N2 phase. The endogenous properties of the N2 interneurons are apparently responsible for the termination of N2 bursts. N3 interneurons display postinhibitory rebound (PIR), and this probably contributes to their burst after the end of the N2 inhibitory input. N2 and N3 interneurons inhibit the N1 cells. When the N3 burst dies away, activity in N1 cells resumes under the stimulus of depolarizing current. Interactions between interneurons are mainly by discrete, monophasic postsynaptic potentials, that follow 1:1. They have relatively short latency (2-12 ms) and duration (up to 100 ms). The synaptic connections between the three types of premotor interneurons are sufficient to account for the sequence of activity seen during feeding.

Action Potentials↗
PubMed1991

Representation of sensory information in the cricket cercal sensory system. I. Response properties of the primary interneurons.

1. Six different types of primary wind-sensitive interneurons in the cricket cercal sensory system were tested for their sensitivity to the orientation and peak velocity of unidirectional airflow stimuli. 2. The cells could be grouped into two distinct classes on the basis of their thresholds and static sensitivities to airflow velocity. 3. Four interneurons (the right and left 10-2 cells and the right and left 10-3 cells) made up one of the two distinct velocity sensitivity classes. The mean firing frequencies of these interneurons were proportional to the logarithm of peak stimulus velocity over the range from 0.02 to 2.0 cm/s. 4. The other two interneurons studied (left and right 9-3) had a higher air-current velocity threshold, near the saturation level of the 10-2 and 10-3 interneurons. The slope of the velocity sensitivity curve for the 9-3 interneurons was slightly greater than that for the 10-2 and 10-3 interneurons, extending the sensitivity range of the system as a whole to at least 100 cm/s. 5. All of the interneurons had broad, symmetrical, single-lobed directional sensitivity tuning curves that could be accurately represented as truncated sine waves with 360 degree period. 6. The four low-threshold interneurons (i.e., left and right 10-2 and 10-3) had peak directional sensitivities that were evenly spaced around the horizontal plane, and their overlapping tuning curves covered all possible air-current stimulus orientations. The variance in the cells' responses to identical repeated stimuli varied between approximately 10% at the optimal stimulus orientations and approximately 30% at the zero-crossing orientations. 7. The two higher threshold interneurons (left and right 9-3) had broader directional sensitivity curves and wider spacing, resulting in reduced overlap with respect to the low-threshold class.

Animals↗
PubMed1994

Rhythmic modulation of the responsiveness of locust sensory local interneurons by walking pattern generating networks.

1. Spiking local interneurons in the thoracic ganglia of the locust are known to process mechanosensory information from leg receptors and to contribute to postural reflexes. It is not clear, however, whether these interneurons are also involved in the control of leg movement during walking or whether their role in mediating local reflexes is phasically modulated by the walking pattern generating networks. To address these questions, intracellular recordings from spiking local interneurons in a midline population were made both in a "fictive walking" preparation reduced to isolated thoracic ganglia and in semi-intact locusts walking on a treadwheel. 2. In fictive walking (and therefore deafferented) preparations, rhythmic synaptic inputs were observed in 72% of the sampled local interneurons. These inputs resulted in a modulation of the interneurons' firing rate in phase with the centrally generated rhythm. A similar rhythmic drive was seen in spiking local interneurons recorded from semi-intact walking locusts. This drive persisted after amputation of the leg from which the interneurons received their sensory inputs. These results indicate that this population of interneurons receives inputs from central networks that participate in the generation of walking. 3. In fictive walking preparations where a hindleg was left attached to its segmental ganglion, individual local interneurons could be characterized physiologically by their receptive field properties. The central inputs were found to modulate the activity of members of all subclasses of interneurons (i.e., purely exteroceptive, purely proprioceptive, and with mixed receptive fields. The mode of modulation observed could oppose or assist the effect of sensory input expected to occur during normal walking.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗
PubMed1997

Regulation of excitatory input to inhibitory interneurons of the dentate gyrus during hypoxia.

The role of metabotropic glutamate receptors (mGluRs) and adenosine receptors in hypoxia-induced suppression of excitatory synaptic input to interneurons residing at the granule cell-hilus border in the dentate gyrus was investigated with the use of whole cell electrophysiological recording techniques in thin (250 microns) slices of immature rat hippocampus. Minimal stimulation evoked glutamatergic excitatory postsynaptic currents (EPSCs) in dentate interneurons in 68 +/- 4% (mean +/- SE) of trials during stimulation in the dentate granule cell layer (GCL) and 48 +/- 3% of trials during stimulation in CA3. Hypoxic episodes, produced by switching the perfusing solution from 95% O2-5% CO2 to a solution containing 95% N2-5% CO2 for 3-5 min, rapidly and reversibly decreased the synaptic reliability, or probability of evoking an EPSC, from either input without reducing EPSC amplitude, consistent with a presynaptic suppression of transmitter release. The mGluR antagonist (+)-alpha-methyl-4-carboxyphenylglycine [(+) MCPG; 500 microM] did not alter synaptic reliability or mean EPSC amplitude in either pathway. However, (+) MCPG significantly attenuated hypoxic suppression of input from both pathways, suggesting that mGluRs activated by release of glutamate partially mediate hypoxic suppression of EPSCs to dentate interneurons. The mGluR agonist (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (ACPD; 100 microM) rapidly decreased the reliability of excitatory transmission from both the GCL (19 +/- 5% of control) and CA3 (39 +/- 15% of control). ACPD also increased the frequency of spontaneous EPSCs and evoked a slow inward current in dentate interneurons. Exogenous adenosine (10-300 microM) decreased synaptic reliability for both pathways and reduced the frequency of spontaneous EPSCs, but did not cause a decrease in the mean amplitude of evoked EPSCs, consistent with a presynaptic suppression of excitatory input to dentate interneurons. Conversely, the selective adenosine A1 receptor antagonists 8-cyclopentyl-1,3-dipropylxanthine (200 nM to 1 microM) and N6-cyclopentyl-9-methyladenine (1 microM) enhanced excitatory input to dentate interneurons by increasing synaptic reliability for both the GCL and CA3 inputs. Adenosine A1 receptor antagonists did not, however, reduce hypoxic suppression of excitatory input to dentate interneurons. These results indicate that hypoxia induces a presynaptic inhibition of excitatory input to dentate interneurons mediated in part by activation of mGluRs, but not adenosine A1 receptors, whereas both mGluRs and adenosine A1 receptors can depress excitatory input to dentate interneurons during normoxic stimulation. Regulation of excitatory input to dentate interneurons provides a mechanism to shape excitatory input to the hippocampus under both normal and pathological conditions.

Animals↗
PubMed1997

Feeding stimulants activate an identified dopaminergic interneuron that induces the feeding motor program in Helisoma.

The neurotransmitter dopamine is shown to play a fundamental role in the generation of the feeding motor pattern and resultant feeding behavior in Helisoma. Application of exogenous dopamine triggered the fictive feeding motor pattern in the isolated CNS and triggered feeding movements in semi-intact preparations. Application of feeding stimulants to the oral cavity excited the putatively dopaminergic buccal interneuron N1a, and depolarization of interneuron N1a triggered the production of the fictive feeding motor pattern. The ability of dopamine superfusion and of interneuron N1a stimulation to activate the fictive feeding motor pattern was blocked by the dopamine antagonist sulpiride. The phase of the fictive feeding motor pattern was reset by brief hyperpolarization of interneuron N1a, demonstrating that interneuron N1a is an integral component of the buccal central pattern generator (CPG). During spontaneous fictive feeding patterns, prolonged hyperpolarizations of interneuron N1a inhibited the production of patterned activity. Exogenous dopamine maintained the fictive feeding motor pattern in the absence of interneuron N1a activity. Interneuron N1a was labeled by the formaldehyde-glutaraldehyde histochemical technique, which is indicative of the presence of dopamine in mollusks. These data suggest that interneuron N1a is an endogenous source of the neuromodulator dopamine, intrinsic to the buccal CPG, and that interneuron N1a has a prominent role in the sensory-motor integration triggering the consummatory response.

Animals↗
PubMed1997

Interneurons in area CA1 stratum radiatum and stratum oriens remain functionally connected to excitatory synaptic input in chronically epileptic animals.

Past work has demonstrated a reduction of stimulus-evoked inhibitory input to hippocampal CA1 pyramidal cells in chronic models of temporal lobe epilepsy (TLE). It has been postulated that this reduction in inhibition results from impaired excitation of inhibitory interneurons. In this report, we evaluate the connectivity of area CA1 interneurons to their excitatory afferents in hippocampal-parahippocampal slices obtained from a rat model of chronic TLE. Rats were made chronically epileptic by a period of continuous electrical stimulation of the hippocampus, which establishes an acute condition of self-sustained limbic status epilepticus (SSLSE). This period of SSLSE is followed by a development of chronic recurrent spontaneous limbic seizures that are associated with chronic neuropathological changes reminiscent of those encountered in human TLE. Under visual control, whole cell patch-clamp recordings of interneurons and pyramidal cells were obtained in area CA1 of slices taken from adult, chronically epileptic post-SSLSE rats. Neurons were activated by means of electrodes positioned in stratum radiatum. Intrinsic membrane properties, including resting membrane potential, action potential (AP) threshold, AP half-height width, and membrane impedance, were unchanged in interneurons from chronically epileptic (post-SSLSE) tissue compared with control tissue. Single stimuli delivered to stratum radiatum evoked depolarizing excitatory postsynaptic potentials and APs in interneurons, whereas paired-pulse stimulation evoked facilitation of the postsynaptic current (PSC) in both control and post-SSLSE tissue. No differences between interneurons in control versus post-SSLSE tissue could be found with respect to the mean stimulus intensity or mean stimulus duration needed to evoke an AP. A multiple linear regression analysis over a range of stimulus intensities demonstrated that a greater number of APs could be evoked in interneurons in post-SSLSE tissue compared with control tissue. Spontaneous PSCs were observed in area CA1 interneurons in both control and post-SSLSE tissue and were markedly attenuated by glutamatergic antagonists. In conclusion, our data suggest that stimulus-evoked and spontaneous excitatory synaptic input to area CA1 interneurons remains functional in an animal model of chronic temporal lobe epilepsy. These findings suggest, therefore, that the apparent decrease of polysynaptic inhibitory PSPs in CA1 pyramidal cells in epileptic tissue is not due to a deficit in excitatory transmission from Schaffer collaterals to interneurons in stratum radiatum and straum oriens.

Animals↗
PubMed1997

Hippocampal interneurons are excited via serotonin-gated ion channels.

Hippocampal interneurons are excited via serotonin-gated ion channels. J. Neurophysiol. 78: 2493-2502, 1997. Serotonergic neurons of the median raphe nucleus heavily innervate hippocampal GABAergic interneurons located in stratum radiatum of area CA1, suggesting that this strong subcortical projection may modulate interneuron excitability. Using whole cell patch-clamp recording from interneurons in brain slices, we tested the effects of serotonin (5-HT) on the physiological properties of these interneurons. Serotonin produces a rapid inward current that persists when synaptic transmission is blocked by tetrodotoxin and cobalt, and is unaffected by ionotropic glutamate and gamma-aminobutyric acid (GABA) receptor antagonists. The 5-HT-induced current was independent of G-protein activation. Pharmacological evidence indicates that 5-HT directly excites these interneurons through activation of 5-HT3 receptors. At membrane potentials negative to -55 mV, the current-voltage (I-V) relationship of the 5-HT current displays a region of negative slope conductance. Therefore the response of interneurons to 5-HT strongly depends on membrane potential and increases greatly as cells are depolarized. Removal of extracellular calcium, but not magnesium, increases the amplitude of 5-HT-induced currents and removes the region of negative slope conductance, thereby linearizing the I-V relationship. The axons of 5-HT-responsive interneurons ramify widely within CA1; some of these interneurons also project to and arborize extensively in the dentate gyrus. The organization of these inhibitory connections strongly suggests that these cells regulate excitability of both CA1 pyramidal cells and dentate granule cells. As our results indicate that 5-HT may mediate fast excitatory synaptic transmission onto these interneurons, serotonergic inputs can simultaneously modulate the output of both hippocampus and dentate gyrus.

Animals↗
PubMed1998

Cooperative mechanisms between leg joints of Carausius morosus I. Nonspiking interneurons that contribute to interjoint coordination.

Three nonspiking interneurons are described in this paper that influence the activity of the motor neurons of three muscles of the proximal leg joints of the stick insect. Interneurons were recorded and stained intracellularly by glass microelectrodes; motor neurons were recorded extracellularly with oil-hook electrodes. The motor neurons innervate the two subcoxal muscles, the protractor and retractor coxae, and the thoracic part of the depressor trochanteris muscle. The latter spans the subcoxal joint before inserting the trochanter, thus coupling the two proximal joints mechanically. The three interneurons are briefly described here. First, interneuron NS 1 was known to become more excited during the swing phase of the rear and the stance phase of the middle leg. When depolarized it excited several motor neurons of the retractor coxae. This investigation revealed that it inhibits the activity of protractor and thoracic depressor motor neurons when depolarized as well. In a pilocarpine-activated animal, the membrane potential showed oscillations in phase with the activity of protractor motor neurons, suggesting that NS 1 might contribute to the transition from swing to stance movement. Second, interneuron NS 2 inhibits motor neurons of protractor and thoracic depressor when depolarized. In both a quiescent and a pilocarpine-activated animal, hyperpolarizing stimuli excite motor neurons of both muscles via disinhibition. In one active animal the disinhibiting stimuli were sufficient to generate swing-like movements of the leg. In pilocarpine-activated preparations the membrane potential oscillated in correlation with the motor neuronal activity of the protractor coxae and thoracic depressor muscle. Hyperpolarizing stimuli induced or reinforced the protractor and thoracic depressor bursts and inhibited the activity of the motor neurons of the retractor coxae muscle, the antagonistic muscle of the protractor. Therefore interneuron NS 2 can be regarded as an important premotor interneuron for the switching from stance to swing and from swing to stance. Finally, interneuron NS 3 inhibits the spontaneously active motor neurons of both motor neuron pools in the quiescent animal. During pilocarpine-induced protractor bursts, depolarizing stimuli applied to the interneuron excited several protractor motor neurons with large action potentials and one motor neuron of the thoracic depressor. No oscillations of the membrane potentials were observed. Therefore this interneuron might contribute to the generation of rapid leg movements. The results demonstrated that the two proximal joints are coupled not only mechanically but also neurally and that the thoracic part of the depressor appears to function as a part of the swing-generating system.

Animals↗
PubMed1999

An intrinsic oscillation in interneurons of the rat lateral geniculate nucleus.

By using the whole cell patch recording technique in vitro, we examined the voltage-dependent firing patterns of 69 interneurons in the rat dorsal lateral geniculate nucleus (LGN). When held at a hyperpolarized membrane potential, all interneurons responded with a burst of action potentials. In 48 interneurons, larger current pulses produced a bursting oscillation. When relatively depolarized, some interneurons produced a tonic train of action potentials in response to a depolarizing current pulse. However, most interneurons produced only oscillations, regardless of polarization level. The oscillation was insensitive to the bath application of a combination of blockers to excitatory and inhibitory synaptic transmission, including 30 microM 6,7-dinitroquinoxaline-2,3-dione, 100 microM (+/-)-2-amino-5-phosphonopentanoic acid, 20 microM bicuculline, and 2 mM saclofen, suggesting an intrinsic event. The frequency of the oscillation in interneurons was dependent on the intensity of the injection current. Increasing current intensity increased the oscillation frequency. The maximal frequency of the oscillation was 5-15 Hz for most cells, with some ambiguity caused by the difficulty of precisely defining a transition from oscillatory to regular firing behavior. In contrast, the interneuron oscillation was little affected by preceding depolarizing and hyperpolarizing pulses. In addition to being elicited by depolarizing current injections, the oscillation could also be initiated by electrical stimulation of the optic tract when the interneurons were held at a depolarized membrane potential. This suggests that interneurons may be recruited into thalamic oscillations by synaptic inputs. These results indicate that interneurons may play a larger role in thalamic oscillations than was previously thought.

Action Potentials↗