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PubMed1997

Appositions made by axons of descending interneurons in the guinea-pig small intestine, investigated by confocal microscopy.

There are four major classes of descending interneurons in the myenteric plexus of the guinea-pig small intestine. In this study, the connections made by two of these classes of descending interneurons with other interneurons and with inhibitory motor neurons have been investigated using confocal, conventional fluorescence and electron microscopy. The terminals of descending interneurons known to contain both bombesin (BN) and nitric oxide synthase (NOS) were identified by BN immunoreactivity (IR). Cholinergic interneurons known to contain somatostatin (SOM) were identified by SOM-IR. The connections of these two groups of interneurons with the following three classes of nerve cell bodies were examined: those with NOS-IR that also contain gamma-aminobutyric acid (GABA) (inhibitory motor neurons), those with only NOS-IR (descending interneurons and inhibitory motor neurons) and those with only GABA-IR (motor neurons). The BN-IR and SOM-IR interneurons were found to form connections with each other, and both types of interneurons provided inputs to motor neurons. Most previous analyses of interconnections in the enteric plexuses have been by conventional fluorescence microscopy and electron microscopy. In the present work these are compared with confocal microscopy. BN-IR varicosities formed pericellular baskets around each class of nerve cell that were easily identifiable with all techniques. Using confocal microscopy, BN-IR varicosities that were in contact with NOS-IR and GABA-IR nerve cells were quantified. Confocal microscopy demonstrated over twice as many contacts as were shown by a previous electron microscopic study. In contrast, conventional fluorescence microscopy showed little indication that SOM-IR varicosities formed inputs to NOS-IR or GABA-IR nerve cells, despite the fact that confocal microscopy revealed direct appositions and electron microscopy revealed synapses. This study has shown that confocal analysis is a valuable adjunct to conventional fluorescence microscopy for determining neuronal circuitry. Moreover, it allows a more rapid collection of data than does electron microscopy. It is concluded that chains of BN-IR and SOM-IR interneurons from descending pathways in the small intestine and that both types of interneuron connect with muscle motor neurons.

Animals↗

PubMed2001

Ubiquitin immunoreactivity in presumed spinal interneurones in motor neurone disease.

Previous studies have demonstrated the presence of ubiquitin-immunoreactivity (Ub-IR) as inclusions and skeins in motor neurones of both the familial and sporadic forms of motor neurone disease (MND). There is evidence that interneurones also degenerate in MND, but Ub-IR in ventral horn spinal interneurones has not been studied previously. Here, Ub-IR was investigated in 1445 presumed interneurones and 1086 presumed motor neurones counted in three random 20-microm sections of the ventral horn of the third lumbar segment of the spinal cord of each of seven controls and seven patients with MND. The ventral horn was divided into four quadrants; the dorsomedial quadrant contains almost exclusively interneurones and the ventrolateral quadrant largely motor neurones. The neurones were also classified by morphological and size criteria into presumed interneurones (< 25 microm) and presumed motor neurones (>or= 25 microm). Ub-IR was classified as inclusions, skeins and dispersed cytoplasmic and nuclear staining. Ub-IR inclusions or skeins were not observed in the controls but 6.6% of neurones (motor neurones and interneurones) showed the presence of dispersed cytoplasm staining and nuclear staining. The incidence of Ub-IR cytoplasmic and nuclear staining was significantly greater in both motor neurones and interneurones of MND patients than controls. Ub-IR was less frequent in MND cases in which a great loss of neurones was observed. Ub-IR was significantly more frequent in motor neurones than interneurones, both in patients and controls. Ub-IR inclusions and skeins were only observed in motor neurones from MND patients. Ub-IR inclusions were not observed in presumed spinal interneurones, while skeins were only seen in three out of 565 of these cells (two of them in the dorsomedial quadrant) in two out of seven patients. Thus, although presumed spinal interneurones occasionally revealed Ub-IR features similar to motor neurones, the rare staining of Ub-IR skeins and the lack of Ub-IR inclusions in interneurones in MND suggests that these neurones only occasionally form ubiquitin-protein conjugates. Neuronal size, rather than type, may be important in determining whether ubiquitin-protein conjugates form in the ventral horn neurones in MND.

Aged↗

PubMed2003

The physiological and morphological characteristics of interneurons caudal to the trigeminal motor nucleus in rats.

In this study we have characterized the membrane properties and morphology of interneurons which lie between the caudal pole of the trigeminal motor nucleus and the rostral border of the facial motor nucleus. Previous studies suggest that many of these interneurons may participate in the genesis of rhythmical jaw movements. Saggital brainstem slices were taken from rats aged 5-8 days. Interneurons lying caudal to the trigeminal motor nucleus were visualized using near-infrared differential interference contrast (DIC) microscopy, and were recorded from using patch pipettes filled with a K-gluconate- and biocytin-based solution. The 127 neurons recorded could be categorized into three subtypes on the basis of their responses to injection of depolarizing current pulses, namely tonic firing (type I), burst firing (type II) and spike-adaptive (type III) neurons. Type I interneurons had a higher input resistance and a lower rheobase than type II neurons. All three neuron subtypes showed 'sag' of the voltage response to injection of large-amplitude hyperpolarizing current pulses, and, in addition, also showed rectification of the voltage response to injection of depolarizing current pulses, with type II neurons showing significantly greater rectification than type I neurons. The axonal arborizations were reconstructed for 44 of 63 neurons labelled with tracer. Neurons of each subtype were found to issue axon collaterals terminating in the brainstem nuclei, including the parvocellular reticular nucleus (PCRt), the trigeminal motor nucleus (Vmot), the supratrigeminal nucleus or the trigeminal mesencephalic nucleus. Twenty-five of the 43 neurons issued collaterals which terminated in the Vmot and the other brainstem nuclei. When viewed under 100x magnification, the collaterals of some interneurons were seen to give off varicosities and end-terminations which passed close to the somata of unidentified neurons in the trigeminal motor nucleus and in the area close to the interneuron soma itself. This suggests that the interneurons may make synaptic contacts both on motoneurons and also on nearby interneurons. These results provide data on the membrane properties of trigeminal interneurons and evidence for their synaptic connections both with nearby interneurons and also with motoneurons. Thus, the interneurons examined could play roles in the shaping, and possibly also in the generation, of rhythmical signals to trigeminal motoneurons.

Anesthetics, Local↗

PubMed1983

Inhibitory interactions between interneurones in reflex pathways from group Ia and group Ib afferents in the cat.

A hypothesis has been verified that laminae V-VI interneurones which mediate non-reciprocal inhibition of motoneurones from group I muscle afferents have collateral actions on other laminae V-VI interneurones. Stimulation within the areas of projection of these inhibitory interneurones in motor nuclei and in Clarke's column would be expected to give rise to monosynaptic i.p.s.p.s in interneurones with disynaptic i.p.s.p.s from group I afferents if the hypothesis were correct. Intracellular records were made from eighty-five laminae V-VI interneurones with input from group Ia muscle spindle and/or group Ib tendon organ afferents. Weak intraspinal stimuli applied in motor nuclei in L7 and S1 segments, or in the lateral funiculus just caudal to Clarke's column in L4, were found to evoke monosynaptic i.p.s.p.s in seventy-two interneurones. These i.p.s.p.s were systematically correlated with disynaptic inhibition from group Ia or Ib afferents but not from other fibres. Such monosynaptic i.p.s.p.s evoked by intraspinal stimuli were seen in forty-two interneurones which themselves projected to the level of Clarke's column and therefore (on the basis of previous evidence) should mediate inhibition of motoneurones. For seven of these interneurones it was also shown directly that they projected to motor nuclei. The inhibition of such interneurones demonstrates mutual interactions between those interneurones which are interposed in inhibitory pathways from group I afferents. Only indirect indications have been obtained for inhibition of interneurones in the excitatory pathways.

Animals↗

PubMed1993

Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus.

1. Whole-cell recordings were made from interneurons located within CA3 stratum radiatum of neonate rat hippocampal slices. All experiments were performed in the continued presence of tetrodotoxin (1 microM) and bicuculline (5 microM) to permit the isolation of spontaneous miniature excitatory synaptic currents (mEPSCs). 2. Two distinct populations of interneurones were identified based on current-voltage relations of kainate and the kinetic properties of spontaneous mEPSCs. These cell types were classified as type I and type II interneurones. 3. The I-V relation of kainate in type I cells was linear or modestly outwardly rectifying. Currents reversed polarity close to 0 mV. The kainate I-V relationship in type II interneurones was strongly inwardly rectifying with little or no outward current passed at potentials up to +50 mV. 4. Spontaneous mEPSCs were observed at a low frequency. At -70 mV mEPSCs received by type I interneurones had fast rise times (approximately 1 ms) and decay time constants (approximately 5 ms) and were mediated by alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptors. Miniature EPSCs on type I interneurones reversed polarity at approximately 0 mV. At +50 mV the kinetics of the mEPSCs on type I interneurones were slowed and comprised both AMPA and N-methyl-D-aspartate (NMDA) receptor-mediated components as revealed by their sensitivity to 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and D-2-amino-5-phosphonovaleric acid (D-APV). 5. The kinetics of spontaneous mEPSCs on type II cells were slower than their type I counterparts at -70 mV. Spontaneous mEPSCs received by type II interneurones showed extreme inward rectification with no cells possessing fast events at +50 mV. In a few cells slowly rising and slowly falling spontaneous mEPSCs were observed at positive holding potentials. These events were abolished by D-APV and were therefore mediated solely by NMDA receptor activation. 6. Type I or type II interneurones filled with Lucifer Yellow or biocytin possessed similar morphologies. Both cell types were typically large triangular cells with three to six branching dendrites often possessing varicosities. The dendrites of these interneurones arborized throughout strata radiatum, pyramidale, oriens and the molecular layer of the dentate gyrus. 7. In the majority of interneurones (both type I and II) the rise times of individual mEPSCs were correlated with their half-width and decay time constant, suggesting that the shape of the mEPSC is in part determined by the dendritic origin of the synaptic input.(ABSTRACT TRUNCATED AT 400 WORDS)

2-Amino-5-phosphonovalerate↗

PubMed1995

Interneurones mediating presynaptic inhibition of group II muscle afferents in the cat spinal cord.

1. To investigate whether dorsal horn interneurones with input from group II muscle afferents induce depolarization of sensory fibres, simultaneous recordings were made from single interneurones in the sacral segments and from sacral dorsal root filaments using the spike-triggered averaging technique. 2. The spike potentials of eighteen out of thirty-eight interneurones tested were followed by dorsal root potentials (DRPs). The DRPs occurred at latencies of 2 and 6-8 ms. Interneurones evoking DRPs at latencies of up to 2 ms are considered likely to be last-order interneurones in pathways of presynaptic inhibition, while those inducing DRPs at longer latencies are considered likely to be first-order interneurones. The former were activated by peripheral afferents with somewhat longer latencies than the latter. However, all interneurones were co-activated by group II muscle and cutaneous afferents, indicating that the depolarization of group II muscle afferents, which these afferents induce, may be mediated by the same interneurones. 3. DRPs evoked by electrical stimulation of peripheral nerves were recorded from both sacral and midlumbar dorsal root filaments. The amplitudes of these DRPs were closely related to the potency with which group II afferents of various nerves activate dorsal horn interneurones in the sacral and midlumbar segments and group II afferents contributed to them more effectively than group I afferents. The second stimulus in a train was more effective than the first, while a third stimulus had little additional effect, indicating that the interneurones involved are relatively easily activated. 4. Intraspinal stimuli applied within the dorsal horn, at the sites where the largest field potentials of group II origin were recorded, evoked distinct DRPs. However, the location of the first- and last-order interneurones in pathways of primary afferent depolarization (PAD) could not be differentiated by this approach because the same stimuli induced positive potentials, which masked the onset of DRPs and precluded localization of the sites from which DRPs might be evoked monosynaptically.

Afferent Pathways↗

PubMed1996

Effects of stimulation of phrenic afferents on cervical respiratory interneurones and phrenic motoneurones in cats.

1. In ten decerebrate, paralysed and ventilated cats, we tested the hypothesis that cervical (C5) respiratory interneurones mediate inhibition of phrenic motoneurone activity resulting from single shocks to the phrenic nerve. 2. Stimulus intensities sufficient to activate all afferents elicited (latency, 4.0 +/- 0.9 ms, mean +/- S.D.) a graded suppression of ipsilateral, but not contralateral (five of seven cats) phrenic nerve activity lasting, in six of seven cats, more than 70 ms and interrupted by a brief (approximately 6-18 ms duration) excitation at latencies between 7 and 30 ms. 3. In twenty-five ipsilateral motoneurones, peristimulus time average of the membrane potentials (-61 +/- 10 mV) showed no effect in eleven; of the fourteen that responded, ten had initial EPSPs (latency, 17.6 +/- 3.0 ms) and four initial IPSPs (latencies, 2.25-4.3 ms). Only one motoneurone had both. No responses with latencies > 60 ms were observed. 4. Peristimulus time averages of extracellular activity of thirty ipsilateral interneurones, twenty-five firing in inspiration (I) and five in expiration (E), showed diverse responses. The initial response of I interneurones was an excitation in eleven, a suppression of activity in nine, and no response in five. Latencies of excitations ranged from 2 to 36.5 ms (median, 14 ms) with durations ranging from 2 to 7 ms (mean, 4.4 +/- 1.6 ms). Latencies of suppression of activity ranged from 2 to 29 ms (median, 10 ms). Two E interneurones were excited (latencies, 11 and 15 ms; durations, 3.5 and 2 ms), two inhibited (latencies, 2 and 12 ms; durations, > 40 and 17 ms, respectively), and one did not respond. 5. In nine interneurones (seven I, two E), peristimulus time averages of the membrane potentials (mean, -62 +/- 14 mV) revealed no effect on three (all I). Of the six that responded, four (three I) had initial IPSPs, two (one I, one E) initial EPSPs. EPSPs had latencies of 11.5 (I interneurone) and 22 ms (E interneurone); the latencies of the IPSPs were 2.75, 3.20, and 2.3 ms for the I interneurones and 15.9 ms for the E interneurone). No responses with latencies > 30 ms were observed. 6. The diverse responses of cervical respiratory interneurones indicates that they do not mediate the prolonged suppression of ipsilateral phrenic activity elicited by stimulation of phrenic afferents. The suppression may result from activation of normally quiescent inhibitory interneurones or from presynaptic inhibition.

Animals↗

PubMed1997

Synchronization of GABAergic interneuronal network in CA3 subfield of neonatal rat hippocampal slices.

1. Cell-attached and whole-cell recordings from interneurons localized in the stratum radiatum of the CA3 subfield (SR-CA3) of neonatal (postnatal days 2-5) rat hippocampal slices were performed to study their activity during the generation of GABAergic giant depolarizing potentials (GDPs) in CA3 pyramidal cells. 2. Dual recordings revealed that during the generation of GDPs in CA3 pyramidal cells, the interneurons fire bursts of spikes, on average 4.5 +/- 1.4 spikes per burst (cell-attached mode). There bursts were induced by periodical large inward currents (interneuronal GDPs) recorded in whole-cell mode. 3. Interneuronal GDPs revealed typical features of polysynaptic neuronal network-driven events: they were blocked by TTX and by high divalent cation medium and they could be evoked in an all-or-none manner by electrical stimulation in different regions of the hippocampus. The network elements required for the generation of GDPs are present in local CA3 circuits since spontaneous GDPs were present in the isolated CA3 subfield of the hippocampal slice. 4. Interneuronal GDPs were mediated by GABAA and glutamate receptors, since: (i) their reversal potential strongly depended on [Cl-]i; (ii) at the reversal potential of GABAA postsynaptic currents an inward component of GDPs was composed of events with the same kinetics as alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor-mediated EPSCs; and (iii) once GABAA receptors were blocked intracellularly by dialysis with F(-)-MgATP-free solution, the remaining component of interneuronal GDPs reversed near 0 mV and rectified at membrane potentials more negative than -20 mV, suggesting an important contribution of NMDA receptors in addition to AMPA receptors. 5. In cell-attached recordings from interneurons, electrical stimulation in the stratum radiatum evoked a burst of spikes that corresponded to evoked GDPs. Pharmacological study of this response revealed that excitation of SR-CA3 interneurons during GDPs is determined by the co-operative depolarizing actions mediated by GABAA and glutamate (AMPA and NMDA) receptors. Interestingly, after blockade of AMPA receptors, GABAA receptor-mediated depolarization enabled the activation of NMDA receptors presumably via attenuation of their voltage-dependent magnesium block. 6. It is concluded that synchronous activation of SR-CA3 interneurons during generation of GDPs is mediated synaptically and is determined by the co-operation of (i) excitatory GABAergic connections between interneurons and (ii) glutamatergic connections to interneurons originating presumably from the pyramidal cells.

Animals↗

PubMed2003

Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from feline group II muscle afferents.

Previous studies have demonstrated that group II muscle afferents exert powerful actions on contralateral motoneurones and that these actions are mediated primarily via lamina VIII commissural interneurones. We examined whether dorsal horn interneurones also contribute to these actions, as they have been shown to contribute to the actions of group II afferents on ipsilateral motoneurones. We tested the susceptibility of IPSPs and EPSPs evoked from group II afferents in contralateral motoneurones to presynaptic inhibition as an indicator of the relative contribution of dorsal horn interneurones to these PSPs, since the monosynaptic activation of dorsal horn interneurones is more weakly and more briefly depressed by presynaptic inhibition than is the monosynaptic activation of lamina VIII and other intermediate zone and ventral horn interneurones. While the earliest components of IPSPs and EPSPs evoked by group II afferents were abolished by conditioning stimulation of group II afferents, consistent with them being evoked disynaptically by commissural interneurones, trisynaptic components of these PSPs were only partly reduced and are therefore attributed to dorsal horn interneurones. The same conditioning stimuli depressed the disynaptic excitation of lamina VIII commissural interneurones by group II afferents much less effectively than they depressed monosynaptic excitation, indicating that dorsal horn interneurones contribute to this disynaptic excitation. On the basis of these observations we conclude that that dorsal horn interneurones contribute to the late actions of group II muscle afferents on contralateral motoneurones through their disynaptic actions on commissural interneurones.

Animals↗

PubMed1983

Interneurons mediating fast postsynaptic inhibition in pyriform cortex of the rabbit.

Interneurons mediating the fast IPSPs in principal cells in the pyriform cortex (PC) of the rabbit were searched for using criteria derived from the analysis of the properties of the fast inhibitory postsynaptic potentials (IPSPs). Thirty units were identified as inhibitory interneurons. The interneurons were activated synaptically by volleys from the olfactory bulb (OB), the lateral olfactory tract (LOT), the anterior commissure (AC), and deep-lying structures of the PC (DPC). The interneurons showed a tendency to discharge repetitively in response to shocks applied to these structures of the basal forebrain (OB, LOT, AC, and DPC). The conditioning OB shocks eliminated the testing LOT-evoked discharges of the interneurons. The conditioning OB shocks eliminated the initial part of the testing OB-evoked discharges, leaving the later part relatively unchanged. On the other hand, the conditioning OB shocks did not completely eliminate the testing DPC- or AC-evoked discharges. A temporal facilitation of discharges in the interneurons was observed in response to volleys from the OB, DPC, or AC. A spatial facilitation of discharges in the interneurons was observed in response to a combination of shocks applied to the OB, DPC, and AC. The interneurons were recorded at depths 525-2,755 microns deep to the turnover point of the component 2 wave of field potentials evoked by volleys through the LOT fibers. They were located mostly in the deeper part of layer III of the PC. Intracellular recordings from the presumed inhibitory interneurons showed that OB stimulation elicited two successive excitatory postsynaptic potentials (EPSPs) on which the bursting discharges were superimposed. These EPSPs were followed by a long-lasting hyperpolarizing potential. A comparison of the latencies of the antidromic activation of the principal cells and the synaptic activation of the inhibitory interneurons following OB or DPC stimulation suggested that the inhibitory interneurons are activated at least partly through the axon collaterals of the principal cells, which project their main axons to the OB or DPC. A circuit diagram was proposed for the neuronal pathways responsible for the fast IPSPs of principal cells in the PC.

Animals↗

PubMed2006

Layer positioning of late-born cortical interneurons is dependent on Reelin but not p35 signaling.

We tested the response of interneurons to the absence of Reelin signaling or p35 in the mouse neocortex. We provide three independent strands of evidence to demonstrate that layering of late-born (but not early-born) interneurons is regulated by Reelin signaling. First, early-born and late-born interneurons behaved differently in mice lacking Reelin or disabled 1 (Dab1). Early-born interneurons showed layer inversion, whereas late-born interneurons did not demonstrate layer inversion but were randomly distributed across the cortex. Second, in p35 mutant brains (in which Reelin signaling is intact), late-born interneurons are appropriately positioned in the upper layers despite the malpositioning of all other cortical neurons in these mice. Third, transplanted late-born interneuron precursors (wild type) into Dab1(-/-) cortices showed appropriate upper layer segregation. Together, these results indicate that, in the absence of Reelin signaling, late-born interneurons fail to laminate properly, and this is restored in an environment in which Reelin signaling is intact. These studies suggest different mechanisms for the stratification of cortical interneurons. Whereas the early-born interneurons appear to be associated with projection neuron layering, late-born interneurons rely on Reelin signaling for their correct lamination.

Animals↗

PubMed2004

Origins of cortical interneuron subtypes.

Cerebral cortical functions are conducted by two general classes of neurons: glutamatergic projection neurons and GABAergic interneurons. Distinct interneuron subtypes serve distinct roles in modulating cortical activity and can be differentially affected in cortical diseases, but little is known about the mechanisms for generating their diversity. Recent evidence suggests that many cortical interneurons originate within the subcortical telencephalon and then migrate tangentially into the overlying cortex. To test the hypothesis that distinct interneuron subtypes are derived from distinct telencephalic subdivisions, we have used an in vitro assay to assess the developmental potential of subregions of the telencephalic proliferative zone (PZ) to give rise to neurochemically defined interneuron subgroups. PZ cells from GFP+ donor mouse embryos were transplanted onto neonatal cortical feeder cells and assessed for their ability to generate specific interneuron subtypes. Our results suggest that the parvalbumin- and the somatostatin-expressing interneuron subgroups originate primarily within the medial ganglionic eminence (MGE) of the subcortical telencephalon, whereas the calretinin-expressing interneurons appear to derive mainly from the caudal ganglionic eminence (CGE). These results are supported by findings from primary cultures of cortex from Nkx2.1 mutants, in which normal MGE fails to form but in which the CGE is less affected. In these cultures, parvalbumin- and somatostatin-expressing cells are absent, although calretinin-expressing interneurons are present. Interestingly, calretinin-expressing bipolar interneurons were nearly absent from cortical cultures of Dlx1/2 mutants. By establishing spatial differences in the origins of interneuron subtypes, these studies lay the groundwork for elucidating the molecular bases for their distinct differentiation pathways.

Animals↗

PubMed2000

Differential expression of group I metabotropic glutamate receptors in functionally distinct hippocampal interneurons.

Metabotropic glutamate receptors (mGluRs) have been proposed to be involved in oscillatory rhythmic activity in the hippocampus. However, the subtypes of mGluRs involved and their precise distribution in different populations of interneurons is unclear. In this study, we combined functional analysis of mGluR-mediated inward currents in CA1 oriens-alveus interneurons with anatomical and immunocytochemical identification of these interneurons and expression analysis of group I mGluR using single-cell reverse transcription-PCR (RT-PCR). Four major interneuron subtypes could be distinguished based on the mGluR-mediated inward current induced by the application of 100 microm trans-(1S,3R)-1-aminocyclopentane-1, 3-dicarboxylic acid (ACPD) under voltage-clamp conditions and the action potential firing pattern under current-clamp conditions. Type I interneurons responded with a large inward current of approximately 224 pA, were positive for somatostatin, and the majority expressed both mGluR1 and mGluR5. Type II interneurons responded with an inward current of approximately 80 pA, contained calbindin, and expressed mainly mGluR1. Type III interneurons responded with an inward current of approximately 60 pA. These interneurons were fast-spiking, contained parvalbumin, and expressed mainly mGluR5. Type IV interneurons did not respond with an inward current upon application of ACPD, yet they expressed group I mGluRs. Activation of group I mGluRs under current-clamp conditions increased spike frequency and resulted in rhythmic firing activity in type I and II, but not in type III and IV, interneurons. RT-PCR results suggest that activation of mGluR1 in the subsets of GABAergic interneurons, classified here as type I and II, may play an important role in mediating synchronous activity.

2-Amino-5-phosphonovalerate↗

PubMed2000

Origin and molecular specification of striatal interneurons.

The striatum, the largest component of the basal ganglia, contains projection neurons and interneurons. Whereas there is considerable agreement that the lateral ganglionic eminence (LGE) is the origin of striatal projection neurons, less is known about the origin of striatal interneurons. Using focal injections of retrovirus into the ventral telencephalon in vitro, we demonstrate that most striatal interneurons tangentially migrate from the medial ganglionic eminence (MGE) or the adjacent preoptic/anterior entopeduncular areas (POa/AEP) and express the NKX2.1 homeodomain protein. Although the majority of striatal interneurons (cholinergic, calretinin(+), and parvalbumin(+)) maintain the expression of NKX2.1 into adulthood, most of the interneurons expressing somatostatin (SOM), neuropeptide Y (NPY), and neural nitric oxide synthase (NOS) appear to downregulate the expression of NKX2.1 as they exit the neuroepithelium. Analysis of striatal development in mice lacking Nkx2.1 suggests that this gene is required for the specification of nearly all striatal interneurons. Similar analysis of mice lacking the Mash1 basic helix-loop-helix (bHLH) or both the Dlx1 and Dlx2 homeodomain transcription factors demonstrates that these genes are required for the differentiation of striatal interneurons. Mash1 mutants primarily have a reduction in early-born striatal interneurons, whereas Dlx1/2 mutants primarily have reduced numbers of late-born striatal interneurons. We also present evidence implicating the Lhx6 and Lhx7 LIM-homeobox genes in the development of distinct interneuron subtypes. Finally, we hypothesize that, within the MGE, radially migrating cells generally become projection neurons, whereas tangentially migrating cells mainly form interneurons of the striatum and cerebral cortex.

Animals↗

PubMed1992

Reliability and effectiveness of transmission from exteroceptive sensory neurons to spiking local interneurons in the locust.

Mechanosensory information from exteroceptive hairs on the legs of a locust is first processed in a segmental ganglion by a midline population of spiking local interneurons for use in adjustments of posture and locomotion. Each interneuron receives excitatory inputs from a characteristic array of these receptors so that the surface of a leg is mapped onto the whole population of interneurons as a series of overlapping receptive fields. The properties of this first synaptic connection, and the contributions of individual afferents forming the receptive fields of the interneurons are examined. The gain of the excitatory synaptic connection between the hair afferents and the interneurons is often high, so that a single afferent spike can lead directly to a spike in the interneuron. Repetitive spikes in a hair afferent evoke EPSPs in an interneuron that decline in amplitude but that may summate. The first EPSP in any sequence is always the largest. The high frequencies of afferent spikes that are evoked by a normal deflection of a hair saturate the synaptic connection so that the amplitude of depolarization is no greater than to a single spike. The EPSPs from two hairs in a receptive field can summate but lead to no heterosynaptic facilitation. High-frequency bursts of spikes in one afferent can reduce the postsynaptic effect of another afferent. The amplitude of the EPSPs and the gain of the synaptic connections differ markedly between the hairs that comprise the receptive field of an interneuron. There are gradients of effectiveness, generally according to the axes of the leg, with one group of adjacent hairs producing the largest-amplitude EPSPs and having the highest gains. Individual hairs may contribute to the receptive field of more than one interneuron, and the gain of these connections may differ. The complexity of a receptive field is further accentuated by the specificity of connections made by the different physiological types of hair receptors. High-threshold hairs may make synaptic connections with an interneuron, but adjacent low-threshold hairs may not. This organization of the receptive fields means that the interneurons are sensitive to certain inputs and can reliably pass on a signal from one hair. It also implies that greater weighting is given to inputs from certain regions.

Animals↗

PubMed1999

Processing of proprioceptive signals by ascending interneurones in the terminal abdominal ganglion of the crayfish.

Intersegmental interneurones are crucial for the appropriate coordination of the activity of local circuits located in different body segments. We have analysed the synaptic inputs to ascending intersegmental interneurones from a proprioceptor in the tailfan of the crayfish. Twenty identified interneurones responded during stimulation of the exopodite-endopodite chordotonal organ. Of these 20 interneurones, three were excited phaso-tonically, nine were excited phasically and eight were inhibited. All received convergent exteroceptive inputs from water-motion- or touch-sensitive hairs on the uropods. The effects of simultaneous exteroceptive and proprioceptive stimulation depended upon the identity of an interneurone. For interneurones that were inhibited by proprioceptive stimulation, suprathreshold exteroceptive responses were reduced to a subthreshold level by simultaneous proprioceptive stimulation. In contrast, for interneurones that were excited by proprioceptive stimulation, the simultaneous application of subthreshold proprioceptive and exteroceptive stimulation elicited action potentials. Two of the interneurones that receive proprioceptive input (NE-1 and RC-8) are known to be presynaptic to giant interneurones that mediate and coordinate the tail-flip. Many of the other interneurones that receive proprioceptive inputs in the tailfan are known to excite abdominal extensor motor neurones. Thus, proprioceptive input to these intersegmental interneurones could serve two roles: first, to extend the abdomen during postural movements or prior to escape and, second, to drive the tail-flip escape response.

Journal Article↗

PubMed1988

Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology.

Stable intracellular recordings were obtained from nonpyramidal cells (interneurons) in stratum lacunosum-moleculare (L-M) of the CA1 region of guinea pig hippocampal slices. The intracellular response characteristics of these interneurons were distinctly different from responses of pyramidal cells and of other interneurons (basket cells and oriens-alveus interneurons). L-M interneurons had a high resting membrane potential (-58 mV), a high input resistance (64 M omega), and a large amplitude (60 mV), relatively long duration (2 msec) action potential. A large afterhyperpolarization (11 mV, 34 msec) followed a single action potential. Most L-M interneurons did not display any spontaneous firing. Lucifer yellow (LY)-filled L-M interneurons showed nonpyramidal morphology. Cells were generally fusiform or multipolar, with aspinous, beaded dendritic processes ramifying in stratum lacunosum-moleculare, radiatum, and (sometimes) oriens. The varicose axon originated from a primary dendrite, projected along stratum lacunosum-moleculare, branched profusely in stratum radiatum, and coursed toward and into stratum pyramidale and occasionally into oriens. Processes of cells with somata in the L-M region of CA1 were not restricted to the CA1 region. The dendritic and axonal processes of some L-M interneurons were seen ascending in stratum lacunosum-moleculare, crossing the hippocampal fissure, and coursing in stratum moleculare of the dentate gyrus. Excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) were evoked in L-M interneurons from stimulation of major hippocampal afferents. EPSPs were most effectively elicited by stimulation of fiber pathways in transverse slices, whereas IPSPs were predominantly evoked when major pathways were stimulated in longitudinal slices. We have identified a population of interneurons with intracellular response characteristics and morphology distinctly different from previously described pyramidal and nonpyramidal neurons of CA1 region. The possible role of these interneurons in hippocampal circuitry is discussed.

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PubMed1997

Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. Local multiglomerular interneurons.

Synapses between three types of antennal lobe neurons, namely, local multiglomerular interneurons, antennal receptor neurons, and gamma-aminobutyric acid (GABA)-immunoreactive neurons, were studied by means of a combination of three different markers. The interneurons were labeled by intracellular injection of horseradish peroxidase (HRP) into a single soma or a small group of neurons. Antennal receptor cells were marked by experimentally induced anterograde degeneration, and GABA-containing neurons were identified by postembedding immunogold staining. The following types of connections were found: Local interneurons receive input synapses from 1) degenerated receptor neuron axons, 2) GABA-immunogold-labeled neurites, and 3) non-GABA-immunoreactive neurons. The interneurons form output synapses onto the same three neuron groups. Contacts were also found between HRP-labeled interneurons themselves. The majority of synapses were dyadic. In most cases, only one postsynaptic neuronal process of the dyads was labeled and, thus, was identified. Polysynaptic connections were found between GABA-immunoreactive neurites, HRP-labeled interneuron processes, and nonlabeled neurites or between HRP-labeled interneuron processes and two interconnected GABA-immunoreactive processes. The present findings provide anatomical evidence for an earlier suggested monosynaptic connection between afferent receptor fibers and local, at that time putative, GABAergic interneurons. They further reveal that local multiglomerular interneurons are synaptically interconnected. The interneurons, in addition, form serial connections via more than one GABA-immunoreactive neuron with non-GABA-immunoreactive and putative projection neurons. Such polysynaptic connections would be a substrate for a feed-forward "disinhibition" of projection neurons, which has been suggested on the basis of electrophysiological findings.

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