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PubMed2002

Morphological characteristics and central projections of two types of interneurons in the visual pathway of Hermissenda.

The synaptic interactions between photoreceptors in the eye and second-order neurons in the optic ganglion of the nudibranch mollusk Hermissenda are well characterized. However, the higher-order neural circuitry of the visual system, consisting of cerebropleural interneurons that receive synaptic input from photoreceptors and project to pedal motor neurons that mediate visually guided behaviors, is only partially understood. In this report we have examined the central projections of two identified classes of cerebropleural interneurons that receive excitatory or inhibitory synaptic input from identified photoreceptors. The classification of the interneurons was based on both morphological and electrophysiological criteria. Type I interneurons received monosynaptic excitatory or inhibitory synaptic input from identified photoreceptors and projected to postsynaptic targets within the cerebropleural ganglion. Type II interneurons, characterized here for the first time, received polysynaptic excitatory or inhibitory synaptic input from identified photoreceptors and projected to postsynaptic targets in either the ipsilateral pedal ganglion or the contralateral cerebropleural ganglion. Type I interneurons exhibited unique intraganglionic projections to different regions of the cerebropleural ganglion, depending on whether they received excitatory or inhibitory synaptic input from identified photoreceptors. Type I interneurons that received monosynaptic excitatory input from identified B photoreceptors terminated near the cerebropleural commissure and had multiple regions of varicosities located at branches that projected from the primary axon. Type I interneurons that received monosynaptic inhibitory input from identified B photoreceptors projected to the anterior cerebropleural ganglion and exhibited varicosities localized to the terminal region of the primary axonal process. Type II interneurons that received polysynaptic inhibitory input from identified photoreceptors projected to the contralateral cerebropleural ganglion. Most type II interneurons that projected to the pedal ganglia received polysynaptic excitatory input from identified photoreceptors. These results indicate that there is at least one additional interneuron in the higher-order visual circuit between type I interneurons and pedal motor neurons responsible for the generation of phototactic locomotion in Hermissenda.

Action Potentials↗
PubMed1980

Distributed processing by visual interneurons of crayfish brain. I. Response characteristics and synaptic interactions.

1. The visual responses and synaptic interactions of a small population of crayfish interneurons are described. 2. The discharge of optic nerve sustaining fibers (tonic on-cells) appears in the brain prior to the onset of the light-evoked discharge of any of the higher order, descending visual interneurons. Direct depolarization of impaled sustaining fibers elicits impulse responses in a large number of descending interneurons. These results indicate that the sustaining fibers provide the visual input to higher order interneurons. 3. Four classes of descending interneurons can be distinguished. All arise in the brain and have axons in the circumesophageal connectives. The response forms vary from tonic to phasic. Two classes of tonic cells are distinguished by response latency and two classes of phasic neurons are distinguished by the rate of response adaptation. The phasic neurons exhibit the most rapid habituation, the largest receptive fields, and the most potent nonvisual inputs. 4. Synaptic interactions are studied by cross-correlation of impulse trains and direct observation of synaptic potentials. About 84% of the cells examined reveal evidence of functional connections to other descending visual interneurons. 5. Cross-correlograms derived from impulses of parallel interneurons exhibit a mean time lage to peak of 6.6 +/- 2.8 ms (SD). The measured delay from EPSP onset to spike onset is 6.0 +/- 4.0 ms. Thus a substantial proportion of the correlogram's time lag to peak is associated with postsynaptic integration time. 6. Direct depolarization of impaled tonic on-cells elicits impulse activity at a fixed delay in other descending interneurons. 7. Synaptic potentials in descending visual interneurons are correlated 1:1 with axon spikes of other descending interneurons. 8. A third of the 80 interactions examined were reciprocal and many cells were implicated in multiple interactions. 9. The results suggest that the descending visual interneurons are organized in a complex network, which can cordinate the discharge of various subpopulations of the ensemble. It is proposed that the coordination of impulses in parallel interneurons may be a mechanism for coding and information transfer in the crayfish nervous system.

Animals↗
PubMed1996

Unitary excitatory synaptic currents in preganglionic neurons mediated by two distinct groups of interneurons in neonatal rat sacral parasympathetic nucleus.

1. Excitatory postsynaptic currents (EPSCs) in parasympathetic preganglionic neurons (PGNs) were examined by the use of the whole cell patch-clamp recording technique in slice preparations of the neonatal rat lumbosacral spinal cord. Synaptic responses were evoked in PGNs by extracellular stimulation of a neighboring interneuron. 2. Stimulation of interneurons medial to the sacral parasympathetic nucleus (SPN) elicited EPSCs or inhibitory postsynaptic currents in 58 and 11%, respectively, of PGNs. Stimulation of interneurons dorsal to the SPN evoked EPSCs in 70% of PGNs. 3. EPSCs occurred at short latency (2.1 ms) and were usually elicited in an all-or-none manner, indicating that they were monosynaptic and mediated by a single interneuron (i.e., unitary). 4. EPSCs were mediated by both non-N-methyl-D-aspartate (non-NMDA) and NMDA receptors. 5. Unitary excitatory postsynaptic potentials evoked by single stimuli did not induce action potentials in PGNs, but repetitive stimulation (> 20 Hz) of the single interneurons could evoke firing of PGNs. 2-Amino-5-phosphonovalerate, an NMDA receptor antagonist, reduced the synaptic depolarization induced in PGNs by high-frequency interneuronal impulses. 6. EPSCs mediated by dorsal interneurons were smaller in amplitude (36.3 +/- 15.7 pA, mean +/- SD) than EPSCs mediated by medial interneurons (88.4 +/- 45.7 pA). 7. Paired-pulse facilitation of EPSCs was observed in PGNs (147.2 +/- 26.2%). The degree of facilitation was higher in dorsal (174.6 +/- 10.3%) than in medial interneuronal pathways (120.9 +/- 3.6%). Within each of interneuronal pathways the degree of facilitation was independent of the magnitude of the unitary EPSC. 8. The results show that PGNs receive monosynaptic glutamatergic excitatory inputs from two distinct populations of interneurons in the dorsal and medial regions of the SPN. These two populations of interneurons are likely to have different functions in the regulation of the preganglionic outflow to the pelvic organs.

Animals↗
PubMed1997

Two types of identified ascending interneurons with distinct GABA receptors in the crayfish terminal abdominal ganglion.

More than half of the identified ascending interneurons originating in the terminal abdominal ganglion of the crayfish received inhibitory sensory inputs from hair afferents innervating the tailfan on the side contralateral to their main branches. Biochemical aspects of this transverse lateral inhibition of ascending interneurons were examined by the use of neurophysiological and pharmacological techniques. Local application of gamma-aminobutyric acid (GABA) and its agonist muscimol into the neuropil induced membrane hyperpolarization of identified ascending interneurons with an increase in membrane conductance. Because the reversal potential of inhibitory postsynaptic potential (IPSPs) in ascending interneurons elicited by the sensory stimulation and GABA injection was similar, and the sensory-stimulated IPSPs of the interneurons were blocked by GABA and muscimol application, this study strongly suggests a GABAergic nature for transverse lateral inhibition of ascending interneurons. According to the response to the GABAA antagonists bicuculline and picrotoxin, ascending interneurons were classified into two types, picrotoxin-sensitive and picrotoxin-insensitive interneurons. Identified ascending interneurons VE-1 and RO-4 showed a pharmacological profile similar to that of the classical GABAA receptor of the vertebrates. Bath application of both bicuculline and picrotoxin reversibly reduced the amplitudes of IPSPs. The other identified ascending interneurons CA-1, RO-1, and RO-2 were not affected significantly by the bath application of GABAA and GABAB antagonists, although bath application of low-chloride saline reversed the sensory-stimulated IPSPs. IPSPs of the picrotoxin-sensitive interneurons had a rather faster time course and shorter duration in comparison with those of the picrotoxin-insensitive interneurons.

Animals↗
PubMed1999

GABAB-Receptor-mediated currents in interneurons of the dentate-hilus border.

GABA(B)-receptor-mediated inhibition was investigated in anatomically identified inhibitory interneurons located at the border between the dentate gyrus granule cell layer and hilus. Biocytin staining was used to visualize the morphology of recorded cells. A molecular layer stimulus evoked a pharmacologically isolated slow inhibitory postsynaptic current (IPSC), recorded with whole cell patch-clamp techniques, in 55 of 63 interneurons. Application of the GABA(B) receptor antagonists, CGP 35348 (400 microM) or CGP 55845 (1 microM) to a subset of 25 interneurons suppressed the slow IPSC by an amount ranging from 10 to 100%. In 56% of these cells, the slow IPSC was entirely GABA(B)-receptor-mediated. However, in the remaining interneurons, a component of the slow IPSC was resistant to GABA(B) antagonists. Subtraction of this antagonist resistant current from the slow IPSC isolated the GABA(B) component (IPSC(B)). This IPSC(B) had a similar onset and peak latency to that recorded from granule cells but a significantly shorter duration. The GABA(B) agonist, baclofen (10 microM), produced a CGP 55845-sensitive outward current in 19 of 27 interneurons. In the eight cells that lacked a baclofen current, strong or repetitive ML stimulation also failed to evoke an IPSC(B), indicating that these cells lacked functional GABA(B) receptor-activated potassium currents. In cells that expressed a baclofen current, the amplitude of this current was approximately 50% smaller in interneurons with axons that projected into the granule cell dendritic layer (22.2 +/- 5.3 pA; mean +/- SE) than in interneurons with axons that projected into or near the granule cell body layer (46.1 +/- 10.0 pA). Similarly, the IPSC(B) amplitude was smaller in interneurons projecting to dendritic (9.4 +/- 2.7 pA) than perisomatic regions (34.3 +/- 5.1 pA). These findings suggest that GABA(B) inhibition more strongly regulates interneurons with axons that project into perisomatic than dendritic regions. To determine the functional role of GABA(B) inhibition, we examined the effect of IPSP(B) on action potential firing and synaptic excitation of these interneurons. IPSP(B) and IPSP(A) both suppressed depolarization-induced neuronal firing. However, unlike IPSP(A), suppression of firing by IPSP(B) could be easily overcome with strong depolarization. IPSP(B) markedly suppressed N-methyl-D-aspartate but not AMPA EPSPs, suggesting that GABA(B) inhibition may play a role in regulating slow synaptic excitation of these interneurons. Heterogeneous expression of GABA(B) currents in hilar border interneurons therefore may provide a mechanism for the differential regulation of excitation of these cells and thereby exert an important role in shaping neuronal activity in the dentate gyrus.

Animals↗
PubMed2000

Fetal hippocampal grafts containing CA3 cells restore host hippocampal glutamate decarboxylase-positive interneuron numbers in a rat model of temporal lobe epilepsy.

Degeneration of CA3-pyramidal neurons in hippocampus after intracerebroventricular kainic acid (KA) administration, a model of temporal lobe epilepsy, results in hyperexcitability within both dentate gyrus and the CA1 subfield. It also leads to persistent reductions in hippocampal glutamate decarboxylase (GAD) interneuron numbers without diminution in Nissl-stained interneuron numbers, indicating loss of GAD expression in a majority of interneurons. We hypothesize that enduring loss of GAD expression in hippocampal interneurons after intracerebroventricular KA is attributable to degeneration of their CA3 afferent input; therefore, fetal CA3 grafts can restore GAD interneuron numbers through graft axon reinnervation of the host. We analyzed GAD interneuron density in the adult rat hippocampus at 6 months after KA administration after grafting of fetal mixed hippocampal, CA3 or CA1 cells into the CA3 region at 45 d after lesion, in comparison with "lesion-only" and intact hippocampus. In dentate and CA1 regions of the lesioned hippocampus receiving grafts of either mixed hippocampal or CA3 cells, GAD interneuron density was both significantly greater than lesion-only hippocampus and comparable with the intact hippocampus. In the CA3 region, GAD interneuron density was significantly greater than lesion-only hippocampus but less than the intact hippocampus. Collectively, the overall GAD interneuron density in the lesioned hippocampus receiving either mixed hippocampal or CA3 grafts was restored to that in the intact hippocampus. In contrast, GADinterneuron density in the lesioned hippocampus receiving CA1 grafts remained comparable with lesion-only hippocampus. Thus, grafts containing CA3 cells restore CA3 lesion-induced depletions in hippocampal GAD interneurons, likely by reinnervation of GAD-deficient interneurons. This specific graft-mediated effect is beneficial because reactivation of interneurons could ameliorate both loss of functional inhibition and hyperexcitability in CA3-lesioned hippocampus.

Animals↗
PubMed1994

Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission.

Based on responses to metabotropic glutamate receptor (mGluR) activation, we have characterized two distinct classes of interneuron in stratum (st.) oriens of the CA1 region of hippocampus. One type of interneuron was strongly excited by 1S,3R-aminocyclopentane dicarboxylic acid (ACPD), responding with a large inward current accompanied by increased baseline noise and prominent current oscillations. A second interneuron population responded with a modest inward current with no changes in baseline noise. These two classes of responses persisted in the presence of tetrodotoxin and antagonists of ionotropic glutamate and GABA receptors, suggesting that the inward currents result from mGluRs on the interneurons themselves. The two physiologically defined cell types correspond to two distinct morphological cell types in st. oriens/alveus, distinguished by very different patterns of local axonal connections. Large oscillatory inward current responses were recorded predominantly from an interneuron type whose axons heavily innervated st. lacunosum. The more modest inward current response was generally found in interneurons whose axons innervated the somata and proximal dendrites of CA1 pyramidal neurons. These differences in physiology and local circuitry imply that activation of mGluRs in st. oriens will cause very strong excitation of interneurons synapsing in st. lacunosum, and weaker excitation of interneurons innervating pyramidal cells at the soma and proximal dendrites. These data suggest that each interneuron population has a specific role in hippocampal function, and that mGluR activation will affect the local circuit differently for each interneuron type. Metabotropic GluR activation also markedly enhanced the amplitudes of the evoked and spontaneous EPSCs received by all interneurons in the region, independent of changes in the postsynaptic holding current and with no change in the kinetics of the EPSC. In contrast to the enhancement of evoked and spontaneous EPSCs, miniature EPSCs recorded in the presence of tetrodotoxin were not increased. These data suggest that ACPD acts at a presynaptic site to potentiate the EPSC. Taken together, these results highlight an important modulatory role for metabotropic receptors located at sites both pre- and postsynaptic to CA1 st. oriens interneurons.

Animals↗
PubMed1998

Hippocampal interneurons expressing glutamic acid decarboxylase and calcium-binding proteins decrease with aging in Fischer 344 rats.

Aging leads to alterations in the function and plasticity of hippocampal circuitry in addition to behavioral changes. To identify critical alterations in the substrate for inhibitory circuitry as a function of aging, we evaluated the numbers of hippocampal interneurons that were positive for glutamic acid decarboxylase and those that expressed calcium-binding proteins (parvalbumin, calbindin, and calretinin) in young adult (4-5 months old) and aged (23-25 months old) male Fischer 344 rats. Both the overall interneuron population and specific subpopulations of interneurons demonstrated a commensurate decline in numbers throughout the hippocampus with aging. Interneurons positive for glutamic acid decarboxylase were significantly depleted in the stratum radiatum of CA1, the strata oriens, radiatum and pyramidale of CA3, the dentate molecular layer, and the dentate hilus. Parvalbumin interneurons showed significant reductions in the strata oriens and pyramidale of CA1, the stratum pyramidale of CA3, and the dentate hilus. The reductions in calbindin interneurons were more pronounced than other calcium-binding protein-positive interneurons and were highly significant in the strata oriens and radiatum of both CA1 and CA3 subfields and in the dentate hilus. Calretinin interneurons were decreased significantly in the strata oriens and radiatum of CA3, in the dentate granule cell and molecular layers, and in the dentate hilus. However, the relative ratio of parvalbumin-, calbindin-, and calretinin-positive interneurons compared with glutamic acid decarboxylase-positive interneurons remained constant with aging, suggesting actual loss of interneurons expressing calcium-binding proteins with age. This loss contrasts with the reported preservation of pyramidal neurons with aging in the hippocampus. Functional decreases in inhibitory drive throughout the hippocampus may occur due to this loss, particularly alterations in the processing of feed-forward information through the hippocampus. In addition, such a profound alteration in interneuron number will likely alter inhibitory control of excitability and neuronal synchrony with behavioral states.

Aging↗
PubMed1979

The morphology of local non-spiking interneurones in the metathoracic ganglion of the locust.

The morphology is described of a number of non-spiking interneurones in the metathoracic ganglion of the locust that control motor neurones innervating muscles in the coxa and femur of a hind leg. The non-spiking interneurones are penetrated with microelectrodes, physiologically characterized, injected with cobalt, and the stain subsequently intensified with silver. The interneurones have diverse shapes but all are local, intraganglionic interneurones. Their cell bodies are 10-20 micrometer in diameter and lie in either the ventral or dorsal layers of cell bodies that form a cortex around the ganglion. The branches of the interneurones are profuse and overlap those of the motor neurones that they affect. On interneurone may have branches in both the most ventral and the most dorsal areas of the neuropile. Most interneurones have branches only in one half of the ganglion, but one interneurone has extensive and asymmetrical regions of branches in both halves of the ganglion (fig. 4). Similar physiological effects can be mediated by interneurones with distinct morphologies. For example, the single slow extensor motor neurone is excited by six distinct morphological types of interneurones (figs. 10-13). It is suggested that as many as 65% of the neurones within a ganglion may be local interneurones, many of which in turn may be non-spiking.

Action Potentials↗
PubMed1987

Opposing parallel connections through crayfish local nonspiking interneurons.

Unilateral local nonspiking interneurons in the terminal (sixth) abdominal ganglion of crayfish (Procambarus clarkii Girard) can be classified into two major groups of PL and AL types by their gross morphology and somatic position. These premotor interneurons are the neural components of uropod motor pattern formation. They receive sensory input from the exopodite of the contralateral side as well as that of the ipsilateral side. Small fluctuations in their membrane potentials cause sustained change in activity of the motoneurons innervating the uropod muscles. PL interneurons, which make noninverting connections to an identified closer, the reductor motoneuron No. 1, mainly receive excitatory input from the afferents of the contralateral exopodite, whereas inverting PL interneurons receive inhibitory input. AL interneurons receive distinctly different input from the afferents. Noninverting AL interneurons mainly receive inhibitory input, whereas inverting AL interneurons receive excitatory input. The rate of discharge of the reductor motoneurons is increased by sensory stimulation. The PL interneurons form either excitatory or disinhibitory pathways, which are relevant in function to the observed increase of the motoneuron. Conversely, the AL interneurons form either inhibitory or disfacilitatory pathways. Thus, the PL and the AL interneurons are fractionated in function and distinguishable in terms of their physiology by their input and output correlations. Functional meaning of the presence of these two types of unilateral local nonspiking interneurons of opposing connections in the uropod motor control system is discussed.

Afferent Pathways↗
PubMed1988

A population of ascending intersegmental interneurones in the locust with mechanosensory inputs from a hind leg.

A population of some 35 intersegmental interneurones with somata in the metathoracic ganglion has been characterized by intracellular recording and staining. These interneurones integrate signals from extero- and proprioceptors on a hind leg. The somata are clustered in an anterior and lateral region of the dorsal cortex, and the axons project to more anterior ganglia in either the ipsilateral or contralateral connectives. Some of these interneurones are excited by afferents from a proprioceptor at the femorotibial joint, the femoral chordotonal organ. An afferent spike evokes a chemically mediated EPSP in an interneurone with a latency and consistency that suggest that the connection is direct. An individual interneurone codes particular features of the movement about the femorotibial joint, responding to flexion, extension, or both directions of movement with either phasic or tonic responses. These interneurones have an extensive field of fine branches ipsilateral to the hind leg from which they receive input. These branches are in lateral and intermediate regions of neuropil to which the afferents of the chordotonal organ also project. Axonal branches, from either an ipsilateral and contralateral axon, are sparse and varicose and occur in dorsal neuropil. Other interneurones are excited by afferents from exteroceptive hairs (trichoid sensilla). An individual interneurone is excited by a particular array of hairs on specific regions of a hind leg. The connections between the afferents and the interneurones appear direct. These interneurones have a dense and compact array of fine branches ipsilateral to the hind leg from which they receive input. These branches are in the most ventral region of neuropil, to which the hair afferents also project. Branches from the ipsilateral axons are sparse and varicose and occur in more dorsal neuropil. The interneurones can thus provide the more anterior ganglia with precise information about the movement of a joint in a hind leg and of the location of an exteroceptive stimulus. This information would be of importance in ensuring the correct co-ordination of the legs during walking.

Animals↗
PubMed2004

Immunolocalization of metabotropic glutamate receptor 1alpha (mGluR1alpha) in distinct classes of interneuron in the CA1 region of the rat hippocampus.

In the hippocampal CA1 region, metabotropic glutamate subtype 1 (mGluR1) receptors have been implicated in a variety of physiological responses to glutamate, which include modulation of synaptic transmission and plasticity, as well as neuronal excitability and synchronization. The mGluR1alpha isoform is characteristically expressed only by nonprincipal cells, and it is particularly enriched in somatostatin (SS)-containing interneurons in stratum oriensalveus. Anatomical and physiological data have indicated the presence of mGluR1alpha in several distinct classes of interneurons with their somata located also in strata pyramidale, radiatum, and lacunosum moleculare. Each different interneuron subtype, as defined by functionally relevant criteria, including input/ output characteristics and expression of selective molecular markers, subserves distinct functions in local hippocampal circuits. We have investigated which of the different CA1 interneuron classes express mGluR1alpha by immunofluorescent labeling, combining antibodies to mGluR1alpha, calcium-binding proteins, and neuropeptides, and by intracellular labeling in vitro. Several types of interneuron that are immunopositive for mGluR1alpha each targeted different domains of pyramidal cells and included (1) O-LM inter-neurons, found to coexpress both SS and parvalbumin (PV); (2) interneurons with target selectivity for other interneurons, expressing vasoactive intestinal polypeptide (VIP) and/or the calcium-binding protein calretinin; (3) procholecystokinin-immunopositive interneurons probably non-basket and dendrite-targeting; and (4) an as-yet unidentified SS-immunoreactive but PV-immunonegative interneuron class, possibly corresponding to oriens-bistratified cells. Estimation of the relative proportion of mGluR1alpha-positive interneurons showed 43%, 46%, and 30% co-labeling with SS, VIP, or PV, respectively. The identification of the specific subclasses of CA1 interneurons expressing mGluR1alpha provides the network basis for assessing the contribution of this receptor to the excitability of the hippocampus.

Animals↗
PubMed1996

The possible role of C5 segment inspiratory interneurons investigated by cross-correlation with phrenic motoneurons in decerebrate cats.

We tested the role of C5 segment inspiratory interneurons in transcribing central respiratory drive to phrenic motoneurons and mediating intersegmental reflexes by cross-correlating the spontaneous activity of 26 interneurons with that of the ipsi -and contralateral C5 phrenic nerves in decerebrate cats. There were 10 interneurons that discharged only during inspiration (phrenic burst) and 16 that discharged tonically with increased firing during inspiration. Of the cross-correlograms for 26 of the interneurons with the ipsilateral phrenic, 20 were flat and 2 had peaks centred about time zero, interpreted as a common activation of the interneurons and motoneurons. The cross-correlograms for 4 other interneurons had troughs centred about time zero, interpreted as a synchronous excitation of the interneurons and inhibition of the motoneurons. Of the cross-correlograms for 23 interneurons with the contralateral phrenic, 22 were flat and 1 had a peak centred about time zero, interpreted as a common activation of the interneuron and motoneurons. Nine of ten cross-correlograms between pairs of interneurons were flat; one had a peak centred about time zero. We conclude that, despite their inspiratory modulated discharge patterns, there is no evidence from this study that the C5 segment inspiratory interneurons convey central respiratory drive to C5 phrenic motoneurons.

Animals↗
PubMed1991

A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus.

The relative proportions of synapses made by retinal and extraretinal terminals on interneurons and relay cells in lamina A of the dorsal lateral geniculate nucleus (LGN) of the cat were estimated quantitatively in a sample of 4003 synapses. Processes of interneurons or relay cells were identified by presence or absence of GABA immunoreactivity, respectively, in thin sections treated with post-embedding anti-GABA immunogold. On the basis of ultrastructural features, synaptic terminals were interpreted as belonging to retinal axons, cortical axons or axon collaterals of relay cells. GABAergic terminals were positively identified by being immunoreactive. GABA(-) terminals with heterogeneous and poorly defined characteristics, which could not be identified in the above classes, were grouped together in an "undetermined" category. Among the total synaptic inputs to interneurons, the following relative percentages of synapses from different terminals were obtained: retinal 25%, cortical 37%, GABAergic 26%, axon collaterals 2%, undetermined 6%. The vast majority of retinal terminals synapse on dendritic appendages of interneurons rather than on their dendritic trunks (about 20:1). By contrast, the majority of cortical terminals synapse on dendrites rather than on dendritic appendages (about 5:1). Virtually all axon-collaterals synapses were established on dendritic appendages. 17% of the dendritic profiles of interneurons contain synaptic vesicles; many of these profiles were seen in postsynaptic relation to cortical axons and in presynaptic relation with relay dendrites. Given the extensive electrotonic lengths of these cells observed by others, and the expected high electric resistance of the slender stalks that are known to connect the dendritic appendages to interneurons, these results suggest that microcircuits involving the interneuronal dendritic appendages with dendrites of relay cells are under predominantly retinal control. The microcircuits established by presynaptic dendritic trunks with relay dendrites, are under predominantly cortical control. The axonal (spiking) output of interneurons would be under control of the few retinal synapses on proximal dendrites of these cells. Among the total synaptic inputs to relay cells, the following relative percentages of different synapses were obtained: retinal 12%, cortical 58%, GABAergic 24%, axon collaterals 0.3%, undetermined 5%. Relay cells receive twice the number of cortical synapses than interneurons, suggesting that direct cortical excitatory influences on relay cells are more preponderant than cortico-interneuron mediated inhibition on these cells. The observed proportions of dendritic profiles of relay cells and interneurons (80% and 20%, respectively) in the geniculate neuropil are similar to the known proportions of somata of both types of cells in the A-laminae.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed2003

Different patterns of synaptic transmission revealed between hippocampal CA3 stratum oriens and stratum lucidum interneurons and their pyramidal cell targets.

Stratum lucidum (SL) interneurons likely mediate feedforward inhibition between the dentate gyrus mossy fibers and CA3 pyramidal cells, while stratum oriens (SO) interneurons likely provide both feedforward and feedback inhibition within the CA3 commissural/associational network. Using dual whole-cell patch-clamp recordings between interneurons and CA3 pyramidal cells, we have examined SL and SO interneurons and their synapses within organotypic hippocampal slice cultures. Biocytin staining revealed different morphologies between these interneuron groups, both being very similar to those found previously in acute slices. The kinetics of IPSCs were similar between the two groups, but the reliability of synaptic transmission of SL interneuron (SL-INT) IPSCs was significantly lower than the virtually 100% reliability (non-existent failure rates) of SO-INT IPSCs. The SL-INT IPSCs also had a lower quantal content than the SO-INT IPSCs. In addition, SL-INTs were less likely than SO-INTs to innervate or to be innervated by nearby CA3 pyramidal cells. Paired-pulse stimulation at 100 ms interstimulus intervals produced similar paired-pulse depression in both interneuron synapses, despite the significantly higher failure rate of IPSCs produced by the SL-INTs compared with SO-INTs. CV analysis supported the hypothesis that paired-pulse depression was presynaptic. During repetitive, high frequency stimulation (>10 Hz for 500 ms) the two different synapses exhibited distinctly different forms of short-term plasticity: all SL interneurons displayed significant short-term facilitation (mean 113% facilitation, n=4), while, by contrast, SO interneuron synapses displayed either short-term depression (mean 42% depression, n=5 of 8) or no net facilitation or depression (n=3 of 8). These results indicate that the synaptic properties of interneurons can be quite different for interneurons in different hippocampal circuits.

Action Potentials↗
PubMed2003

Large variability in synaptic N-methyl-D-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus.

Pyramidal cells receive input from several types of GABA-releasing interneurons and innervate them reciprocally. Glutamatergic activation of interneurons involves both alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and N-methyl-D-aspartate (NMDA) type glutamate receptors expressed in type I synapses, mostly on their dendritic shafts. On average, the synaptic AMPA receptor content is several times higher on interneurons than in the spines of pyramidal cells. To compare the NMDA receptor content of synapses, we used a quantitative postembedding immunogold technique on serial electron microscopic sections, and analysed the synapses on interneuron dendrites and pyramidal cell spines in the CA1 area. Because all NMDA receptors contain the obligatory NR1 subunit, receptor localisation was carried out using antibodies recognising all splice variants of the NR1 subunit. Four populations of synapse were examined: i). on spines of pyramidal cells in stratum (str.) radiatum and str. oriens; ii). on parvalbumin-positive interneuronal dendritic shafts in str. radiatum; iii). on randomly found dendritic shafts in str. oriens and iv). on somatostatin-positive interneuronal dendritic shafts and somata in str. oriens. On average, the size of the synapses on spines was about half of those on interneurons. The four populations of synapse significantly differed in labelling for the NR1 subunit. The median density of NR1 subunit labelling was highest on pyramidal cell spines. It was lowest in the synapses on parvalbumin-positive dendrites in str. radiatum, where more than half of these synapses were immunonegative. In str. oriens, synapses on interneurons had a high variability of receptor content; some dendrites were similar to those in str. radiatum, including the proximal synapses of somatostatin-positive cells, whereas others had immunoreactivity for the NR1 subunit similar to or higher than synapses on pyramidal cell spines. These results show that synaptic NMDA receptor density differs between pyramidal cells and interneurons. Some interneurons may have a high NMDA receptor content, whereas others, like some parvalbumin-expressing cells, a particularly low synaptic NMDA receptor content. Consequently, fast glutamatergic activation of interneurons is expected to show cell type-specific time course and state-dependent dynamics.

Animals↗
PubMed1999

Patterns of spontaneous activity and morphology of interneuron types in organotypic cortex and thalamus-cortex cultures.

The physiological and morphological properties of interneurons in infragranular layers of rat visual cortex have been studied in organotypic cortex monocultures and thalamus-cortex co-cultures using intracellular recordings and biocytin injections. Cultures were prepared at the day of birth and maintained for up to 20 weeks. Twenty-nine interneurons of different types were characterized, in addition to 170 pyramidal neurons. The cultures developed a considerable degree of synaptically driven "spontaneous" bioelectric activity without epileptiform activity. Interneurons in cortex monocultures and thalamus-cortex co-cultures had the same physiological and morphological properties, and also pyramidal cell properties were not different in the two culture conditions. All interneurons and the majority of pyramidal cells displayed synaptically driven action potentials. The physiological group of fast-spiking interneurons included large basket cells, columnar basket cells (two cells with an arcade axon) and horizontally bitufted cells. The physiological group of slow-spiking interneurons included Martinotti cells and a "long-axon" cell. Analyses of the temporal patterns of activity revealed that fast-spiking interneurons have higher rates of spontaneous activity than slow-spiking interneurons and pyramidal cells. Furthermore, fast-spiking interneurons fired spontaneous bursts of action potentials in the gamma frequency range. We conclude from these findings that physiological and morphological properties of interneurons in organotypic mono- and co-cultures match those of interneurons characterized in vivo or in acute slice preparations, and they maintain in long-term cultures a well-balanced state of excitation and inhibition. This suggests that cortex-intrinsic or cell-autonomous mechanisms are sufficient for the expression of cell type-specific electrophysiological properties in the absence of afferents or sensory input.

Animals↗
PubMed1999

Alterations of perisomatic GABA synapses on hippocampal CA1 inhibitory interneurons and pyramidal cells in the kainate model of epilepsy.

In the kainate model of epilepsy, electrophysiological and anatomical modifications occur in inhibitory circuits of the CA1 region of the rat hippocampus. Using postembedding GABA immunocytochemistry and electron microscopy, we characterized perisomatic GABA and non-GABA synaptic contacts in CA pyramidal cells, and GABAergic interneurons of stratum oriens/alveus and stratum lacunosum-moleculare, and examined if changes occurred at these synapses at two weeks post-kainate treatment. We found that, in control rats, the number and total length of perisomatic GABA synapses were significantly smaller (approximately 40-50%) in lacunosum-moleculare interneurons than in oriens/alveus interneurons and pyramidal cells. Additionally, the number and total length of perisomatic non-GABA synapses were different among all cell types, with these parameters increasing significantly in the following order: pyramidal cells<lacunosum-moleculare interneurons<oriens/alveus interneurons. Following kainate treatment, we found that the number and total length of GABA synapses were significantly increased in lacunosum-moleculare interneurons (by 76% and 100%, respectively), but were unchanged in pyramidal cells and oriens/alveus interneurons. In addition, the mean length of individual GABA synapses was significantly increased (by 17%) in pyramidal cells after kainate treatment. In contrast, no changes were observed at non-GABA synapses in any cell type examined after kainate treatment. These results indicate that, in control animals, the ultrastructural correlates of perisomatic GABA inhibition are less pronounced in lacunosum-moleculare than oriens/alveus interneurons or pyramidal cells, whereas those of perisomatic excitation are more prominent in oriens/alveus than lacunosum-moleculare interneurons, and much less present in pyramidal cells. In addition, our results with kainate-treated animals suggest that cell-specific changes in perisomatic inhibition may occur in CA1 inhibitory interneurons in the chronically hyperexcitable hippocampus. The ultrastructural correlates of perisomatic inhibition were increased in lacunosum-moleculare interneurons, which may thus suggest some disinhibition of pyramidal cells. However, the ultrastructural correlates of perisomatic inhibition were increased in pyramidal cells, implying some enhancement of perisomatic inhibition of principal cells in the hyperexcitable hippocampus.

Animals↗