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PubMed1994

The activity of interneurons during locomotion in the in vitro necturus spinal cord.

1. Less than two segments of the cervical spinal cord of the mudpuppy (Necturus maculatus) is sufficient to generate a locomotor rhythm with application of N-methyl-D-aspartic acid (NMDA). We have recorded intracellularly from rhythmically active interneurons in these segments and classified them according to their phase of firing within the step cycle and their afferent input. 2. Four classes of interneurons were found: flexor, flexor-->extensor, extensor, and extensor-->flexor. Interneurons that burst during the transition from flexion to extension or vice versa are referred to as "transitional" interneurons and represent the majority (68%) of rhythmically active interneurons studied in the mudpuppy spinal cord. 3. All flexor interneurons received only inhibitory input from cutaneous and dorsal root afferents, whereas the flexor-->extensor interneurons that responded received only excitatory input from dorsal root and cutaneous afferents. All extensor interneurons and all but one extensor-->flexor interneuron received no afferent input from the cutaneous or dorsal root afferents we stimulated. 4. Other interneurons have been classified as "tonic" cells. They fire continuously when the mudpuppy is walking and are silent when the mudpuppy is not walking. These interneurons receive no afferent input from the sources tested and may be responsible for turning locomotion on and off. 5. In conclusion, the presence of many transitional interneurons with specific patterns of afferent input may be required for the phasing of legged locomotion. We believe the in vitro preparation of the mudpuppy spinal cord and forelimb is an excellent model for studying the firing properties of interneurons during legged locomotion.

Afferent Pathways↗
PubMed1994

Descending control of nonspiking local interneurons in the terminal abdominal ganglion of the crayfish.

1. Electrical stimulation of afferents innervating an exopodite causes a closing pattern of activity in the uropod motor neurons. In this reflex two distinct types of nonspiking local interneurons, posterolateral (PL) and anterolateral (AL) types, classified by their gross morphology and somata location, receive sensory inputs and control the motor output to the uropod. 2. In the sensory-motor pathway, the PL and AL nonspiking local interneurons formed opposing and parallel connections with uropod motor neurons. For example, the PL interneurons that excited the closer, reductor motor neuron by injecting depolarizing current received depolarizing postsynaptic potentials (PSPs), whereas the AL interneurons of the same output received hyperpolarizing PSPs. The PL interneurons that inhibited the reductor motor neuron received hyperpolarizing PSPs, whereas the AL interneurons of the similar output received depolarizing PSPs. 3. During fictive abdominal extension, induced by electrical stimulation of extension-evoking command fibers in the second-third abdominal connective, the uropod motor neurons show an opening pattern of activity that is opposite to the pattern elicited by sensory stimulation. Furthermore, sensory stimulation during ongoing fictive abdominal extension has little effect on the uropod motor neurons. 4. Except for the nonspiking local interneurons, the majority of other local circuit neurons, i.e., spiking local interneurons and ascending interneurons, are not driven by the descending inputs during abdominal extension. 5. A comparison of the responses of the nonspiking local interneurons to both sensory and descending inputs reveals that the majority of nonspiking local interneurons receive both inputs, but the sign of response to each is frequently opposite. This study suggests that the degree of excitability of two distinct types of PL and AL nonspiking local interneurons induced by sensory inputs changes depending on whether the crayfish is in a resting posture or is active with full extension of the abdomen. Ongoing abdominal extension in swimming or defensive crayfish would shift the gain of reflex pathways through the PL and AL interneurons, and motor response resulting from sensory inputs would be modulated.

Abdomen↗
PubMed1996

Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices.

1. Intrinsic membrane properties and pharmacologically isolated excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs, respectively) were characterized with the use of whole cell current- and voltage-clamp recordings, in combination with biocytin labeling, in different subtypes of CA1 interneurons and pyramidal cells in rat hippocampal slices. 2. Three classes of interneurons were selected on the basis of their soma location in the CA1 region: 1) in stratum (str.) oriens near the alveus (O/A), 2) near str. pyramidale, and 3) near the border of str. radiatum and lacunosum-moleculare. Each class of biocytin-labeled cells demonstrated specific cellular morphology. The somata of all interneurons were nonpyramidal in shape and usually multipolar. However, the pattern of dendritic and axonal arborizations of labeled interneurons differed in each class. 3. In current-clamp recordings, all interneuron subtypes had shorter-duration and smaller-amplitude action potentials than pyramidal cells. Fast- and medium-duration afterhyperpolarizations were larger in amplitude in interneurons. Cell input resistance was greater and membrane time constant was faster in all interneuron subtypes than in pyramidal cells. 4. Depolarizing current pulses evoked regular firing in all classes of interneurons, whereas burst firing was observed in 50% of pyramidal cells. With hyperpolarizing current pulses, all nonpyramidal and pyramidal cell types displayed inward rectification followed by anodal break excitation. 5. Electrical stimulation of nearby afferents evoked excitatory postsynaptic potentials (EPSPs) in all cells. EPSPs were of short duration and usually followed by inhibitory postsynaptic potentials (IPSPs). EPSPs were mediated by glutamate, because they were blocked by non-N-methyl-D-aspartate (non-NMDA) and NMDA antagonists [6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and (+/-)-2-amino-5-phosphonopentanoic acid (AP5), respectively]. In the presence of these antagonists, IPSPs were evoked in isolation and reversed near -72 mV. 6. In voltage-clamp recordings, non-NMDA EPSCs were isolated pharmacologically in the presence of AP5 and the gamma-aminobutyric acid-A (GABAA) antagonist bicuculline (BIC). Their properties were similar in all interneuron subtypes and pyramidal cells. Current-voltage (I-V) relations were linear, and mean reversal potentials were near 5 mV. Non-NMDA EPSCs were reversibly antagonized by CNQX. 7. NMDA EPSCs were pharmacologically isolated during CNQX and BIC application and were observed in all cell types. I-V relations of NMDA EPSCs demonstrated a region of negative slope at membrane potentials between -80 and -20 mV and their reversal potential was near 7 mV. The rise time of NMDA EPSCs was significantly slower in O/A interneurons than in other cell types. NMDA EPSCs were reversibly antagonized by AP5. 8. GABAA IPSCs were pharmacologically isolated in AP5 and CNQX and their properties were similar in all cell types. I-V relations of GABAA IPSCs were linear with mean reversal potentials near -32 mV. GABAA IPSCs were reversibly blocked by BIC. 9. In conclusion, morphologically different subtypes of interneurons located in O/A, near str. pyramidale, and near the str. radiatum/lacunosum-moleculare border displayed intrinsic membrane properties that were distinct from pyramidal cells, but were similar among them. In contrast, the properties of non-NMDA, NMDA, and GABAA postsynaptic currents were similar between interneurons and pyramidal cells, except for NMDA EPSCs, which had slower rise times in O/A interneurons.

Animals↗
PubMed2000

Monosynaptic connections between identified A and B photoreceptors and interneurons in Hermissenda: evidence for labeled-lines.

The cellular and synaptic organization of the eye of the nudibranch mollusk Hermissenda is well-documented. The five photoreceptors within each eye are mutally inhibitory and can be classified into two types: A and B based on electrophysiological and anatomical criteria. Two of the three type B and two type A photoreceptors can be further identified according to their medial or lateral positions within each eye. In addition to reciprocal synaptic connections between photoreceptors, photoreceptors also project to second-order neurons in the cerebropleural ganglion. The second-order neurons receive convergent synaptic input from two additional sensory pathways; however, it has not been previously established if lateral A, lateral B, or medial B photoreceptors converge onto the same second-order neurons. To determine the specific synaptic organization of these components of the visual system, we have examined monosynaptic connections between identified lateral and medial type A and B photoreceptors and second-order cerebropleural (CP) interneurons. We found that monosynaptic connections between identified lateral A and lateral and medial B photoreceptors and CP interneurons follow a labeled-line principle. Illumination of the eyes or extrinsic depolarizing current applied to identified photoreceptors evoked excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs, respectively) in different CP interneurons. The PSPs in CP interneurons followed one-for-one spikes in the photoreceptors and could be elicited in artificial seawater solutions containing high divalent cations. Identified photoreceptors projected to more than one CP interneuron and expressed both excitatory and inhibitory connections with the different CP interneurons. In examples where a monosynaptic connection between a lateral B photoreceptor and a CP interneuron was identified, lateral A, medial A, or medial B photoreceptors did not project to the same CP interneuron. Moreover, when connections between medial B and CP interneurons were identified, lateral A, medial A, and lateral B connections were not found to project to the same CP interneuron. Similar results were obtained for a lateral A and CP interneuron connection. These results indicate that divergent labeled-lines exist between specific photoreceptors and second-order CP interneurons and potential convergence of synaptic input from primary and secondary elements of the visual system must occur at sites that are postsynaptic to the CP interneurons.

Action Potentials↗
PubMed2003

Sonic hedgehog and bone morphogenetic protein regulate interneuron development from dorsal telencephalic progenitors in vitro.

Cortical progenitors are competent to produce interneurons, but do not generate large numbers of interneurons in vivo under normal circumstances. This could reflect the absence of an inductive signal in the environment of the dorsal telencephalon and/or the presence of an inhibitory signal. To determine whether either or both mechanisms regulate interneuron generation, progenitors in dorsomedial and dorsolateral wall explants of mouse telencephalon were marked with a retrovirus and cultured under several conditions. When cultured separately, progenitors in dorsomedial wall explants produced fewer GABAergic interneurons than progenitors in dorsolateral wall explants. When cocultured with ventral telencephalic cells, however, dorsomedial wall progenitors produced more GABAergic interneurons than in dorsomedial wall explants alone. The inductive effect of ventral telencephalon depended on sonic hedgehog (Shh) and could be mimicked by exogenous Shh. In contrast, exogenous bone morphogenetic protein 4 (BMP4) reduced the production of interneurons in dorsolateral wall explants and inhibited the induction by exogenous Shh. Moreover, inhibiting BMP signaling in dorsomedial wall progenitors with a dominant-negative BMP receptor Ib (dnBMPIb) virus increased their production of interneurons, even if Shh was blocked. Shh and dnBMPRIb increased proliferation and the generation of interneurons, but FGF2 did not induce interneurons, although it increased proliferation. This suggests that proliferation per se does not control the production of interneurons. Our findings suggest that the generation of interneurons by dorsal telencephalic progenitors is normally limited by excess levels of BMPs. Shh may promote the generation of interneurons by antagonizing BMP, but may not be required directly for the generation of interneurons.

Animals↗
PubMed1989

Distribution of intersegmental inputs to nonspiking local interneurons and motor neurons in the locust.

Intersegmental interneurons in a mesothoracic population that receive inputs from extero- and proprioceptors on a middle leg of a locust (Laurent, 1987a) make direct synaptic connections with nonspiking local interneurons and motor neurons controlling the movements of the ipsilateral hindleg. Of 25 direct connections that were established, 80% are excitatory, and 60% are made with nonspiking interneurons. Two or more intersegmental interneurons with outputs of either polarity and with different or overlapping receptive fields can converge onto one metathoracic nonspiking interneuron. Direct connections were found with motor neurons of the coxotrochanteral, femorotibial, and tibiotarsal joints of the hindleg. An intersegmental interneuron can make divergent connections with several motor neurons of the same pool or with a motor neuron and a nonspiking interneuron presynaptic to it. By virtue of the lateral inhibitory connections between nonspiking interneurons controlling different pools of motor neurons (Burrows, 1979), an intersegmental interneuron can excite directly one pool and disynaptically inhibit the antagonistic pool. Metathoracic nonspiking interneurons also receive inputs from afferents of mechanoreceptors on a hindleg. They thus have 2 receptive fields: one on the hindleg whose motor neurons they control and one on the ipsilateral middle leg, provided by inputs from the mesothoracic intersegmental interneurons. Nonspiking local interneurons are thus a point of convergence of local and intersegmental pathways. The effectiveness of the intersegmental pathways can thus be modified by local inputs to the nonspiking interneurons.

Animals↗
PubMed2001

Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles.

Neurobiotin was injected into individual spinal interneurons in the Xenopus tadpole to discern their anatomical features and complete axonal projection patterns. Four classes of interneuron are described, with names defining their primary axon projection: Dorsolateral ascending and commissural interneurons are predominantly multipolar cells with somata and dendrites exclusively in the dorsal half of the spinal cord. Ascending interneurons have unipolar somata located in the dorsal half, but their main dendrites are located in the ventral half of the spinal cord. Descending interneurons show bigger variance in their anatomy, but the majority are unipolar, and they all have a descending primary axon. Dorsolateral commissural interneurons are clearly defined using established criteria, but the others are not, so cluster analysis was used. Clear discriminations can be made, and criteria are established to characterize the three classes of interneuron with ipsilateral axonal projections. With identifying criteria established, the distribution and axonal projection patterns of the four classes of interneuron are described. By using data from gamma-aminobutyric acid immunocytochemistry, the distribution of the population of ascending interneurons is defined. Together with the results from the axonal projection data, this allows the ascending interneuron axon distribution along the spinal cord to be estimated. By making simple assumptions and using existing information about the soma distributions of the other interneurons, estimates of their axon distributions are made. The possible functional roles of the four interneuron classes are discussed.

Afferent Pathways↗
PubMed2006

Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala.

The basolateral amygdala (BLA) is critical for the generation of emotional behavior and the formation of emotional memory. Understanding the neuronal mechanisms that contribute to emotional information processing in the BLA will ultimately require knowledge of the anatomy and physiology of its constituent neurons. Two major cell classes exist in the BLA, pyramidal projection neurons and nonpyramidal interneurons. Although the properties of projection neurons have been studied in detail, little is known about the properties of BLA interneurons. We have used whole-cell patch clamp recording techniques to examine the physiological properties of 48 visually identified putative interneurons from the rat anterior basolateral amygdalar nucleus. Here, we report that BLA interneurons can be differentiated into four electrophysiologically distinct subtypes based on their intrinsic membrane properties and their response to afferent synaptic input. Interneuron subtypes were named according to their characteristic firing pattern generated in response to transient depolarizing current injection and were grouped as follows: 1) burst-firing interneurons (n = 13), 2) regular-firing interneurons (n = 11), 3) fast-firing interneurons (n = 10), and 4) stutter-firing interneurons (n = 14). Post hoc histochemical visualization confirmed that all 48 recorded neurons had morphological properties consistent with their being local circuit interneurons. Moreover, by using triple immunofluorescence (for biocytin, calcium-binding proteins, and neuropeptides) in conjunction with patch clamp recording, we further demonstrated that over 60% of burst-firing and stutter-firing interneurons also expressed the calcium-binding protein parvalbumin (PV(+)). These data demonstrate that interneurons of the BLA show both physiological and neurochemical diversity. Moreover, we demonstrate that the burst- and stutter-firing patterns positively correlate with PV(+) immunoreactivity, suggesting that these neurons may represent functionally distinct subpopulations.

Action Potentials↗
PubMed1987

The morphology of a population of thoracic intersegmental interneurones in the locust.

A population of intersegmental interneurones with axons extending from the meso- to the metathoracic ganglion of the locust is described. They receive specific mechanosensory inputs from one mesothoracic leg. Their cell bodies are in group at the posterior of the mesothoracic ganglion, lying over the lateral base of each connective, and their primary neurites emerge in one of four bundles. Their mesothoracic branches are ipsilateral to the cell bodies and the leg from which they receive inputs. Each interneurone has two to six mesothoracic secondary neurites that divide and form a dense field of arborizations in specific regions of the neuropil so that each individual interneurone has a characteristic shape that is an elaboration of a basic and common plan. An interneurone excited by tibial campaniform sensilla and tarsal hair afferents branches in the intermediate neuropil and the ventral association center where the afferents from these receptors also project. An interneurone excited by proprioceptive inputs from the tarsus arborizes in the dorsal and intermediate neuropils, lateral to the ventral intermediate and ventral median tracts, in the same area as the proprioceptors afferents. An interneurone inhibited by proprioceptive inputs from the tibia (and wing) arborizes only in the dorsal neuropil, where there are no afferent projections. Some interneurones have one to three axonal branches with sparse and varicose side branches in the mesothoracic ganglion, which resemble the metathoracic axonal branches. The metathoracic axonal branches are mostly restricted to the dorsal neuropil and the dorsal part of the intermediate neuropil where local non-spiking interneurones and motor neurones controlling movements of the hind leg also project. The overlap between the branches of the sensory afferents and the intersegmental interneurones in the mesothoracic ganglion and between those of the nonspiking local interneurones or motor neurones and intersegmental interneurones in the metathoracic ganglion suggest that these interneurones are responsible for transferring information about the action of one leg to an adjacent leg.

Animals↗
PubMed1990

Morphology of a population of mechanosensory ascending interneurones in the metathoracic ganglion of the locust.

A population of ascending interneurones with cell bodies in the metathoracic ganglion of the locust is described. Interneurones are characterised by their morphology (revealed by intracellular cobalt injection) and by their physiological responses to afferent stimulation. All interneurones have their somata in the ventral cortex of the ganglion, in an area just posterior to the medial tracheae. On the basis of gross morphology the interneurones can be divided into three groups: (1) those that have a main area of fine neurites ipsilateral to the soma and an ipsilateral ascending axon; (2) interneurones that also have their main neurites ipsilateral to the soma but have a contralateral ascending axon, and (3) interneurones that have their main stimulation of sensory receptors on the hind leg ipsilateral to the main neurites. Interneurones receiving excitatory inputs from tactile hairs on the hind leg have branches in the most ventral neuropil, whereas interneurones receiving input from leg proprioceptors have branches in the more intermediate and dorsolateral neuropil. The branching pattern of an interneurone and the size and position of the receptive field on the leg are correlated. Interneurones with restricted branching patterns have restricted receptive fields. The position of the ventral branching reflects the position of the receptive field on the leg. An interneurone with a receptive field restricted to the femur has ventral branches in an anterior position in the ganglion; an interneurone with a receptive field restricted to the tarsus has ventral branches in a more posterior position.

Animals↗
PubMed1990

Morphological variability, segmental relationships, and functional role of a class of commissural interneurons in the spinal cord of goldfish.

As part of an attempt to understand the spinal control of the segmented axial musculature in goldfish, commissural spinal interneurons that are electronically coupled to the Mauthner axon (M-axon) were studied with intracellular recording and staining to examine their morphology, segmental relationships, and functional role. Prior studies suggested that these cells might mediate the crossed inhibition that blocks excitation of motoneurons on one side of the body during an escape bend to the opposite side. Simultaneous intracellular recordings from a M-axon, a commissural interneuron coupled to it, and a presumed primary motoneuron show that: (1) the interneurons produce monosynaptic, Cl(-)-dependent IPSPs in contralateral motoneurons, (2) the interneurons are responsible for the short latency, crossed spinal inhibition in the M-cell network, and (3) more than one interneuron terminates on each postsynaptic cell. Reconstructions of interneurons from wholemounts show that they form a fairly homogeneous morphological class of cells. Each one is unipolar, with an axon that crosses the cord and then usually bifurcates into a short, thin ascending branch and a thicker, longer descending one. Neighboring interneurons have overlapping terminal arbors consistent with the physiological data showing convergence of interneurons onto the same postsynaptic cell. The interneurons showed little relationship with body segments as defined by ventral roots. Their axons usually straddled segmental boundaries, with terminals typically occupying parts of two adjacent segments. Thus the functional unit of these cells is probably not a segment or a complete group of segments, but instead includes only parts of two adjacent segments. The presence of interneurons like these suggests that the overt peripheral segmentation of trunk musculature is not necessarily reflected in the organization of neurons that control those segments. A consideration of some functional characteristics of the activation of overlapping, serially repeated arrays of interneurons by descending pathways leads to the conclusion that the high conduction velocity of the M-axon, and the large size and short longitudinal extent of the axons of the inhibitory interneurons promote a strong, brief inhibition that is appropriate for the production of an escape turn that has a rapid bend to one side.

Animals↗
PubMed1994

Development of interneurons with ipsilateral projections in embryonic rat spinal cord.

Considerable progress has been made in recent years in identifying molecules with restricted expression in mammalian spinal cord at early developmental stages. However, the significance of the different expression patterns for most of these molecules is unclear because so little is known about the development of various classes of spinal interneurons. Recently, we have characterized the development of rat spinal cord interneurons with an axon that crosses in the ventral commissure (Silos-Santiago and Snider, J. Comp. Neurol., 325:514, 1992). In the current study, we describe the morphological development of ipsilaterally projecting spinal interneurons in laminae V-VIII of the thoracic spinal cord. These neurons were labelled by retrograde lateral diffusion of DiI after crystals were placed in various locations in the embryonic thoracic cord. By E14, approximately 48 hours after the first interneurons are generated, eight different groups of ipsilateral interneurons are present in the spinal cord. By E15, these groups of ipsilateral interneurons have reached distinct locations within the gray matter. Even at this early stage, different groups of cells have elaborated characteristic dendritic arborizations. By E19, at least 17 different types of ipsilateral interneurons can be identified on the basis of location and dendritic morphology. In general, ipsilateral interneurons are located more dorsally and laterally than commissural interneurons at all stages of embryonic development. Furthermore, in comparison with commissural neurons, fewer ipsilateral interneurons have dendritic arbors with a mediolateral orientation in the transverse plane. This work demonstrates that rat embryonic spinal cord contains a large number of morphologically distinct classes of interneurons that extend axons into the ipsilateral lateral funiculus. These neurons can be distinguished from commissural neurons on the basis of location and morphology. These results, taken together with those from our previous study, provide a framework for the localization of gene expression to different classes of spinal interneurons at early developmental stages.

Animals↗
PubMed2001

Glutamic acid decarboxylase-67-positive hippocampal interneurons undergo a permanent reduction in number following kainic acid-induced degeneration of ca3 pyramidal neurons.

Kainic acid (KA)-induced degeneration of CA3 pyramidal neurons leads to synaptic reorganization and hyperexcitability in both dentate gyrus and CA1 region of the hippocampus. We hypothesize that the substrate for hippocampal inhibitory circuitry incurs significant and permanent alterations following degeneration of CA3 pyramidal neurons. We quantified changes in interneuron density (N(v)) in all strata of the dentate gyrus and the CA1 and CA3 subfields of adult rats at 1, 4, and 6 months following intracerebroventricular (icv) KA administration, using glutamic acid decarboxylase-67 (GAD-67) immunocytochemistry. At 1 month postlesion, GAD-67-positive interneuron density was significantly reduced in all strata of every hippocampal region except stratum pyramidale of CA1. The reduction in GAD-67-positive interneuron density either persisted or exacerbated at 4 and 6 months postlesion in every stratum of all hippocampal regions. Further, the soma of remaining GAD-67-positive interneurons in dentate gyrus and CA3 subfield showed significant hypertrophy. Thus, both permanent reductions in the density of GAD-67-positive interneurons in all hippocampal regions and somatic hypertrophy of remaining GAD-67-positive interneurons in dentate gyrus and CA3 subfield occur following icv KA. In contrast, the density of interneurons visualized with Nissl in CA1 and CA3 regions was nearly equivalent to that in the intact hippocampus at all postlesion time points. Collectively, these results suggest that persistent reductions in GAD-67-positive interneuron density observed throughout the hippocampus following CA3 lesion are largely due to a permanent loss of GAD-67 expression in a significant fraction of interneurons, rather than widespread degeneration of interneurons. Nevertheless, a persistent decrease in interneuron activity, as evidenced by permanent down-regulation of GAD-67 in a major fraction of interneurons, would likely enhance the degree of hyperexcitability in the CA3-lesioned hippocampus.

Animals↗
PubMed2006

Differential expression of Kv3.1b and Kv3.2 potassium channel subunits in interneurons of the basolateral amygdala.

The expression of Kv3.1 and Kv3.2 voltage-gated potassium channel subunits appears to be critical for high-frequency firing of many neuronal populations. In the cortex these subunits are mainly associated with fast-firing GABAergic interneurons containing parvalbumin or somatostatin. Since the basolateral nuclear complex of the amygdala contains similar interneurons, it is of interest to determine if these potassium channel subunits are expressed in these same interneuronal subpopulations. To investigate this issue, peroxidase and dual-labeling fluorescence immunohistochemistry combined with confocal laser scanning microscopy was used to determine which interneuronal subpopulations in the basolateral nuclear complex of the rat amygdala express Kv3.1b and Kv3.2 subunits. Antibodies to parvalbumin, somatostatin, calretinin, and cholecystokinin were used to label separate subsets of basolateral amygdalar interneurons. Examination of immunoperoxidase preparations suggested that the expression of both channels was restricted to nonpyramidal interneurons in the basolateral amygdala. Somata and proximal dendrites were intensely-stained, and axon terminals arising from presumptive basket cells and chandelier cells were lightly stained. Immunofluorescence observations revealed that parvalbumin+ neurons were the main interneuronal subpopulation expressing the Kv3.1b potassium channel subunit in the basolateral amygdala. More than 92-96% of parvalbumin+ neurons were Kv3.1b+, depending on the nucleus. These parvalbumin+/Kv3.1b+ double-labeled cells constituted 90-99% of all Kv3.1b+ neurons. Parvalbumin+ neurons were also the main interneuronal subpopulation expressing the Kv3.2 potassium channel subunit. More than 67-78% of parvalbumin+ neurons were Kv3.2+, depending on the nucleus. However, these parvalbumin+/Kv3.2+ double-labeled cells constituted only 71-81% of all Kv3.2+ neurons. Most of the remaining neurons with significant levels of the Kv3.2 subunit were somatostatin+ interneurons. These Kv3.2-containing somatostatin+ interneurons constituted 27-50% of the somatostatin+ population, depending on the nucleus in question. These data suggest that both fast-firing and burst-firing parvalbumin+ interneurons in the basolateral amygdala express the Kv3.1b subunit. The significance of Kv3.2 expression in some parvalbumin+ and somatostatin+ interneurons remains to be determined.

Amygdala↗
PubMed1998

Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro.

1. Hippocampal non-principal neurons at the stratum radiatum-stratum lacunosum-moleculare border (R-LM interneurons) of the CA1 area may constitute several cell classes and have been implicated in the generation of GABAergic unitary IPSPs. Using biocytin-filled electrodes we recorded R-LM interneurons intracellularly in vitro and determined their postsynaptic effects in concomitantly recorded pyramidal cells. 2. Light microscopic analysis revealed four populations of R-LM interneurons with distinct axons: (1) basket cells (n = 4) with axons predominantly ramifying in the pyramidal cell layer; (2) Schaffer collateral/commissural pathway-associated interneurons (n = 10) stratifying in stratum radiatum and, to a lesser extent, stratum oriens; (3) perforant pathway-associated interneurons (n = 6) innervating the perforant path termination zone in stratum lacunosum-moleculare of the CA1 area as well as equivalent portions of the dentate gyrus and subiculum; and (4) neurogliaform interneurons (n = 2) characterized by their dense, compact axonal and dendritic arbour. 3. Random electron microscopic sampling of synaptic targets revealed a preponderance of pyramidal neurons as postsynaptic elements. Basket cells had a synaptic target preference for somata and proximal dendrites, whereas the remainder of R-LM interneurons innervated dendritic shafts and spines. The axon of dendrite-targeting cells formed up to six putative contacts with individual postsynatpic pyramidal cells. 4. Anatomically recovered R-LM interneurons (n = 22) had a mean resting membrane potential of -56.7 +/- 3.6 mV, a membrane time constant of 12.9 +/- 7.7 ms and an input resistance of 86.4 +/- 29.2 M omega. Depolarizing current pulses generally elicited overshooting action potentials (70.8 +/- 6.9 mV) which had a mean duration, when measured at half-amplitude, of 0.7 +/- 0.1 ms. In response to prolonged (> 200 ms) depolarizing current pulses all R-LM interneurons displayed (a varying degree of) spike frequency adaptation. 5. Basket cells, Schaffer-associated and neurogliaform interneurons elicited small-amplitude (< 2 mV), short-latency IPSPs in postsynaptic pyramids (n = 5, 13 and 1, respectively). Those interactions in which an effect was elicited with the repetitive activation of the presynaptic neuron (n = 13) showed a substantial degree of postsynaptic response summation. Unitary IPSPs had fast kinetics and, whenever tested (n = 5; 1 basket cell and 4 Schaffer-associated interneurons), were abolished by the GABAA receptor antagonist bicuculline. 6. Thus, R-LM interneurons comprise several distinct populations which evoke fast GABAA receptor mediated IPSPs. The domain-specific innervation of postsynaptic pyramidal cells suggests functionally diverse effects on the integration of afferent information in functionally non-equivalent compartments of pyramidal cells.

Action Potentials↗
PubMed1981

Common interneurones in reflex pathways from group 1a and 1b afferents of ankle extensors in the cat.

1. Input from group I afferents of ankle and toe extensors, other muscles, skin nerves and descending tracts to interneurones of Rexed's laminae V-VI in the cat spinal cord was analysed using intracellular recording from these interneurones. Adequate stimuli (muscle stretches) were used to activate selectively group Ia muscle spindle afferents of triceps surae and plantaris while other fibre systems were excited electrically. 2. Ia and Ib afferents of ankle and toe extensors were found to co-excite, co-inhibit or exert opposite synaptic actions in 41, 33, and 50% of the analysed interneurones, respectively. Taking into account both excitatory and inhibitory input from these two groups of afferents, 64% of the interneurones appeared to be used in common in reflex pathways from muscle spindles and tendon organs of ankle and toe extensors. 3. Selective input from Ib afferents of triceps surae and plantaris (excitation and/or inhibition) was found in 36% of the interneurones; there was evidence for a similarly selective input from Ia afferents. 4. A great majority (over 90%) of the interneurones excited by group I afferents were also inhibited by group I afferents, from either the same or other muscles. 5. Both monosynaptic and disynaptic e.p.s.p.s from Ia and/or Ib afferents from other muscles and from fibres in the ipsilateral funiculi were found in a great proportion of the same interneurones, together with disynaptic e.p.s.p.s from low threshold cutaneous afferents. 6. Intracellular staining with horseradish peroxidase revealed four different patterns of axonal projections of the analysed interneurones: (i) projections to motor nuclei and the intermediate region, (ii and III) projections only to the intermediate region, locally or combined with projections to different rostro-caudal levels, and (iv) projections to the opposite side of the spinal cord. 7. A large proportion of interneurones projecting to motor nuclei displayed input from both Ia and Ib afferents although such an input was a feature of interneurones with other projections as well. No systematic differences in the input from group I afferents were found for interneurones with different axonal projections. In contrast disynaptic e.p.s.p.s of cutaneous origin and monosynaptic e.p.s.p.s upon stimulation of ipsilateral spinal tracts appeared predominantly in interneurones projecting to motor nuclei.

Afferent Pathways↗
PubMed1985

Organization of input to the interneurones mediating group I non-reciprocal inhibition of motoneurones in the cat.

Patterns of convergence of different presynaptic fibre types onto interneurones mediating non-reciprocal inhibition of motoneurones have been studied in order to investigate to what extent the population of these interneurones is homogeneous or can be divided into subgroups on the basis of their input. In a sample of interneurones, all of which were interposed in pathways from the group I afferents of one group of muscles (triceps surae and plantaris), individual interneurones exhibited a wide variety of convergence patterns. Some interneurones were influenced by only a few types of afferent or descending fibre systems whereas others were influenced by many. Furthermore, various fibre systems excited and/or inhibited individual interneurones in different combinations. While there appeared to be too many patterns of convergence to allow any simple classification into a few distinct groups of interneurones, two possibilities were considered. One was that certain presynaptic fibre types influence individual interneurones in preferred combinations. The other was that they converge entirely at random. To investigate this, the frequencies of convergence of various pairs of fibre types were predicted assuming that each of them influences a proportion of the interneurones independently of other sources. Generally, there was close correspondence between such predicted and observed frequencies of occurrence of tested combinations of input. These findings are thus compatible with an organization whereby individual presynaptic fibres innervate a random sample of the population of interneurones. Deviations from the predicted incidence of convergence patterns were found primarily for synaptic actions mediated di- or oligosynaptically and are attributed to a consequence of convergence at the pre-interneuronal level. A particular consequence of such an organization is that interneurones in pathways of non-reciprocal inhibition are shared by afferents of different muscles in a continuum of combinations. The functional implications of this arrangement are discussed.

Action Potentials↗
PubMed1994

Interneurones in pathways from group II muscle afferents in sacral segments of the feline spinal cord.

1. Properties of dorsal horn interneurones that process information from group II muscle afferents in the sacral segments of the spinal cord have been investigated in the cat using both intracellular and extracellular recording. 2. The interneurones were excited by group II muscle afferents and cutaneous afferents but not by group I muscle afferents. They were most effectively excited by group II afferents of the posterior biceps, semitendinosus, triceps surae and quadriceps muscle nerves and by cutaneous afferents running in the cutaneous femoris, pudendal and sural nerves. The earliest synaptic actions were evoked monosynaptically and were very tightly locked to the stimuli. 3. EPSPs evoked monosynaptically by group II muscle afferents and cutaneous afferents of the most effective nerves were often cut short by disynaptic IPSPs. As a consequence of this negative feedback the EPSPs gave rise to single or double spike potentials and only a minority of interneurones responded with repetitive discharges. However, the neurones that did respond repetitively did so at a very high frequency of discharges (0.8-1.2 ms intervals between the first 2-3 spikes). 4. Sacral dorsal horn group II interneurones do not appear to act directly upon motoneurones because: (i) these interneurones are located outside the area within which last order interneurones have previously been found and (ii) the latencies of PSPs evoked in motoneurones by stimulation of the posterior biceps and semitendinosus, cutaneous femoris and pudendal nerves (i.e. the main nerves providing input to sacral interneurones) are compatible with a tri- but not with a disynaptic coupling. Spatial facilitation of EPSPs and IPSPs following synchronous stimulation of group II and cutaneous afferents of these nerves shows, however, that sacral interneurones may induce excitation or inhibition of motoneurones via other interneurones. 5. Comparison of the properties of group II interneurones in the sacral segments with those of previously studied group II interneurones in the midlumbar segments leads to the conclusion that these two populations of neurones are specialized for the processing of information from different muscles and skin areas. In addition, equivalents of only one of the two subpopulations of midlumbar interneurones have been found at the level of the pudendal nucleus: neurones with input from group II but not from group I muscle afferents. Neurones integrating information from group I and II muscle afferents and in direct contact with motoneurones thus seem to be scarce in the sacral segments.(ABSTRACT TRUNCATED AT 400 WORDS)

Afferent Pathways↗