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PubMed1998

Synaptic connectivity of distinct hilar interneuron subpopulations.

Dual intracellular recordings of hilar interneurons and CA3 pyramidal cells were performed in transverse slices of guinea pig hippocampus in the presence of the convulsant compound 4-aminopyridine (4-AP) and ionotropic glutamate receptor antagonists. Under these conditions, interneurons burst fire synchronously, producing synchronized inhibitory postsynaptic potentials (sIPSPs) in pyramidal cells. Three different hilar interneuron subpopulations that contributed to the sIPSP were identified based on their projection properties and morphology. These three types were pyramidal-like stellate interneurons, spheroid interneurons, and oviform interneurons. Physiologically, pyramidal-like stellate interneurons could be differentiated from the other interneuron subpopulations because they generated short synchronized bursts of action potentials coincident with the hyperpolarizing and depolarizing gamma-aminobutyric acid-A (GABAA)-mediated inhibitory postsynaptic potentials (IPSPs) recorded in pyramidal cells. The bursts in pyramidal-like stellate cells were abolished by theGABAA-receptor blocker, bicuculline. In contrast, spheroid interneurons of the dentate-hilus (D-H) border and oviform hilar interneurons exhibited prolonged bicuculline-resistant bursts that occurred coincident with the GABAB pyramidal cell sIPSPs. Pyramidal-like stellate interneurons likely did not contribute to the generation of synchronized GABAB responses in hippocampal pyramidal cells. Spheroid interneurons were unique among these subpopulations of interneurons in that the bicuculline-resistant bursts in spheroid interneurons were sustained by a synaptic depolarization that persisted in the presence of antagonists of ionotropic glutamate, GABAA and GABAB receptors [6-cyano-7-nitroquinoxaline-2,3-dione, 20 microM; 3-3(2-carboxipiperazine-4-yl)propyl-1-phosphonate, 20 microM; bicuculline, 10-15 microM; CGP 55845A, 20 microM]. This novel depolarizing potential reversed between -30 and 0 mV. No noticeable synaptic depolarization sustaining burst firing could be isolated in oviform interneurons, suggesting that firing in this interneuron subpopulation was synchronized by nonsynaptic mechanisms. The results of the present study indicate that the hilar inhibitory circuit is composed of at least three different subpopulations of interneurons, distinguishable by their morphological characteristics and synaptic inputs and outputs. These findings give further support to the hypothesis that there are distinct populations of interneurons producing GABAA and GABAB responses with defined functional roles within the hippocampal inhibitory circuit. Notably, we found that spheroid interneurons were unique among the hilar interneurons studied, in that the synchronized bursts observed in these cells are sustained by a novel ionotropic glutamate and GABA receptor-independent synaptic depolarization.

4-Aminopyridine↗
PubMed2002

Cortical interneurons: from Cajal to 2001.

After the collective work of many investigators, beginning with the early studies of Cajal, the following main [figure: see text] conclusions may be drawn regarding the morphology, biochemical characteristics and synaptic connections of interneurons: 1. Interneurons show a great variety of morphological, biochemical and physiological types. They constitute approximately 15-30% of the total population of neurons. 2. Because of the heterogeneity of interneurons and the lack of consensus as to which characteristics are essential for an individual neuron to be considered a member of a given cell type, there is no definitive classification of interneurons. Nevertheless, certain interneurons can be readily recognized by their unique morphological characteristics, or they can be more generally divided into subgroups on the basis of their biochemical characteristics, patterns of axonal arborization, or synaptic connections with pyramidal cells. 3. All interneurons have a more or less dense axonal arborization distributed near the cell body, mainly within the area occupied by their dendritic field. However, some interneurons may display, in addition, prominent long, horizontal or vertical axonal collaterals. [figure: see text] 4. Most interneurons form symmetrical synapses with both pyramidal cells and other interneurons, with the exception of chandelier cells, which only form synapses with the axon initial segment of pyramidal cells. Furthermore, interneurons are not only connected by chemical synapses (unidirectional connections), but they may also form electrical synapses through gap junctions (bidirectional) in a specific manner. 5. With the exception of chandelier cells, other types of interneurons include among their synaptic targets more than one type of postsynaptic element. But the degree of preference for these postsynaptic elements varies markedly between different types of interneurons. 6. The number of synapses made by a single axon originating from a given interneuron on another neuron is on the order of ten or less. Since, in general, cortical neurons receive many more interneuronal (symmetrical) synapses (on the order of a few hundred or thousand), a considerable convergence of various types of interneurons to pyramidal cells and interneurons appears to occur. 7. Most interneurons are GABAergic and also express a number of different neurotransmitters (or their synthesizing enzymes), neuropeptides and calcium-binding proteins. Thus, interneurons are, biochemically, widely heterogeneous. 8. Some of the morphologically identifiable neurons can be characterized by their particular biochemical characteristics, and some biochemically definable subgroups of interneurons display a particular morphology. However, different morphological types of GABAergic neurons may share one or several neurotransmitters, neuroactive substances and/or other molecular markers. Therefore, a great variety of subgroups of morphologically and biochemically identifiable neurons exist. 9. Some interneurons appear to be common to all species and, therefore, may be considered as basic elements of cortical circuits, whereas others may represent evolutionary specializations which are characteristic of particular mammalian subgroups and, thus, cannot be taken as essential, or general, features of cortical organization. 10. Given the complexity of cortical circuits and the areal and species differences, it is impossible to draw a "sufficiently" complete basic diagram of cortical microcircuitry that is valid for all cortical areas and species.

Animals↗
PubMed1982

Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology.

1. As part of a continuing investigation of the organization of the spinal cord of the lamprey, propriospinal interneurons with axons projecting contralaterally and caudally (CC interneurons) were surveyed with intracellular recordings. 2. CC interneurons were identified by recording their axon spikes extracellularly in the spinal cord during intracellular stimulation of the cell body. The axon projections of Cc interneurons were confirmed after intracellular injection and development of horseradish peroxidase. 3. Intracellular stimulation of CC interneurons produced synaptic potentials in myotomal motoneurons, lateral interneurons and other CC interneurons that lay caudally on the opposite side of the spinal cord. Most CC interneurons were inhibitory, but some were excitatory. 4. CC interneurons were divided into three classes on the basis of reticulospinal Müller cell inputs. CC1 interneurons were excited by the ipsilateral Müller cell B1 and the contralateral Mauthner cell. CC1 interneurons were inhibitory. They were excited polysynaptically by ipsilateral sensory dorsal cells and were inhibited by contralateral dorsal cells. They were distinguished morphologically by having no rostral axon branch and no contralateral dendrites. CC1 interneurons were phasically active during fictive swimming with their peak depolarizations preceding those of myotomal motoneurons by about 0.15 cycle. 5. CC2 interneurons were also inhibitory, but they were distinguished from CC1 interneurons by their excitation from the ipsilateral Müller cells B2-4 nd by their thin rostral and thicker caudal axonal branches on the contralateral side of the spinal cord. 6. CC3 interneurons were excitatory, and they were inhibited by the ipsilateral Müller cell I1. CC3 interneurons could have contralateral dendrites and bifurcating axons, and they had lower average axonal conduction velocities than CC1 and CC2 interneurons. 7. Inhibitory CC interneurons may be important for motor coordination in the lamprey. Movements of the lamprey body during reflexes and swimming consist of contraction and relaxation of myotomal muscles on opposite sides of the body. By being coactive with ipsilateral myotomal motoneurons, inhibitory CC interneurons could contribute to the inhibition of contralateral motoneurons during these movements.

Animals↗
PubMed1990

Input and output connections of an anteromedial group of spiking local interneurons in the metathoracic ganglion of the locust.

Intracellular recordings were made from an anteromedial group of spiking local interneurons in the metathoracic ganglion of the locust to determine the input connections that shape their mechanoreceptive fields on a hindleg and the output connections that define their effects on hindleg motor neurons. The receptive fields of these interneurons may contain excitatory and inhibitory regions. An excitatory region on the ipsilateral hind leg is formed by direct excitatory connections of the afferents from exteroceptors. Afferent spikes consistently evoke EPSPs in interneurons with a central synaptic latency of 1.2-1.5 msec. The connections appear to be direct and chemically mediated. An inhibitory region of a receptive field is not formed by direct afferent connections. Instead, spiking local interneurons of a midline group, which also receive direct excitatory inputs from the afferents, make direct inhibitory connections with anteromedial interneurons. Spikes in particular midline interneurons consistently evoke IPSPs in anteromedial interneurons with a central synaptic latency of about 1.0 msec. The connections appear to be direct and chemically mediated. By contrast, spikes in anteromedial interneurons could not be linked to any synaptic potentials in midline interneurons, so that direct connections are unidirectional and inhibitory. The large inhibitory regions to the receptive fields of anteromedial interneurons result from convergent inhibitory inputs of several midline interneurons. Each midline interneuron may make inhibitory output connections with several anteromedial interneurons, but there is a high degree of specificity in these divergent connections. Anteromedial interneurons make excitatory output connections with specific hind leg motor neurons. EPSPs in motor neurons follow spikes in the interneurons with short and consistent synaptic latencies of about 1.0 msec. The connections appear to be direct and chemically mediated. Two or more anteromedial interneurons with overlapping receptive fields may converge onto one motor neuron, and, in turn, one interneuron may make divergent connections with several motor neurons of the same pool. This pattern of connections suggests that these interneurons are essential elements in the local circuitry responsible for the expression of local reflexes of a leg. They provide an excitatory drive to the motor neurons in parallel to that from nonspiking local interneurons when particular arrays of exteroceptors are stimulated.

Action Potentials↗
PubMed1996

Electrophysiological and morphological properties of interneurones in the rat dorsal lateral geniculate nucleus in vitro.

1. Intracellular recordings were made from putative interneurones (n = 24) and thalamocortical (TC) projection neurones (n = 45) in slice preparations of the rat dorsal lateral geniculate nucleus (dLGN) in order to compare the electrophysiological properties of these neuronal types. 2. Intracellular injection of biocytin to electrophysiologically identified neurones (n = 34) revealed the morphology of putative interneurones (n = 4) to be similar to class B and that of TC neurones (n = 30) to be similar to class A Golgi-impregnated neurones. 3. Interneurones had resting membrane potentials (-52 mV) relatively positive to those of TC neurones (-63 mV), shorter time constants (36.8 and 58.2 ms, respectively), but similar steady-state input resistances (164 and 180 M omega, respectively). Steady-state voltage-current relationships were nearly linear in interneurones, but highly non-linear in TC neurones. 4. The structure of action potential firing evoked at the break of hyperpolarizing voltage transients was dependent upon neuronal type. Interneurones fired a single action potential or a burst of action potentials with a maximum frequency of < 130 Hz, whilst TC neurones fired a high frequency burst with a minimum frequency of > 250 Hz. In addition, well-defined burst firing of action potentials in response to depolarizing voltage excursions, from membrane potentials negative to -65 mV, could be evoked in TC neurones, but not in interneurones. 5. The directly evoked action potentials of interneurones were characterized by an initial slow pre-potential preceding the fast upstroke of the action potential. The amplitude and width of interneurones' action potentials were smaller than those of TC neurones and the amplitude and duration of the single action potential after-hyperpolarization were greater in interneurones. Both interneurones and TC neurones fired action potentials repetitively in response to suprathreshold voltage excursions, with interneurones demonstrating a greater degree of spike-frequency adaptation. Following a train of action potentials, interneurones and TC neurones generated a slow after-hyperpolarizing potential: in interneurones but not TC neurones this potential was followed by a slow depolarizing potential. 6. An intrinsic, subthreshold membrane potential oscillatory activity with a mean frequency of approximately 8 Hz was observed in interneurones. 7. Electrical stimulation of the optic tract evoked in interneurones apparently pure EPSPs, pure IPSPs or a mixture of EPSPs and IPSPs. EPSPs were found to be biphasic and mediated by the activation of non-N-methyl-D-aspartate (NMDA) and NMDA excitatory amino acid receptors. IPSPs and the response to the iontophoretic application of GABA were found to reverse between -65 and -70 mV. The application of GABAB receptor agonists failed to affect the membrane properties of six of seven interneurones tested. In addition spontaneous EPSPs and IPSPs were recorded in interneurones. 8. These results demonstrate that the electrophysiological properties of putative interneurones are distinct from those of TC neurones of the rat dLGN. The implications of these findings for the control of visual responsiveness of TC neurones are discussed.

Animals↗
PubMed2003

Use-dependent shift from inhibitory to excitatory GABAA receptor action in SP-O interneurons in the rat hippocampal CA3 area.

Cortical inhibitory interneurons set the pace of synchronous neuronal oscillations implicated in synaptic plasticity and various cognitive functions. The hyperpolarizing nature of inhibitory postsynaptic potentials (IPSPs) in interneurons has been considered crucial for the generation of oscillations at beta (15-30 Hz) and gamma (30-100 Hz) frequency. Hippocampal basket cells and axo-axonic cells in stratum pyramidale-oriens (S-PO) play a central role in the synchronization of the local interneuronal network as well as in pacing of glutamatergic principal cell firing. A lack of conventional forms of plasticity in excitatory synapses onto interneurons facilitates their function as stable neuronal oscillators. We have used gramicidin-perforated and whole cell clamp recordings to study properties of GABAAR-mediated transmission in CA3 SP-O interneurons and in CA3 pyramidal cells in rat hippocampal slices during electrical 5- to 100-Hz stimulation and during spontaneous activity. We show that GABAergic synapses onto SP-O interneurons can easily switch their mode from inhibitory to excitatory during heightened activity. This is based on a depolarizing shift in the GABAA reversal potential (EGABA-A), which is much faster and more pronounced in interneurons than in pyramidal cells. We also found that the shift in interneuronal function was frequency dependent, being most prominent at 20- to 40-Hz activation of the GABAergic synapses. After 40-Hz tetanic stimulation (100 pulses), GABAA responses remained depolarizing for approximately 45 s in the interneurons, promoting bursting in the GABAergic network. Hyperpolarizing EGABA-A was restored >60 s after the stimulus train. Similar but spontaneous GABAergic bursting was induced by application of 4-aminopyridine (100 microM) to slices. A shift to depolarizing IPSPs by the GABAAR permeant weak acid anion formate provoked interneuronal population bursting, supporting the role of GABAergic excitation in burst generation. Furthermore, depolarizing GABAergic potentials and synchronous interneuronal bursting were enhanced by pentobarbital (100 microM), a positive allosteric modulator of GABAARs, and were blocked by picrotoxin (100 microM). Intriguingly, GABAergic bursts displayed short (<1 s) oscillations at 15-40 Hz, even though only depolarizing GABAA responses were seen in the SP-O interneurons. This beta-gamma rhythmicity in the interneuron network was dependent on electrotonic coupling, and was abolished by blockade of gap junctions with carbenoxolone (200 microM). Results here implicate the rapid activity-dependent degradation of hyperpolarizing IPSPs in SP-O interneurons in setting the temporal limits for a given interneuron to participate in beta-gamma oscillations synchronized by GABAergic synapses. Furthermore, they imply that mutual GABAergic excitation provided by interneurons may be an integral part in the function of neuronal networks. We suggest that the use-dependent change in EGABA-A could represent a form of short-term plasticity in interneurons promoting coherent and sustained activation of local GABAergic networks.

Animals↗
PubMed1983

Spiking local interneurons as primary integrators of mechanosensory information in the locust.

A population of spiking local interneurons in the metathoracic ganglion of the locust is vigorously excited by particular sensory stimuli from the hindlegs and participates in local postural reflexes. We examined the inputs from singly innervated mechanoreceptors (hairs and campaniform sensilla) to these spiking local interneurons, to nonspiking local interneurons, and to motor neurons that are also elements of local reflex pathways. Recordings were made intracellularly from the interneurons and motor neurons and extracellularly from afferent fibers. The physiological evidence is consistent with the spiking local interneurons being excited by direct, chemically mediated synaptic inputs from the afferents. Each afferent spike is followed at a constant latency by an excitatory postsynaptic potential (EPSP) in a spiking local interneuron, even at instantaneous frequencies as high as 300 Hz. The estimated synaptic delay is 1.5 ms, similar to that measured at other presumed monosynaptic connections within the same ganglion. Cobalt stains of individual interneurons, and of the central projections of afferent fibers show that both branch within the same ventral region of neuropil. Afferents from several hairs and campaniform sensilla converge on an individual spiking local interneuron. One interneuron is shown to receive inputs from at least seven hairs and four campaniform sensilla, but these represent only a tiny fraction of the total number of such sensilla on a hindleg. Practical limitations to the number of sensilla that can be tested for each interneuron means that the degree of convergence is likely to be considerably underestimated. We found no evidence that nonspiking local interneurons or motor neurons receive direct inputs from the afferents tested. Neurons of both types are, however, affected by stimulation of individual hairs, and the resulting pattern of postsynaptic potentials (PSPs) is similar to the pattern of spikes evoked in the spiking local interneurons. We infer from the evidence presented here and elsewhere (10, 11) that the spiking local interneurons are involved in at least two types of pathways for local interactions: 1) sensory neuron-spiking local interneuron-motor neuron, and 2) sensory neuron-spiking local interneuron-nonspiking local interneuron-motor neuron. We conclude that the spiking local interneurons are major elements in the primary integration of inputs from external receptors on the hindlegs.

Animals↗
PubMed1987

Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology.

Electrophysiological and anatomical techniques were used to determine the role, in the hippocampal circuitry, of local circuit neurons located at the oriens/alveus border (O/A interneurons). Intracellular recording from these cells showed that their response characteristics were clearly nonpyramidal: high input resistance, short membrane time constant, short-duration action potential, pronounced, brief afterhyperpolarizations (AHP), and nondecremental firing during intrasomatic depolarizing current pulses. Intracellular Lucifer yellow (LY) injection and subsequent fluorescence microscopy confirmed their nonpyramidal nature. O/A interneuron somata were bipolar or multipolar; their dendrites projected mostly parallel to the alveus, except for 1 or 2 processes that turned perpendicularly, and ascended through stratum oriens and pyramidale and into radiatum. Their axons were seen to branch profusely in stratum oriens and pyramidale. Simultaneous intracellular recordings from O/A interneurons and CA 1 pyramidal cells showed that pyramidal cells directly excite these interneurons. Major hippocampal afferents also directly excited the O/A interneurons. In a small number of interneuron-pyramidal pairs, stimulation of the O/A interneuron directly inhibited pyramidal cells. In one case, reciprocal connections were observed: The pyramidal cell excited the interneuron, and the interneuron inhibited the pyramidal cell. In 1 interneuron-to-interneuron pair, an inhibitory connection from O/A interneuron to stratum pyramidale interneuron was also observed. With intracellular HRP injections into O/A interneurons and subsequent electron microscopy, we observed that O/A interneuron axons made contacts with pyramidal and nonpyramidal cells. HRP-filled symmetric synaptic contacts were found on pyramidal cell dendrites and somata. HRP-filled axons also made contacts with pyramidal cell initial segments. HRP-filled O/A interneuron axon contacts were also found on nonpyramidal cell dendrites in stratum oriens. These electrophysiological and anatomical results suggest that O/A interneurons make synaptic contact with pyramidal cells and may mediate feedforward and feedback inhibition onto CA 1 pyramidal cells.

Animals↗
PubMed1987

Inhibitory interactions between spiking and nonspiking local interneurons in the locust.

Simultaneous intracellular recordings were made from pairs of spiking and nonspiking local interneurons in the metathoracic ganglion of the locust to search for interactions that might underlie tactile and proprioceptive reflexes of a leg. A spike in a spiking local interneuron is followed after a consistent latency (0.6 +/- 0.12 msec, mean +/- SD) by an IPSP in a particular nonspiking interneuron. The connection appears to be direct and chemically mediated. By contrast, manipulating the membrane potential of a nonspiking interneuron by injecting current through the recording electrode has no direct effect on a spiking local interneuron. The direct interactions between pairs of these local interneurons are thus one-way. If, however, the current injected into a nonspiking interneuron is sufficient to evoke a movement by exciting motor neurons, then the spiking interneuron can be excited or inhibited by the resulting reafference. The spiking local interneurons have excitatory regions in their receptive fields formed by arrays of exteroreceptors or by proprioceptors at specific joints. The inhibitory connections mean that the postsynaptic nonspiking interneurons have corresponding inhibitory regions to their receptive fields. Several spiking local interneurons with similar receptive fields may converge onto one nonspiking interneuron. Some nonspiking interneurons, however, have larger receptive fields than an individual spiking interneuron, again indicating convergence of inputs. The specificity of the inhibitory connections preserves the spatial representation of sensory information for use in particular reflexes. For example, touching hairs on the ventral femur evokes a reflex extension of the tibia. Spiking interneurons excited by these receptors inhibit a nonspiking interneuron that would cause the opposing and therefore unwanted flexion movement. Viewed in this behavioral context, the pattern of connections between the local interneurons forms the basis of the circuitry for the local reflex adjustments of posture and locomotion.

Action Potentials↗
PubMed2001

Cerebral-buccal pathways in Aplysia californica: synaptic connections, cooperative interneuronal effects and feedback during buccal motor programs.

Ingestion of seaweed by Aplysia is in part mediated by cerebral-buccal interneurons that drive rhythmic motor output from the buccal ganglia and in some cases cerebral-buccal interneurons act as members of the feeding central pattern generator. Here we document cooperative interactions between cerebral-buccal interneuron 2 and cerebral-buccal interneuron 12, characterize synaptic input to cerebral-buccal interneuron 2 and cerebral-buccal interneuron 12 from buccal peripheral nerve 2,3, describe a synaptic connection between cerebral-buccal interneuron 1 and buccal neuron B34, further characterize connections made by cerebral-buccal interneurons 2 and -12 with B34 and B61/62, and describe a novel, inhibitory connection made by cerebral-buccal interneuron 2 with a buccal neuron. When cerebral-buccal interneurons 2 and 12 were driven synchronously at low frequencies, ingestion-like buccal motor programs were elicited, and if either was driven alone, indirect synaptic input was recruited in the other cerebral-buccal interneuron. Stimulation of BN2,3 recruited both ingestion and rejection-like motor programs without firing in cerebral-buccal interneurons 2 or 12. During motor programs elicited by cerebral-buccal interneurons 2 or 12, high-voltage stimulation of BN2,3 inhibited firing in both cerebral-buccal interneurons. Our results suggest that cerebral-buccal interneurons 2 and 12 use cooperative interactions to modulate buccal motor programs, yet firing in cerebral-buccal interneurons 2 or 12 is not necessary for recruiting motor programs by buccal peripheral nerve BN2,3, even in preparations with intact cerebral-buccal pathways.

Animals↗
PubMed2000

Effects of monoamines on interneurons in four spinal reflex pathways from group I and/or group II muscle afferents.

Effects of locally applied serotonin (5-HT) and noradrenaline (NA) were tested on extracellularly recorded responses of single spinal interneurons in deeply anaesthetized cats. These effects were tested on: (i) interneurons mediating reciprocal inhibition from group Ia afferents; (ii) interneurons mediating non-reciprocal inhibition from group Ia and Ib afferents; (iii) intermediate zone interneurons co-excited by group I and II afferents; and (iv) dorsal horn interneurons excited by group II afferents. Effects of monoamines were tested on responses evoked at latencies compatible with monosynaptic coupling. Responses evoked by group Ia and/or Ib muscle afferents were facilitated in all of the tested interneurons both by NA and 5-HT. Responses evoked by group II muscle afferents were depressed in the majority of the interneurons but were facilitated in some of them. 5-HT depressed these responses in all dorsal horn interneurons and in one subpopulation of intermediate zone interneurons, while it facilitated them in another subpopulation of intermediate zone interneurons. NA depressed them in all intermediate zone interneurons and in one subpopulation of dorsal horn interneurons, while it facilitated them in another subpopulation of dorsal horn interneurons. The results of this study lead to the conclusions that: (i) modulation of synaptic actions of muscle spindle and tendon organ afferents on spinal interneurons by 5-HT and NA is related to both the type of the afferent and the functional type of the interneuron; and that (ii) 5-HT and NA counteract each others' actions on some interneuronal types but mutually enhance them on the others.

Afferent Pathways↗
PubMed1992

Analysis and modeling of the multisegmental coordination of shortening behavior in the medicinal leech. II. Role of identified interneurons.

1. Mechanical stimulation of the leech, Hirudo medicinalis, elicits withdrawal behavior that has two components: local bending in the segment stimulated and shortening in outlying segments. Local bending is characterized by excitation of longitudinal muscle on one side of the segment and inhibition on the other side. In shortening, all longitudinal muscles are excited. We wished to understand how these distinct motor patterns are produced by a nervous system with segmentally iterated neurons, a configuration that places some limitations on the complexity of connection patterns. 2. We searched for neurons in the segmental nervous system that subserved shortening behavior, expecting to find at least one interneuron in each segment that was involved in shortening behavior exclusively. We found instead that all interneurons involved in shortening are also involved in local bending, and no individual interneuron can completely account for shortening. 3. The motor output caused by individual identified interneurons is not entirely consistent with the shortening motor output pattern. For instance, one interneuron, cell 115, has the same pattern of motor effects from segment to segment, causing excitation of dorsal excitatory motor neurons and inhibition of ventral excitatory motor neurons. These effects would cause dorsal local bending, not shortening, in a few segments. Only one interneuron, cell 125, has motor effects that would cause shortening. 4. Individual interneurons were hyperpolarized while single sensory cells were stimulated, to quantify the contributions of individual interneurons to the observed motor pattern. Interneurons 115 and 125, and the inhibitory motor neuron, cell 1, were found to have significant roles in producing the shortening motor output. 5. A quantitative estimate of the role of each interneuron type showed that the identified interneurons account for most of the excitation of dorsal motor neurons, but for very little of the excitation of ventral motor neurons. This predicts that at least one additional interneuron type remains to be identified, one that would provide excitation to ventral motor neurons in several segments. 6. A back-propagation trained neural network model was constructed to predict the connections of the as yet unidentified interneurons. To match the known properties of interneurons, it was necessary to include a segmental similarity constraint in the training algorithm for segmentally iterated model neurons. The modeled networks predicted that there are at least two kinds of interneurons yet to be found. Also, the modeling showed that interneurons can have input and output patterns that differ very little from segment to segment but yet produce major differences in the motor output.

Action Potentials↗
PubMed1996

Morphology and physiology of abdominal projection interneurones in the locust with mechanosensory inputs from ovipositor hair receptors.

The anatomy and physiological properties of eight non-giant projection interneurones which originate from the locust terminal abdominal ganglion and receive wind and tactile inputs from ovipositor hair receptors are described. Their cell bodies (diameter 25-40 mu m) are clustered in the anterolateral region of the eighth abdominal neuromere, and their axons ascend through either the contralateral or the ipsilateral connective to more anterior abdominal ganglia. In contrast to the giant interneurones, they have small-diameter axons and are not sensitive to cercal hair wind inputs. According to their arborisation pattern within the terminal abdominal ganglion, the non-giant projection interneurones can be divided into those with main central arborisations in the ventral neuropil (anterolateral interneurones 1-6, ALIN1-ALIN6) and those with arborisations in the dorsal neuropil (ALIN7 and ALIN8). Interneurones of the first type possess four to six secondary neurites, which form a dense dendritic field in the ventral neuropil, either contralaterally or ipsilaterally to their soma. Two interneurones have contralaterally ascending axons and main dendritic fields contralateral to their soma. Two interneurones have contralaterally ascending axons and ipsilateral main dendritic fields. One interneurone has an ipsilaterally ascending axon and an ipsilateral main dendritic field. The primary neurites of interneurones with contralateral axons transverse the ganglion through dorsal commissure I. Five interneurones have unilateral ventral dendritic fields. One interneurone possesses bilateral ventral branches. Some interneurones project only in the eighth abdominal neuromere, whereas others send branches posteriorly into the neuropil of the ninth abdominal neuromere. Interneurones of the second type send three to four secondary neurites to the dorsal neuropil of the eighth and ninth abdominal neuromeres. One interneurone has an ascending axon in the ipsilateral connective and the other in the contralateral connective. The axons of the projection interneurones pass through a lateral or dorsal tract to the seventh abdominal ganglion. Their axonal projections are sparse, remain ipsilateral to the axons, and are confined to the dorsomedial neuropil. ALIN1-ALIN7 are depolarised and spike in response to wind and direct mechanical deflection of trichoid sensilla on both left and right ovipositor valves. They respond with more spikes to stimulation of hairs on the ventral valve ipsilateral to their main dendritic field. ALIN8, in contrast, shows a delayed inhibitory/excitatory response.

Abdomen↗
PubMed1997

Distribution of GABAergic premotor nonspiking local interneurones in the terminal abdominal ganglion of the crayfish.

The inhibitory neurotransmitter of premotor nonspiking local interneurones in the crayfish terminal abdominal ganglion was investigated physiologically and immunocytochemically. Depolarization of a nonspiking interneurone evoked a hyperpolarization in a uropod motor neurone. The amplitude of hyperpolarization in the motor neurone was gradually decreased under low-calcium/high-magnesium saline. Local pressure injection of gamma-aminobutyric acid (GABA) into the neuropil caused a similar hyperpolarization of the motor neurone. These physiological studies suggested a GABAergic inhibitory interaction between nonspiking interneurones and the motor neurones. Premotor nonspiking interneurones are classified into two subgroups ofposterolateral (PL) and anterolateral (AL) interneurones, and AL interneurones are further divided into three subtypes. A combination of intracellular staining from nonspiking local interneurones with Lucifer yellow and immunocytochemical staining with an antiserum directed against GABA revealed that all the PL interneurones sampled in this study showed GABA-like immunoreactivity. A population of cell bodies (n = 6-11) with a small diameter (15-30 microm) packed together forming a cluster showed GABA-like immunoreactivity, and the cell bodies of most PL interneurones were found in this cluster. To compare the number and the pattern of main branches of PL interneurones, cells were classified into three identifiable sets of interneurones, called PL-1, PL-2, and PL-3. By contrast, about one-half of AL interneurones, especially the third subtype of AL interneurones, which have cell bodies located ventrolaterally in the ganglion, did not show GABA-like immunoreactivity. Furthermore, the position of cell bodies of GABA-immunoreactive AL interneurones was scattered compared to that of PL interneurones.

Abdomen↗
PubMed1983

Interneurons in the flight system of the locust: distribution, connections, and resetting properties.

The organization and functional properties of interneurons in the flight system of the locust, Locusta migratoria, were investigated by using intracellular recording and staining techniques. Interneurons were found to be distributed within the three thoracic and the first three abdominal ganglia, and they could be subdivided into three organizational categories: (1) members of one of two serially homologous groups controlling either the forewing or the hindwing, (2) unique individuals with no known homologues in other ganglia, and (3) members of a set of serial homologous in the metathoracic and first three abdominal ganglia. Interneurons in the last two categories influenced both forewing and hindwing motoneurons in a similar manner. Thus interneuronal organization is not characterized by two distinct homologous groups of interneurons for the separate control of forewing and hindwing motor activity. Flight interneurons may also form two separate functional categories: (1) those making short latency connections to motoneurons (premotor interneurons), and (2) those which reset the flight rhythm when depolarized by brief current pulses (pattern generator interneurons). None of the ten premotor interneurons we identified influenced the flight rhythm when depolarized and none of the three groups of pattern generator interneurons were found to form short latency connections with motoneurons. This separation of function may allow phase-shifts in motor output for flight control without changes in wingbeat frequency. Pattern generator interneurons influence motor output to both forewings and hindwings. Thus we conclude that the flight rhythm is generated in a distributed neuronal oscillator driving both the pairs of wings. The organization of flight interneurons is considerably more complex than predicted from existing models of the flight system, or anticipated from the relative simplicity of the motor output. Our finding of homologous sets of interneurons in the abdominal ganglia supports the notion that insect flight evoked from a behavior using appendages distributed along the thorax and the abdomen. Thus the organization of flight interneurons may reflect an interneuronal system which controlled the behavior from which flight evolved.

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PubMed1987

Neural control of a cyclic postural behavior in the crayfish, Procambarus clarkii: the pattern-initiating interneurons.

As part of its repertoire of defensive behaviors, the crayfish, Procambarus clarkii, may respond to mildly threatening tactile or visual stimuli from the front of its body by walking backwards. During this behavior, the abdomen undergoes complex cyclical movements involving flexion and extension of the postural musculature which cause the tail to alternately contact and withdraw from the substrate. Intracellular neuropil recordings and dye injections were used to search for the interneurons responsible for initiating this postural motor pattern in the crayfish abdomen. Several diverse morphological types of interganglionic pattern-initiating (PI) interneurons were found. Each interneuron, when driven intracellularly, was capable of eliciting the same motor program, in its entirety, throughout the abdominal nerve cord. During pattern generation, PI interneurons exhibited a burst of spikes preceding the motor output. Silencing single PI interneurons with hyperpolarizing current during pattern generation failed to affect the motor program, indicating a redundancy of pattern-initiating function. The observations of extensive dye-coupling with other parallel axons, consistent dye-coupling with other identified cells in the pattern-initiating system, and the presence of multiple spike amplitudes in the bursts suggested electrotonic coupling among the PI interneurons. An additional group of interganglionic interneurons, the partial pattern-initiating (PPI) interneurons, were found to comprise a significant subset of the pattern-initiating system. As with the PI cells, the PPI interneurons exhibited a complex burst of spikes just preceding the patterned motor program. However, the PPI interneurons were only capable of eliciting an incomplete, though recognizable, postural motor pattern. Silencing any PPI interneuron during pattern generation caused a deficit in the motor pattern, indicating either an absence or lesser degree of functional redundancy within the PPI interneuron population compared to that occurring within the PI interneuron group. We conclude that a large number of PI interneurons are presynaptic to a relatively small group of PPI interneurons which, in turn, conduct pattern-initiating signals to the ganglionic oscillators. Our results indicate that pattern-initiation is accomplished through a command system involving multiple command elements organized in a coordinated interganglionic network.

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PubMed1998

Indications for coupling between feline spinocervical tract neurones and midlumbar interneurones.

The possibility of collateral segmental actions of spinocervical tract (SCT) neurones upon interneurones with input from cutaneous and group II muscle afferents was investigated in deeply anaesthetized cats. To this end, intracellular and/or extracellular recordings were made from 35 dorsal horn and 15 intermediate zone interneurones in midlumbar segments of the spinal cord and effects of stimulation of the ipsilateral dorso-lateral funiculus (DLF) at C3 and C1 levels, i.e. below and above the lateral cervical nucleus where axons of SCT cells terminate, were compared. The stimuli applied at the C3 segment were within the range of stimuli (50-100 microA) required for antidromic activation of SCT neurones in the same experiment. Those applied at the C segment (200-500 microA) were at least 3 times stronger than C3 stimuli. Under the same experimental conditions, long ascending and descending tract neurones (dorsal spino-cerebellar and rubro-spinal tract neurones) with axons in the DLF were activated at similar thresholds from the C and C3 segments. Intracellular recordings were made from 29 interneurones of which 19 (65%) were dorsal horn and 10 (35%) were intermediate zone interneurones. Excitatory postsynaptic potentials (EPSPs) evoked by single stimuli applied at the C3 segment, but not the C segment, were found in 14 (48%) of those interneurones; their latencies (3.0-5.7 ms) and frequency following with only minimal temporal facilitation were as required for potentials being evoked monosynaptically by the fastest conducting SCT neurones. Extracellular recordings were made from 30 interneurones (24 dorsal horn and 6 intermediate zone interneurones), and in these neurones spike potentials induced from the C3, but not from the C segment, were evoked only by short trains of stimuli. However, their latencies from the first effective stimulus (4.3-5.4 ms) were compatible with mono- or oligosynaptically mediated collateral actions of SCT neurones. They were found in 10 (33%) of the 30 investigated interneurones. Similar effects of C3 stimuli were found in similar proportions of dorsal horn interneurones and intermediate zone interneurones. Indications were also found for synaptic actions evoked by C3 stimuli that could not be attributed to direct collateral actions of SCT neurones. In some intracellularly recorded dorsal horn interneurones, short-latency EPSPs were evoked from the C3 segment by the 2nd or 3rd stimulus in the train, but not by single stimuli. In other dorsal horn and intermediate zone interneurones, inhibitory postsynaptic potentials (IPSPs) were evoked from the C3 segment at minimal latencies (2.7-3.2 ms), which might be too short to allow their mediation via SCT neurones. We conclude that SCT neurones might be used to forward information from muscle group II and cutaneous afferents not only to neurones in the lateral cervical nucleus and via them to thalamus and cerebral cortex but also to interneurones in spinal reflex pathways. Thereby reflex actions evoked from group II and cutaneous afferents might be co-ordinated with responses mediated by supraspinal neurones. We conclude also that dorsal horn and intermediate zone mid-lumbar interneurones might contribute to the previously reported di-and poly-synaptic excitation or inhibition of postsynaptic dorsal column (PSDC), spinothalamic tract (STT) and spinomesencephalic tract (SMT) neurones by collateral actions of SCT cells. Thereby these interneurones might contribute to the co-ordination of responses mediated by various populations of supraspinal neurones.

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PubMed1996

Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex.

1. Using dual intracellular recordings in slices of adult rat neocortex, twenty-four IPSPs activated by single presynaptic interneurones were studied in simultaneously recorded pyramidal cells. Fast spiking interneurones inhibited one in four or five of their close pyramidal neighbours. No reciprocal connections were observed. After recordings neurones were filled with biocytin. 2. Interneurones that elicited IPSPs were classified as classical fast spiking (n = 10), as non-classical fast spiking (n = 3, including one burst-firing interneurone), as unclassified, or slow interneurones (n = 8), or as regular spiking interneurones (n = 3), i.e. interneurones whose electrophysiological characteristics were indistinguishable from those of pyramidal cells. 3. All of the seven classical fast spiking cells anatomically fully recovered had aspiny, beaded dendrites. Their partially myelinated axons ramified extensively, varying widely in shape and extent, but randomly selected labelled axon terminals typically innervated somata and large calibre dendrites on electron microscopic examination. One 'autapse' was demonstrated. One presumptive regular spiking interneurone axon made four somatic and five dendritic connections with unlabelled targets. 4. Full anatomical reconstructions of labelled classical fast spiking interneurones and their postsynaptic pyramids (n = 5) demonstrated one to five boutons per connection. The two recorded IPSPs that were fully reconstructed morphologically (3 and 5 terminals) were, however, amongst the smallest recorded (< 0.4 mV). Some connections may therefore involve larger numbers of contacts. 5. Single axon IPSPs were between 0.2 and 3.5 mV in average amplitude at -55 to -60 mV. Extrapolated reversal potentials were between -70 and -82 mV. IPSP time course correlated with the type of presynaptic interneurone, but not with IPSP latency, amplitude, reversal potential, or sensitivity to current injected at the soma. 6. Classical fast spiking interneurones elicited the fastest IPSPs (width at half-amplitude 14.72 +/- 3.83 ms, n = 10) and unclassified, or slow interneurones the slowest (56.29 +/- 23.44 ms, n = 8). Regular spiking interneurone IPSPs had intermediate half-widths (27.3 +/- 3.68 ms, n = 3). 7. Increasingly brief presynaptic interspike intervals increased the peak amplitude of, but not the area under, the summed IPSP. Only at interspike intervals between 10 and 20 ms did IPSP integrals exhibit paired pulse facilitation. Paired pulse depression was apparent at < 10 and 20-60 ms. During longer spike trains, summing IPSPs decayed to a plateau potential that was relatively independent of firing rate (100-250 Hz). Thereafter, the voltage response could increase again. 8. Summed IPSPs elicited by two to fifteen presynaptic spike trains decayed as, or more rapidly than, single-spike IPSPs. Summed IPSPs elicited by > 20 spikes (> 150 Hz), however, resulted in an additional, more slowly decaying component (latency > 50 ms, duration > 200 ms). The possible involvement of GABAB receptors in this component is discussed. 9. It is suggested that three broad classes of interneurones may activate GABAA receptors on relatively proximal portions of neocortical pyramidal neurones. The different time courses of the IPSPs elicited by the three classes may reflect different types of postsynaptic receptor rather than dendritic location. An additional class, burst firing, spiny interneurones appear to activate GABAA receptors on more distal sites.

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