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PubMed1987

[Existence of respiratory interneurons in the cervical spinal cord of the rabbit].

A spinal "respiration" generator has been shown to fire phrenic motoneurones in rhythmic bursts. It is very likely driven through bulbo-spinal inspiratory neurones in intact preparations. Although no direct evidence for respiratory interneurones at the C4-C5 spinal levels has been obtained so far (except for Renshaw cells ), it is currently believed that only few inspiratory inputs to the phrenic motoneurones are transmitted monosynaptically from the medulla. We have tried here to record spinal interneuronal respiratory activities in decorticate, unanaesthetized, vagotomized and curarized rabbit preparations. Different functional categories of interneurones could be identified at the C4-C5 spinal levels: inspiratory and expiratory interneurons with various discharge patterns which rather well correspond to the functional categories of inspiratory and expiratory bulbo-spinal neurones described by Bianchi and Richter. In addition, multiunit inspiratory bursting could be followed over several 100 microns during each electrode penetration. The different categories of interneurones were encountered laterally from 700 to 1,000 microns, at depths ranging from 300 to 500 microns dorsally to the phrenic nucleus, down to the nucleus itself. These results indicate that part of the medullary inspiratory drive is channelled via spinal cord interneurones; they also suggest that an inhibition of phrenic motoneurones from the bulbo-spinal expiratory drive takes place via interneurones.

Animals↗

PubMed1988

Identification of motoneurons and interneurons in the spinal network for escapes initiated by the mauthner cell in goldfish.

We used intracellular recording and staining techniques to study the spinal circuitry of the escape behavior (C-start) initiated by the Mauthner axon (M-axon) in goldfish. Simultaneous intracellular recordings from one or both M-axons and a spinal neuron, followed by HRP labeling of the spinal cell, show that each M-axon makes monosynaptic, chemical excitatory synapses onto 2 populations of ipsilateral spinal neurons. The first consists of the large primary motoneurons that, based on earlier work (Fetcho, 1986), innervate exclusively the faster, white muscle fiber types in the myomeres. The second group of cells is formed by previously undescribed descending interneurons with ipsilateral axonal branches that have contacts with primary and secondary motoneurons spread over 2 or more body segments. Indirect evidence suggests that these descending interneurons are excitatory, and they may explain the polysynaptic activation of motoneurons observed in earlier studies of the spinal circuitry (Diamond, 1971). Both classes of neurons excited by the ipsilateral M-axon are disynaptically inhibited by the contralateral one. The morphology and physiology indicate that this inhibition is mediated by interneurons that are electrotonically coupled to one M-axon and have processes that cross the cord to inhibit contralateral neurons in the region where these postsynaptic cells receive excitatory input from the other M-axon. We have identified interneurons with the physiological and morphological features of these predicted crossed inhibitory interneurons. These cells are electrotonically coupled to the ipsilateral M-axon and receive a chloride-dependent disynaptic inhibitory input from the contralateral M-axon. Their very simple somata give rise to a process that crosses the spinal cord between the 2 M-axons. Once on the opposite side of the cord, the crossing process sends myelinated branches that run rostrally and caudally, roughly parallel to the contralateral M-axon. Processes that arise from these longitudinal branches terminate in a striking association with collaterals of the M-axon; nearly every M-axon collateral along the longitudinal course of an interneuron is met by a branch or branches of the interneuron whose terminals are apposed to neurons postsynaptic to the collateral.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

PubMed1986

Processing by local interneurons of mechanosensory signals involved in a leg reflex of the locust.

At the distal end of the tibia of a locust hind leg are 2 pairs of movable spurs that can be moved by contact with external objects--as, for example, when the body sways from side to side and loads one leg unevenly or when the foot is placed on rough ground--but not by direct muscular action. Movements imposed on a spur evoke phasic bursts of spikes in the axon of a single receptor cell at its base. If the displacement is maintained, however, the response adapts within a few seconds. The afferents from these spur receptors excite particular spiking local interneurons with cell bodies at the ventral midline of the metathoracic ganglion. Each afferent spike is consistently followed at a constant latency by a depolarizing potential in one of these interneurons. The potential can evoke a spike, and its amplitude is enhanced by a hyperpolarization applied to the interneuron. The central delay to this chemically mediated EPSP, which also includes conduction time to synaptic sites, probably indicates a direct connection. Some spiking local interneurons are excited by the 2 anterior spurs but are unaffected by the 2 posterior ones, while others receive the converse pattern of inputs. The receptive fields of these interneurons also include regions on either the anterior or posterior surfaces of the tibia with excitatory inputs from hair afferents. A reliable inhibitory reflex effect on the single levator tarsi is evoked by movement of any of the 4 spurs. The inhibitory potentials are not caused directly by the sensory afferents but involve the spiking local interneurons upon which the afferents synapse. The receptive field of this motor neuron therefore results from the convergence of inputs from a few interneurons. Motor neurons of other tarsal muscles are unaffected by movement of the spurs, but those of some more proximal muscles may be excited. These reflex effects should enhance the traction of the tarsus with the ground.

Afferent Pathways↗

PubMed1995

Hippocampal CA1 interneurons: an in vivo intracellular labeling study.

Fast spiking interneurons in the CA1 area of the dorsal hippocampus were recorded from and filled with biocytin in anesthetized rats. The full extent of their dendrites and axonal arborizations as well as their calcium binding protein content were examined. Based on the spatial extent of axon collaterals, local circuit cells (basket and O-LM neurons) and long-range cells (bistratified, trilaminar, and backprojection neurons) could be distinguished. Basket cells were immunoreactive for parvalbumin and their axon collaterals were confined to the pyramidal layer. A single basket cell contacted more than 1500 pyramidal neurons and 60 other parvalbumin-positive interneurons. Commissural stimulation directly discharged basket cells, followed by an early and late IPSPs, indicating interneuronal inhibition of basket cells. The dendrites of another local circuit neuron (O-LM) were confined to stratum oriens and it had a small but high-density axonal terminal field in stratum lacunosum-moleculare. The fastest firing cell of all interneurons was a calbindin-immunoreactive bistratified neuron with axonal targets in stratum oriens and radiatum. Two neurons with their cell bodies in the alveus innervated the CA3 region (backprojection cells), in addition to rich axon collaterals in the CA1 region. The trilaminar interneuron had axon collaterals in strata radiatum, oriens and pyramidale with its dendrites confined to stratum oriens. Commissural stimulation evoked an early EPSP-IPSP-late depolarizing potential sequence in this cell. All interneurons formed symmetric synapses with their targets at the electron microscopic level. These findings indicate that interneurons with distinct axonal targets have differential functions in shaping the physiological patterns of the CA1 network.

Animals↗

PubMed1995

Physiological and morphological heterogeneity of dentate gyrus-hilus interneurons in the gerbil hippocampus in vivo.

A variety of morphological types of dentate gyrus/hilus interneurons have been described, but little is known about their corresponding physiological characteristics. To address this issue, intracellular responses to current injection and perforant path stimulation were obtained from putative dentate interneurons in anaesthetized adult gerbils. Our sample of interneurons showed heterogeneity in their intrinsic physiological characteristics and spike thresholds to perforant path stimulation, suggesting the existence of distinct physiologically-defined classes. 'Fast-spiking' interneurons had a low threshold to perforant path stimulation, whereas 'slow-spiking' interneurons responded with predominantly inhibitory potentials. In several cases, cells were intracellularly labelled with biocytin for visualization. Interneurons with different physiological traits had distinct morphological features. These results confirm that, as in hippocampus proper, morphologically identifiable interneurons in the dentate hilus show electrophysiological features that are likely to reflect functionally specific roles in informational processing.

Animals↗

PubMed1995

Interneurons and inhibition in the dentate gyrus of the rat in vivo.

Inhibitory cells are critically involved in shaping normal hippocampal function and are thought to be important elements in the development of hippocampal pathologies. However, there is relatively little information about the extent and pattern of axonal arborization of hippocampal interneurons and, therefore, about the sphere of influence of these cells. What we do know about these cells is based largely on in vitro slice studies, in which interneuronal interactions may be severely attenuated. The present study was carried out to provide a more realistic picture of interneuron influence. Intracellular recordings were obtained from dentate interneurons in the intact brain of anesthetized rats, and cells were intracellularly labeled with biocytin. The axonal arbors of two classes of dentate interneurons were traced through the hippocampus; each was found to extend long distances (up to half of the total septotemporal length of the hippocampus) perpendicular to the hippocampal lamellae and to target preferential strata. These results suggest that dentate interneurons have far-reaching effects on target cells in distant hippocampal lamellae. One implication of this finding is that dentate neurons should receive more inhibitory synaptic drive in vivo than in slice preparations, in which many inhibitory axon collaterals are amputated. Synaptic responses to perforant path stimulation were examined in granule cells, mossy cells, and CA3 pyramidal cells in vivo, for comparison with previously published results from hippocampal slice studies. In vivo, all cell types showed excitatory synaptic responses that were brief and limited by robust IPSPs that were larger in amplitude and conductance than responses to comparable stimuli recorded in vitro. This difference could not be explained by a change in the intrinsic physiological properties of the cells in the slice preparation, because those parameters were similar in vivo and in vitro. We conclude that dentate gyrus inhibitory interneurons can affect the excitability of neurons in distant areas of the hippocampus, and that these distant influences cannot be appreciated in conventional in vitro preparations.

Animals↗

PubMed1994

[Electrophysiological characteristics of morphologically identified chandelier interneurons in rat hippocampal slices].

Using standard intracellular recording and staining techniques, 4 chandelier interneurons were sampled and anatomically confirmed from 39 physiologically identified interneurons in rat hippocampal slices. Compared to pyramidal and granule cells, all 4 chandelier interneurons-(CA1 region, n = 3, dentate gyrus, n = 1) had typical action potentials of interneurons, i. e., a shorter duration of action potential was followed by a deep after hyperpolarization. However, all these 4 cells exhibited a varying degree of spike frequency adaptation in response to depolarizing current injection, which usually do not occur in basket interneurons. Morphologically, axonal terminals of chandelier cells were beaded and exclusively distributed in the stratum oriens of the CA1 and the granule cell layer of the dentate gyrus, where the initial segments of pyramidal and granule cells are located. These results indicate that the chandelier interneurons differ from basket interneurons in the rat hippocampus with in physiology and in morphology.

Action Potentials↗

PubMed1994

Analysis of the feeding motor pattern in the pond snail, Lymnaea stagnalis: photoinactivation of axonally stained pattern-generating interneurons.

We have photoinactivated identified feeding interneurons known as N1 and N2 neurons. These are pattern-generating neurons that are active in the protraction of the radula and rasping phases, respectively, of the feeding cycle of the pond snail. The N1 or N2 feeding interneurons in the buccal ganglia were filled with the fluorescent dye 5(6)-carboxyfluorescein (5-CF) from the cut end of the nerve that contains their axon. Filling the cerebrobuccal connective (N = 151) stained just one N1 cell in the contralateral buccal ganglion. Filling the postbuccal nerve stained neurons symmetrically in both buccal ganglia (N = 75): only one labeled cell in each ganglion is an N2 interneuron. The feeding rhythm was evoked by depolarizing a modulatory neuron, the SO, located in the buccal ganglia. The axonally filled N1 interneuron was irradiated at its axon in the buccal commissure with blue laser light (intensity of 0.5 MW.m-2). Irradiation of just one N1 completely blocked the feeding rhythm (seven preparations). In seven further preparations, N1 ablation slowed the SO-driven feeding rhythm and weakened the N1 input to the feeding neurons. Irradiation of the cell bodies of both the filled left and right N2 interneurons killed the cells but did not produce any consistent change in the feeding rate (15 preparations). The feeding interneurons and motoneurons still showed the characteristic N2 phase synaptic inputs, so more, as yet unidentified, N2 neurons must be located in other parts of the buccal ganglia. We conclude that the participation of the identified N1 interneurons is essential for the normal feeding pattern while other, still to be identified N2 neurons must be present and must contribute to the feeding rhythm. We suggest that the extra redundancy of the N2 network may be related to the greater necessity of sensory feedback control during rasping than during protraction of the radula.

Animals↗

PubMed1993

Alpha-bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression.

The nicotinic cholinergic antagonist alpha-bungarotoxin (alpha-BT) binds throughout the rat hippocampal formation. The binding is displaceable by d-tubocurarine. The most heavily labeled cells are GABA-containing interneurons in the dentate and in Ammon's horn. These neurons have several different morphologies and contain several neuropeptides. alpha-BT-labeled interneurons in the dentate are small cells between the granular and molecular layers that often contain neuropeptide Y. alpha-BT-labeled interneurons in CA1 are medium-sized interneurons, occasionally found in stratum pyramidale, but more often found in stratum radiatum and stratum lacunosum moleculare. These neurons often contain cholecystokinin. The largest alpha-BT-labeled interneurons are found in CA3, in both stratum radiatum and stratum lucidum. These neurons are multipolar and frequently are autofluorescent. They often contain somatostatin or cholecystokinin. These large interneurons have been found to receive medial septal innervation and may also have projections that provide inhibitory feedback directly to the medial septal nucleus. The cholinergic innervation of the hippocampus from the medial septal nucleus is under the trophic regulation of NGF and brain-derived neurotrophic factor, even in adult life. Expression of mRNA for both these factors is increased in CA3 and the dentate after intraventricular administration of alpha-BT, but not after administration of the muscarinic antagonist atropine. alpha-BT-sensitive cholinergic receptors on inhibitory interneurons may be critical to medial septal regulation of the hippocampal activity, including the habituation of response to sensory input.

Animals↗

PubMed1993

Functional uncoupling of inhibitory interneurons plays an important role in short-term sensitization of Aplysia gill and siphon withdrawal reflex.

Attempts to explain learning-associated potentiation of synaptic transmission in model systems such as withdrawal reflexes in the mollusk Aplysia or the hippocampus of vertebrates have focused on the mechanisms by which transmitter release is increased in the principal elements of the circuit. Increased transmission in neuronal networks such as the gill and siphon withdrawal reflex (GSWR) of Aplysia may, however, also be caused by a decrease of transmitter release by inhibitory interneurons. The importance and function of cholinergic inhibitory transmission in the GSWR network were investigated. Central application of the nicotinic cholinergic antagonist d-tubocurarine (d-TC) considerably potentiated gill contractions, evoked either by nerve stimulation or by tactile stimulation of the siphon. Compound EPSPs evoked in motoneurons upon siphon nerve stimulation were also significantly prolonged following application of d-TC, but were unaffected by hexamethonium, a blocker of excitatory ACh receptors in Aplysia. Recordings from excitatory interneurons showed that they received excitation followed by powerful inhibitory input upon stimulation of the siphon nerve. Application of d-TC completely blocked this rapid inhibition, thus prolonging the compound EPSPs evoked in the interneurons. These effects were obtained at a concentration of d-TC (100 microM) that almost totally blocked fast inhibitory cholinergic transmission, but was without effect on monosynaptic connections between sensory neurons and motoneurons of the reflex. Facilitation of (1) compound EPSCs in motoneurons and (2) evoked excitatory interneuronal firing was reduced in preparations already disinhibited by pretreatment with d-TC. Facilitation of sensory-motor synapses, however, was not reduced in the presence of d-TC, indicating that facilitatory interneurons are still activated under cholinergic blockade. These data show that transmission through the GSWR neuronal network is gated by a feedback inhibitory mechanism. They also suggest that a reduction of cholinergic inhibition onto excitatory interneurons may be a mechanism through which transmission within the GSWR network is increased during various forms of learning, such as sensitization. These data place new emphasis on the important role of inhibitory interneurons in determining the plastic properties of neuronal networks, in both invertebrates and vertebrates.

Acetylcholine↗

PubMed1995

Physiological and morphological heterogeneity of dentate gyrus-hilus interneurons in the gerbil hippocampus in vivo.

Action Potentials↗

PubMed1997

Evoked excitability changes at the terminals of midlumbar premotor interneurons in the cat spinal cord.

We present evidence that the electrical excitability of the terminals of a group of spinal premotor interneurons can be increased after stimulation of sensory afferents. The interneurons were located in the midlumbar segments of the spinal cord and had projections to the lower lumbar motor nuclei. Thresholds for antidromic activation of a substantial number of interneurons were reduced after electrical stimulation of group II muscle afferents. Several observations suggest that the excitability changes are unlikely to have arisen from electrotonic spread of depolarization from the interneuron soma to its terminals or by environmental changes in the vicinity of the terminals related to neuronal activity. A particularly interesting possibility is that the excitability of the central terminals of the interneurons is increased because they are depolarized by a mechanism similar to that acting at the terminals of primary sensory afferents (primary afferent depolarization, PAD), which accompanies one type of presynaptic inhibition. This type of presynaptic action has been shown in premotor interneurons in the lamprey but not in the mammalian spinal cord. From our observations the organization of the systems generating excitability changes at the interneuron terminals seem in general to parallel the organization of the systems generating PAD at afferent terminals, raising the possibility that common principles might underlie the operation of this form of presynaptic control.

Animals↗

PubMed1997

Inhibitory control of GABAergic interneurons in the hippocampus.

Hippocampal GABAergic interneurons are responsible for controlling the output and efficacy of synaptic input of large principal cell populations and, thereby, determine the oscillatory discharge patterns and synaptic plasticity in the hippocampus. Single interneurons are able to prevent repetitive firing of postsynaptic pyramidal cells (R. Miles, K. Tóth, A.I. Gulyás, N. Hájos, and T.F. Freund. Neuron, 16: 815-823, 1996), whereas on occasion a single pyramidal cell may be able to activate an interneuron under in vitro conditions (A.I. Gulyás, R. Miles, A. Sik, K. Tóth, N. Tamamaki, and T.F. Freund. Nature (London), 366: 683-687, 1993). Inhibition is therefore extremely powerful. Transient suppression of interneuronal activity allows the precise timing and synchronization of inhibitory postsynaptic potentials arriving at principal cells. A rhythmic suppression or modulation of interneuron discharge may be brought about by input from at least two major sources: (i) from other local interneurons or (ii) from subcortical centers. Of the possible local sources, in the present review particular attention will be paid to GABAergic neurons specialized to innervate other interneurons. Subcortical pathways known to modulate specific inhibitory functions in the hippocampus, i.e., the GABAergic and cholinergic septohippocampal and the serotonergic raphe hippocampal pathways, will also be reviewed. Roles of these control mechanisms may include the generation of theta and higher frequency oscillations and the selective removal of inhibition from the termination zone of specific excitatory afferents, thereby increasing their efficacy and (or) plasticity.

Acetylcholine↗

PubMed1998

Characterization of tactile-sensitive interneurons in the abdominal ganglia of the cockroach, Periplaneta americana.

Tactile stimulation of an insect's abdomen evokes various behaviors including grooming and vigorous escape responses. We tested a sample of 37 tactile-sensitive abdominal interneurons for various morphological and physiological characteristics, including their ability to excite thoracic interneurons that are known to integrate wind information conducted by giant interneurons in the classical escape response. The results suggest that abdominal tactile-sensitive interneurons are heterogeneous both in anatomical and physiological properties. In general, these cells are very small interganglionic interneurons that respond to tactile stimulation at more than one abdominal segment. However, the larger population contained virtually all types of cells. Some projected anteriorly, others posteriorly, and still others projected in both directions. For most cells, the soma was on the side opposite to their axons, but in 24% of the cells it was on the same side. Patterns of dendritic arbors also varied among cells. However, tactile sensitivity was in general consistent with the morphological bias noted in dendritic branch patterns. We were able to document the existence of tactile abdominal interneurons that connect directly to thoracic interneurons involved in escape (TI[A]s). However, instances of demonstrated connectivity were rare. One cell that did show connectivity (AI652) was characterized in detail, and its properties were appropriate for conducting tactile signals in a directional escape system. The dendritic arbors were biased to the side that was ipsilateral to the cell's soma and axon. As a result, this cell's abdominal inputs and thoracic outputs are on the same side. This pattern is appropriate for generating the sensory fields recorded previously in TI(A)s. Its axon was located in the ventral median tract, which should bring it close to the integrating region of the TI(A)s.

Abdomen↗

PubMed1999

Opioid receptor subtype expression defines morphologically distinct classes of hippocampal interneurons.

The inhibition of hippocampal pyramidal cells occurs via inhibitory interneurons making GABAergic synapses on distinct segments of the postsynaptic membrane. In area CA1 of the hippocampus, the activation of mu- and delta-opioid receptors inhibits these interneurons, thereby increasing the excitability of the pyramidal cells. Through the use of selective opioid agonists and biocytin-filled whole-cell electrodes, interneurons possessing somata located within stratum oriens of hippocampal slices were classified according to the location of their primary axon termination and the expression of mu- or delta-opioid receptors. Activation of these opioid receptor subtypes resulted in outward currents in the majority of interneurons, which is consistent with their inhibition. Post hoc morphological analysis revealed that those interneurons heavily innervating the pyramidal cell body layer were much more likely to express mu-opioid receptors, whereas cells with axons ramifying in the pyramidal neuron dendritic layers were more likely to express delta-opioid receptors, as defined by the generation of outward currents. This morphological segregation of interneuron projections suggests that mu receptor activation would diminish GABA release onto pyramidal neuron somata, thereby increasing their excitability and output. Conversely, inhibition of interneurons via delta receptor activation would amplify afferent signaling to pyramidal neuron dendrites by reducing GABAergic inhibition of these structures.

Animals↗

PubMed2000

Zebrafish evx1 is dynamically expressed during embryogenesis in subsets of interneurones, posterior gut and urogenital system.

The even-skipped-related homeobox genes (evx) are widely distributed through animal kingdom and are thought to play key role in posterior body patterning and neurogenesis. We have cloned and analyzed the expression of evx1 in zebrafish (see also Borday et al. (Dev. Dyn. 220 (2001) in press) which displays a dynamic and restricted expression pattern during neurogenesis. In spinal cord, rhombencephalon, and epiphysis, evx1 is expressed in several subsets of emerging interneurones prior to their axonal outgrowth, identified as primary interneurones and a subset of Pax2.1(+) commissural interneurones. In the hindbrain, evx1 is expressed in reticulospinal interneurones of rhombomeres 5 and 6 as well as in rhombomere 7 interneurones. The latest emerging evx1(+) interneurones in the hindbrain correspond to commissural interneurones. evx1 is also dynamically transcribed during the formation of the posterior gut and the uro-genital system in mesenchymal cells that border the pronephric ducts, the wall of the pronephric duct, and later in the posterior gut and the wall of the uro-genital opening. In larvae, the ano-rectal epithelium and the muscular layer that surrounds the analia-genitalia region remain stained up to 27 days. In contrast other vertebrates, evx1displays no early nor caudal expression in zebrafish.

Amino Acid Sequence↗

PubMed2003

Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations.

Electrical coupling between pyramidal cell axons, and between interneuron dendrites, have both been described in the hippocampus. What are the functional roles of the two types of coupling? Interneuron gap junctions enhance synchrony of gamma oscillations (25-70 Hz) in isolated interneuron networks and also in networks containing both interneurons and principal cells, as shown in mice with a knockout of the neuronal (primarily interneuronal) connexin36. We have recently shown that pharmacological gap junction blockade abolishes kainate-induced gamma oscillations in connexin36 knockout mice; without such gap junction blockade, gamma oscillations do occur in the knockout mice, albeit at reduced power compared with wild-type mice. As interneuronal dendritic electrical coupling is almost absent in the knockout mice, these pharmacological data indicate a role of axonal electrical coupling in generating the gamma oscillations. We construct a network model of an experimental gamma oscillation, known to be regulated by both types of electrical coupling. In our model, axonal electrical coupling is required for the gamma oscillation to occur at all; interneuron dendritic gap junctions exert a modulatory effect.

Animals↗

PubMed1997

Local interneurons define functionally distinct regions within lobster olfactory glomeruli

Whole-cell recording coupled with biocytin injection revealed four types of interneurons intrinsic to the olfactory lobe (OL) of the spiny lobster Panulirus argus. Each type of neuron had a distinct pattern of arborization within the three anatomically defined regions of OL glomeruli (cap, subcap and base). Type I interneurons innervated all three regions, while types II, III and IV branched only in the cap, subcap and base, respectively. Type I interneurons responded to electrical stimulation of the antennular (olfactory) nerve with a burst of 120 action potentials and a 110 s depolarization. Type II (cap) interneurons responded to the same input with a burst of 13 action potentials followed by a shorter hyperpolarization. Type III (subcap) interneurons responded with a burst of 16 action potentials followed by a delayed, 0.54 s depolarization. Type IV (base) interneurons responded with a brief depolarization or a burst of 13 action potentials followed by a 1 s hyperpolarization. The regionalized arborization and the different response properties of the type II, III and IV interneurons strongly imply that lobster olfactory glomeruli contain functionally distinct regions, a feature that should be useful in understanding the multiple synaptic pathways involved in processing olfactory input.

Journal Article↗