Synaptic mechanisms of spike generation in bursts by neurons of the carp tectum and olfactory bulb

Synaptic mechanisms of burst activity generation in certain neurons of the tectum opticum and mechanisms of generation of stimulation-induced group discharges by certain secondary neurons of the olfactory bulb were analyzed in carp (Cyprinus carpio L.). Spikes of the spontaneous discharge in neurons of the tectum were accompanied by depolarizing after-potentials, which caused the burst discharges of these cells. Evidence is given in support of the synaptic nature of the after-potential; it is suggested that it is generated by a recurrent collateral mechanism. Synaptic bombardment causing the appearance of a group discharge in olfactory bulb neurons and groups of spikes in their spontaneous activity was found to be intermittent in character. These features of unit activity in the olfactory bulb are shown to be connected with the presence of excitatory synaptic interaction between several neurons, probably dendro-dendritic in nature.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiay, Vol. 14, No. 5, pp. 483–490, September–October, 1982.     

Electrical characteristics of granule cells of the carp olfactory bulb

Intracellular responses of granule cells and secondary neurons of the carp olfactory bulb to electrical stimulation of the olfactory nerve and olfactory tract were investigated. Synaptic responses of granule cells to both types of stimuli consisted of an early and late EPSP and IPSP. Comparison of responses of the secondary and granule neurons indicated that the granule cells are interneurons of postsynaptic inhibition of secondary neurons. The results suggest that dendro-dendritic and recurrent collateral pathways exist for the activation of granule cells and that inhibitory synapses are located on those dendrites of the secondary neurons that are in contact with endings of olfactory nerve fibers.M. V. Lomonosov State University, Moscow. Translated from Neirofiziologiya, Vol. 7, No. 6, pp. 597–602, November–December, 1975.     

Inhibition in the fish olfactory bulb

Inhibition in the olfactory bulb of the carp was studied by recording potentials from secondary neurons intracellularly. Three types of inhibition — trace, early, and late — can arise in neurons of the olfactory bulb. Trace inhibition corresponds to hyperpolarization about 20 msec in duration, which is closely connected with the spike, but it is not after-hyperpolarization but an IPSP. Early and late inhibition correspond to IPSPs of different parameters. The first has a latency of 0–50 msec (relative to the spike) and a duration of 60–400 msec; the corresponding values for the second are 100–400 msec and 0.5–3 sec. The possible mechanisms of these types of inhibition are discussed.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 3, No. 6, pp. 650–656, November–December, 1971.     

Complex action potentials of secondary neurons of the rat olfactory bulb

Complex action potentials arising spontaneously or evoked by stimulation of the lateral olfactory tract in secondary neurons of the rat olfactory bulb were recorded. The amplitude and duration of the complex potentials varied depending on synchronization of onset of the individual components (of which more than four were distinguished) and their combination. It is suggested that complex potentials were recorded in cases when the electrode was located in the region of the junction between spike-generating zones (the branching node of the dendrite, the junction of the soma with the dendrites and axon). It is concluded that there are numerous generating zones in the dendrites of the secondary olfactory neurons. Evoked action potentials appeared after the following latent periods: first, about 1 msec; second, about 2 msec; and third, about 3 msec. The results of the analysis showed that the antidromic response appeared after the shortest latent period. These results are evidence of the existence of considerable and varied representation of excitatory synapses in secondary neurons (besides the excitatory input in the olfactory glomeruli).M. B. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 8, No. 6, pp. 575–582, November–December, 1976.     

Electrotonic interaction between secondary neurons of the carp olfactory bulb

Responses of secondary neurons of the carp olfactory bulb evoked by electrical stimulation of the olfactory tract were investigated by intracellular recording. In most neurons spike responses were identified as antidromic. Their latent periods varied from 2.5 to 55 msec. Two other types of responses of secondary neurons had constant latent periods: the pseudo-antidromic spike and a fast low-amplitude depolarization potential. It is concluded that these responses are generated by the antidromic spike of a neighboring neuron, connected electrotonically with the recorded neuron.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 8, No. 5, pp. 490–496, September–October, 1976.     

Generation of spike activity by dendrites of secondary neurons of the rat olfactory bulb

Experiments on secondary neurons of the rat olfactory bulb showed the existence of a third region of action potential generation. It evidently consists of dendrites. This is shown by the distance from the soma of the point where action potentials arise initially and by the recording of spontaneous action potentials of comparatively low amplitude, not spreading into the axon. Action potentials are generated by apical dendrites and also, perhaps, by basal dendrites. Besides partial action potentials with stable amplitude, partial action potentials with, for practical purposes, a stepwise changing amplitude also were recorded. It is suggested that the amplitude of the partial action potentials is modified by IPSPs in the spike-generating zones.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 8, No. 3, pp. 282–290, May–June, 1976.     

Morphology and physiology of multiglomerular olfactory projection neurons in the spiny lobster

Whole-cell patch-clamp recording was used to characterize olfactory projection neurons in an isolated brain preparation of the spiny lobster, Panulirus argus. Responses to electrical stimulation of the olfactory afferents were recorded from projection neuron somata using biocytin-filled electrodes. All projection neurons were multiglomerular, innervating up to 80% of all olfactory lobe glomeruli, but the innervation was heterogeneous. Most neurons densely innervated only 3–4 glomeruli; the remaining glomeruli in their dendritic arbor were sparsely innervated, thereby creating two distinct patterns of intraglomerular branching. Projection neurons responded to orthodromic stimulation with an initial depolarization and spiking followed by a 1–3 s hyperpolarization. The inhibitory phase of the response was lower in threshold and longer in latency than the excitatory phase, a response pattern also reported in olfactory projection neurons of insects and vertebrates. The somata of the projection neurons supported voltage-activated currents and TTX-sensitive action potentials, suggesting that the soma, although spatially separated from the axon and dendrites, may play a significant functional role in these cells. Dye coupling between some projection neurons correlated with the presence of multiple amplitude action potentials, suggesting that at least some projection neurons may be coupled via gap junctions.     

Guidepost neurons for the lateral olfactory tract: Expression of metabotropic glutamate receptor 1 and innervation by glutamatergic olfactory bulb axons

The guidepost neurons for the lateral olfactory tract, which are called lot cells, are the earliest‐generated neurons in the neocortex. They migrate tangentially and ventrally further down this tract, and provide scaffolding for the olfactory bulb axons projecting into this pathway. The molecular profiles of the lot cells are largely uncharacterized. We found that lot cells specifically express metabotropic glutamate receptor subtype‐1 at a very early stage of development. This receptor is functionally competent and responds to a metabotropic glutamate receptor agonist with a transient increase in the intracellular calcium ion concentration. When the glutamatergic olfactory bulb axons were electrically stimulated, lot cells responded to the stimulation with a calcium increase mainly via ionotropic glutamate receptors, suggesting potential neurotransmission between the axons and lot cells during early development. Together with the finding that lot cells themselves are glutamatergic excitatory neurons, our results provide another notable example of precocious interactions between the projecting axons and their intermediate targets. © 2012 Wiley Periodicals, Inc. Develop Neurobiol, 2012     

The alarm reaction in crucian carp is mediated by olfactory neurons with long dendrites

In the present study, we applied a lipophilic tracer, Dil (1,1-dilinoleyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate), to the synaptic region of the medial olfactory bulb in formaldehyde-fixed preparations from the crucian carp. We observed staining both in the axons of secondary neurons leading to the brain and in the olfactory receptor neurons (ORNs) of the olfactory epithelium. In those preparations, where staining of the tract was restricted to axons of the medial part of the medial olfactory tract, the majority (86-98%) of the somata of the sensory neurons were found in the deep layers of olfactory epithelium. Since the medial bundle of the medial olfactory tract mediates alarm behaviour in the crucian carp, we conclude that the sensory neurons with long dendrites participate in the reception of alarm pheromones.     

Hyperpolarization-activated and cyclic nucleotide-gated channels are differentially expressed in juxtaglomerular cells in the olfactory bulb of mice

In the olfactory bulb, input from olfactory receptor neurons is processed by neuronal networks before it is relayed to higher brain regions. In many neurons, hyperpolarization-activated and cyclic nucleotide-gated (HCN) channels generate and control oscillations of the membrane potential. Oscillations also appear crucial for information processing in the olfactory bulb. Four channel isoforms exist (HCN1–HCN4) that can form homo- or heteromers. Here, we describe the expression pattern of HCN isoforms in the olfactory bulb of mice by using a novel and comprehensive set of antibodies against all four isoforms. HCN isoforms are abundantly expressed in the olfactory bulb. HCN channels can be detected in most cell populations identified by commonly used marker antibodies. The combination of staining with marker and HCN antibodies has revealed at least 17 different staining patterns in juxtaglomerular cells. Furthermore, HCN isoforms give rise to an unexpected wealth of co-expression patterns but are rarely expressed in the same combination and at the same level in two given cell populations. Therefore, heteromeric HCN channels may exist in several cell populations in vivo. Our results suggest that HCN channels play an important role in olfactory information processing. The staining patterns are consistent with the possibility that both homomeric and heteromeric HCN channels are involved in oscillations of the membrane potential of juxtaglomerular cells.     

Investigation of habituation reaction of neurons of the cat motor cortex

The neuronal and total surface activity of the cortical representation of the motor analyzer in the region of the posterior sigmoid gyrus of the cat brain in response to rhythmical light, sound, and electrical stimuli and their complexes was analyzed. Two groups of neurons were found, of which the first is characterized by a gradual decrease in the number of peaks in the response and by their subsequent disappearance and the second by the absence of a discharge in response to stimulation and by its development before the application of the next stimulus. The first group was comprised of neurons which do not have background activity and the second was made up of neurons with a background activity of 0.4–3.7 imp/sec. This reorganization of the activity of cortical neurons in response to rhythmical stimulation is considered to be a habituation phenomenon.A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 3, No. 3, pp. 245–251, May–June, 1971.     

Integral evoked potentials and single unit activity in the frog olfactory bulb

Integral evoked potentials and intracellular potentials of single units were recorded from the frog olfactory bulb in response to afferent stimulation by two methods: electrical stimulation of the olfactory nerve and natural stimulation with odorous substances. At least four components can be distinguished in the response of the olfactory bulb to single electrical stimulation: an integral action potential of the olfactory nerve fibers, a synaptic glomerular potential, and two polysynaptic components. Responses of mitral and superficial (interglomerular) bulb cells to orthodromic electrical stimulation and antidromic stimulation of the olfactory tract are described. A functional similarity between the mitral cells of frogs and the analogous cells of rabbits is noted. Responses of the bulb to stimulation of olfactory receptors by odorous substances are characterized by regular waves of potentials. Corresponding waves of postsynaptic potentials are observed in the interglomerular cells of the bulb. These latter must, therefore, participate in generation of the rhythmic response. During stimulation by odorous substances, prolonged PSPs, producing excitation or inhibition of the spike discharge, arise in various cells of the bulb. The results of component analysis of the integral response and the functional properties of single bulb units are discussed.Institute of Problems of Information Transmission, Academy of Sciences of the USSR, Moscow; Institute of Biology of Internal Waters, Academy of Sciences of the USSR, Borok, Yaroslavl'Region. Translated from Neirofiziologiya, Vol. 1, No. 3, pp. 269–277, November–December, 1969.     

Glomerulus development in the absence of a set of mitral-like neurons in the insect olfactory lobe

Mitral cells are the first neurons in the mammalian olfactory bulb to synapse with olfactory receptor axons during glomerulus development, and in an invertebrate, the moth Manduca sexta, mitral-like neurons overlap very early with olfactory receptor axons as they begin to form protoglomeruli. The possibility for early interaction between receptor neurons and mitral-like neurons led us to ask whether such an interaction plays an essential role in glomerulus development. In the current study in the moth, we surgically removed a major class of these mitral-like neurons before glomeruli began to form and asked: (a) Is the formation of the array of olfactory glomeruli triggered by an interaction of the first-arriving receptor axons with the dendrites of mitral-like neurons? (b) At the level of individual glomeruli, must the mitral-like dendrites be in place either to maintain receptor axons in a glomerular arrangement, or to guide later-growing dendrites of other types into the developing glomeruli? Our results indicate that even without the participation of this group of mitral-like neurons, the array of sexually isomorphic ordinary glomeruli forms and the basic substructure of individual glomeruli develops apparently normally. We conclude that the mitral-like neurons in Manduca are not essential for the formation of ordinary olfactory glomeruli during development. © 1998 John Wiley & Sons, Inc. J Neurobiol 36: 41–52, 1998     

Responses of cortical neurons to local application of excitatory amino acids to their dendrites and soma

The efficacy of excitation induced by iontophoretic application of excitatory amino acids to the soma or different parts of the dendritic tree has been compared in experiments performed on parietal cortex slices. Spike activity was recorded extracellularly from single nerve cells of layer V. In total, the responses of 125 neurons were analyzed. Upon application of glutamate and aspartate to the neuronal soma and the majority of dendrites, latencies of excitatory responses did not exceed 500 msec. In 18% of cases, neuronal responses to transmitter application to basal and apical dendrites had longer (2–3 sec) latencies. The maximum intensity of responses was observed when excitatory amino acids had been applied to the soma or proximal parts of dendrites. If applied at a distance of over 100 µm to basal and 300 µm to apical dendrites, glutamate and aspartate elicited cellular responses whose intensity was 2–3 times lower than that of the responses induced by application to the soma. The maximum distances at which somatic spike responses could be recorded were 350 µm and 800 µm for basal and apical dendrites, respectively. Different latencies of the responses to somatic and dendritic applications of excitatory amino acids in some neurons, as well as high efficacy of responses to stimulation of remote parts of dendritic tree, may indicate nonidentity of electrical properties of dendritic and somatic membranes.Neirofiziologiya/Neurophysiology, Vol. 25, No. 6, pp. 437–446, November–December, 1993.     

The sox gene Dichaete is expressed in local interneurons and functions in development of the Drosophila adult olfactory circuit

In insects, the primary sites of integration for olfactory sensory input are the glomeruli in the antennal lobes. Here, axons of olfactory receptor neurons synapse with dendrites of the projection neurons that relay olfactory input to higher brain centers, such as the mushroom bodies and lateral horn. Interactions between olfactory receptor neurons and projection neurons are modulated by excitatory and inhibitory input from a group of local interneurons. While significant insight has been gleaned into the differentiation of olfactory receptor and projection neurons, much less is known about the development and function of the local interneurons. We have found that Dichaete, a conserved Sox HMG box gene, is strongly expressed in a cluster of LAAL cells located adjacent to each antennal lobe in the adult brain. Within these clusters, Dichaete protein expression is detected in both cholinergic and GABAergic local interneurons. In contrast, Dichaete expression is not detected in mature or developing projection neurons, or developing olfactory receptor neurons. Analysis of novel viable Dichaete mutant alleles revealed misrouting of specific projection neuron dendrites and axons, and alterations in glomeruli organization. These results suggest noncell autonomous functions of Dichaete in projection neuron differentiation as well as a potential role for Dichaete‐expressing local interneurons in development of the adult olfactory circuitry. © 2012 Wiley Periodicals, Inc. Develop Neurobiol, 2013     

The source of spontaneous activity in the main olfactory bulb of the rat

Introduction

In vivo, most neurons in the main olfactory bulb exhibit robust spontaneous activity. This paper tests the hypothesis that spontaneous activity in olfactory receptor neurons drives much of the spontaneous activity in mitral and tufted cells via excitatory synapses.

Methods

Single units were recorded in vivo from the main olfactory bulb of a rat before, during, and after application of lidocaine to the olfactory nerve. The effect of lidocaine on the conduction of action potentials from the olfactory epithelium to the olfactory bulb was assessed by electrically stimulating the olfactory nerve rostral to the application site and monitoring the field potential evoked in the bulb.

Results

Lidocaine caused a significant decrease in the amplitude of the olfactory nerve evoked field potential that was recorded in the olfactory bulb. By contrast, the lidocaine block did not significantly alter the spontaneous activity of single units in the bulb, nor did it alter the field potential evoked by electrical stimulation of the lateral olfactory tract. Lidocaine block also did not change the temporal patters of action potential or their synchronization with respiration.

Conclusions

Spontaneous activity in neurons of the main olfactory bulb is not driven mainly by activity in olfactory receptor neurons despite the extensive convergence onto mitral and tufted cells. These results suggest that spontaneous activity of mitral and tufted is either an inherent property of these cells or is driven by centrifugal inputs to the bulb.     

Postsynaptic excitation and in hibition in neurons of the turtle general cortex in response to moving stimuli

Responses of the general cortex to moving stimuli were studied in turtles. The evoked potential, the synaptic nature of its individual components, and the mechanisms of their generation were analyzed. The evoked potential had a negative-positive sequence. The negative part consisted of a slow negative wave on which fast negative complexes were superposed. These components reflected EPSPs of afferent nature generated on dendrites of the principal neurons. The first fast negative complex was followed by a rhythmic discharge superposed on the slow negative and positve waves. The negative waves of the rhythmic discharge were shown to reflect EPSPs and the positive waves IPSPs, probably generated on dendrites of cortical neurons. The rhythmic EPSP — IPSPs are evidently generated by a feedback mechanism, whereas the positive wave reflects dendritic IPSPs of the principal neurons.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 9, No. 3, pp. 249–256, May–June, 1977.     

A Circadian Clock in the Olfactory Bulb Anticipates Feeding during Food Anticipatory Activity

Rabbit pups ingest food, in this case milk, once a day with circadian periodicity and are a natural model of food anticipatory activity. During nursing, several sensory systems receive information about properties of the food, one of them being the olfactory system, which has received little attention in relation to synchronization by food. In addition, the olfactory bulb has a circadian pacemaker that exhibits rhythms independently of the suprachiasmatic nucleus, but the biological functions of these rhythms are largely unknown. In the present contribution, we hypothesized that circadian suckling of milk synchronizes rhythms in the olfactory bulb. To this aim we explored by immunohistochemistry, rhythms of FOS and PER1 proteins, as indicators of activation and reporter of oscillations, respectively, through a complete 24-h cycle in periglomerular, mitral and granular cell layers of both the main and the accessory olfactory bulb. Subjects were 7-day-old rabbit pups scheduled to nurse during the night (02∶00 h) or day (10∶00 h), and also fasted subjects, to explore the possible persistence of oscillations. In the three layers of the main olfactory bulb, FOS was high at time of nursing, then further increased 1.5 h afterward, and then decreased to increase again in advance of the next nursing bout. This pattern persisted, without the postprandial increase, in fasted subjects with a shift in subjects nursed at 02∶00. PER1 was increased 2–8 h after nursing and this increase persisted in most cell layers, with a shift, in fasted subjects. In the accessory olfactory bulb we only observed a consistent pattern of FOS expression in the mitral cell layer of nursed subjects, similar to that of the main olfactory bulb. We conclude that the main olfactory bulb is synchronized during milk ingestion, but during fasting its oscillations perhaps are modulated by the suprachiasmatic nucleus, as proposed for rodents.     

Glutamate spillover mediates excitatory transmission in the rat olfactory bulb.

In the CNS, glutamate typically mediates excitatory transmission via local actions at synaptic contacts. In the olfactory bulb, mitral cell dendrites release glutamate at synapses formed only onto the dendrites of inhibitory granule cells. Here, I show excitatory transmission mediated solely by transmitter spillover between mitral cells in olfactory bulb slices. Dendritic glutamate release from individual mitral cells causes self-excitation via local activation of N-methyl-D-aspartate (NMDA) receptors. Paired recordings reveal that glutamate release from one cell generates NMDA receptor-mediated responses in neighboring mitral cells that are enhanced by blockade of glutamate uptake. Furthermore, spillover generates spontaneous NMDA receptor-mediated population responses. This simultaneous activation of neighboring mitral cells by a diffuse action of glutamate provides a mechanism for synchronizing olfactory principal cells.