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.     

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.     

Rhythmic activity of the olfactory bulb of the carp under nembutal anesthesia

The effect of nembutal intraperitoneal injections upon the induced waves and orthodromic potentials of the olfactory bulb (OB) induced by odor stimulation and paired electric stimuli of the olfactory nerve was examined in immobilized by diplacine carp (cyprinus carpio L.). The nembutal anesthesia resulted in a gradual decrease in frequency of induced waves tested by orthodromic response and amplitude of spontaneous electric activity ob OB. The changes found under nembutal anesthesia in evoked electric activity of OB were also observed in chronic and acute intersection of the olfactory tracts.     

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.     

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.     

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.     

Pharmacological analysis of slow potentials recorded in forg olfactory bulb during natural stimulation

Pharmacological agents (strychnine, picrotoxin, pentobarbital, chloralose, GABA, penicillin, morphine) were used to investigate the nature of the slow potential recorded in the frog olfactory bulb in response to natural stimulation. Three possible hypotheses were tested: 1) The slow potential is neuroglial in nature; 2) it is the analog of the dorsal-root potential of the spinal cord and reflects depolarization of primary afferents arising in the terminals of the olfactory nerve and responsible for presynaptic inhibition in the frog olfactory bulb; 3) the slow potential reflects postsynaptic processes. The results showed great similarity between changes in the slow and dorsal-root potentials of the spinal cord in response to the action of pharmacological agents. However, the slow potential is evidently a complex response and incorporates at least one other component — depolarization of the dendrites of unknown nature.     

An in vitro study of long-term potentiation in the carp (Cyprinus carpio L.) olfactory bulb

Long-term potentiation (LTP) of synaptic transmission is considered a cellular mechanism for neural plasticity and memory formation. Previously, we showed that in the carp olfactory bulb, LTP occurs at the dendrodendritic mitral-to-granule cell synapse following tetanic electrical stimulation applied to the olfactory tract, and suggested that it is involved in the process of olfactory memory formation. As a first step towards understanding mechanisms underlying plasticity at this synapse, we examined the effects of various drugs (glutamate and GABA receptor agonists and antagonists, noradrenaline, and drugs affecting cAMP signaling) on dendrodendritic mitral-to-granule cell synaptic transmission in an in vitro preparation. Two forms of LTP are involved: a postsynaptic form (tetanus-evoked LTP) and a presynaptic form. The postsynaptic form is evoked at the granule cell dendrite following tetanic olfactory tract stimulation and is suppressed by the NMDA receptor antagonist, D-AP5, enhanced by noradrenaline, and occluded by the metabotropic glutamate receptor agonist, trans-ACPD. The presynaptic form occurs at the mitral cell dendrite following blockade of the GABA_A receptor by picrotoxin and bicuculline, or via activation of cAMP signaling by forskolin and 8-Br-cAMP.     

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.     

Electrical signaling in the olfactory bulb

The olfactory bulb employs lateral and feedback inhibitory pathways to distribute odor information across parallel assemblies of mitral and granule cells. The pathways involve dendritic action potentials that can interact with a variety of voltage-dependent conductances and synaptic transmission to produce complex and dynamic patterns of activity. Electrical coupling also helps to ensure proper coordination and synchronization of these patterns. These mechanisms provide numerous options for dynamic modulation and control of signaling in the olfactory bulb.     

Gender distinction in neural discrimination of sex pheromones in the olfactory bulb of crucian carp, Carassius carassius

Studies on projection of the sensory neurons onto the olfactory bulb in fish have revealed a clear subdivision into spatially different areas that each responded specifically to different classes of odorants. Amino acids induce activity in the lateral part, bile salts induce activity in the medial part, and alarm substances induce activity in the posterior part of the medial olfactory bulb. In the present study, we demonstrate a new feature of the bulbar chemotopy showing that neurons specifically sensitive to sex pheromones are located in a central part of the ventral olfactory bulb in crucian carp. Extensive single-unit recordings were made from these neurons, stimulating with four sex pheromones, 17,20beta-dihydroxy-4-pregnen-3-one, 17,20beta-dihydroxy-4-pregnen-3-one-20-sulfate, androstenedione, and prostaglandin F(2alpha), known to induce specific reproductive behaviors in males of carp fish. All substances were applied separately to the sensory epithelium at a concentration of 10(-9) M. Of the 297 neurons recorded in males, the majority (236 or 79.5%) responded exclusively to one of the four sex pheromones and thus showed a high specificity. Of the 96 neurons recorded from the olfactory bulb in females, only 1 unit showed such a specific activation. These findings reflect remarkable differences between males and females in the discriminatory power of the olfactory neurons toward these sex pheromones. The gender differences are discussed in relation to behavior studies, expression of olfactory receptors, and the convergence of sensory neurons onto the secondary neurons in the olfactory bulb.     

Axon mis-targeting in the olfactory bulb during regeneration of olfactory neuroepithelium

During development, primary olfactory axons typically grow to their topographically correct target zone without extensive remodelling. Similarly, in adults, new axons arising from the normal turnover of sensory neurons essentially project to their target without error. In the present study we have examined axon targeting in the olfactory pathway following extensive chemical ablation of the olfactory neuroepithelium in the P2-tau:LacZ line of mice. These mice express LacZ in the P2 subpopulation of primary olfactory neurons whose axons target topographically fixed glomeruli on the medial and lateral surfaces of the olfactory bulb. Intraperitoneal injections of dichlobenil selectively destroyed the sensory neuroepithelium of the nasal cavity without direct physical insult to the olfactory neuron pathway. Primary olfactory neurons regenerated and LacZ staining revealed the trajectory of the P2 axons. Rather than project solely to their topographically appropriate glomeruli, the regenerating P2 axons now terminated in numerous inappropriate glomeruli which were widely dispersed over the olfactory bulb. While these errors in targeting were refined over time, there was still considerable mis-targeting after four months of regeneration.     

Inhibition in the olfactory bulb of the lizard

Inhibition in neurons of the lizard olfactory bulb was investigated by intracellular recording. The hyperpolarization arising in the neurons after the spike in the response to orthodromic and antidromic activation is similar in composition and reflects the development of early and late IPSPs, differing from one another in latency, duration, and mechanism of generation. The early IPSP is evidently generated by the functioning of dendrodendritic synapses, formed by dendrites of the interglomerular cell on the membrane of the apical dendrites of the secondary neurons, whereas synapses generating the late IPSP are located on the basal dendrites and are formed by endings of the granular cells. The mechanisms of generation of the early and late IPSPs in the secondary neurons are discussed. A classification of neurons of the lizard olfactory bulb is given on the basis of analysis of their intracellular activity.     

Connectivity and dynamics in the olfactory bulb

Dendrodendritic interactions between excitatory mitral cells and inhibitory granule cells in the olfactory bulb create a dense interaction network, reorganizing sensory representations of odors and, consequently, perception. Large-scale computational models are needed for revealing how the collective behavior of this network emerges from its global architecture. We propose an approach where we summarize anatomical information through dendritic geometry and density distributions which we use to calculate the connection probability between mitral and granule cells, while capturing activity patterns of each cell type in the neural dynamical systems theory of Izhikevich. In this way, we generate an efficient, anatomically and physiologically realistic large-scale model of the olfactory bulb network. Our model reproduces known connectivity between sister vs. non-sister mitral cells; measured patterns of lateral inhibition; and theta, beta, and gamma oscillations. The model in turn predicts testable relationships between network structure and several functional properties, including lateral inhibition, odor pattern decorrelation, and LFP oscillation frequency. We use the model to explore the influence of cortex on the olfactory bulb, demonstrating possible mechanisms by which cortical feedback to mitral cells or granule cells can influence bulbar activity, as well as how neurogenesis can improve bulbar decorrelation without requiring cell death. Our methodology provides a tractable tool for other researchers.