Spontaneous activity of first- and second-order neurons in the frog olfactory system (original) (raw)
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Origins of correlated spiking in the mammalian olfactory bulb
Mitral/tufted (M/T) cells of the main olfactory bulb transmit odorant information to higher brain structures. The relative timing of action potentials across M/T cells has been proposed to encode this information and to be critical for the activation of downstream neurons. Using ensemble recordings from the mouse olfactory bulb in vivo, we measured how correlations between cells are shaped by stimulus (odor) identity, common respiratory drive, and other cells’ activity. The shared respiration cycle is the largest source of corre- lated firing, but even after accounting for all observable factors a residual positive noise correlation was observed. Noise correlation was maximal on a ∼100-ms timescale and was seen only in cells separated by <200 μm. This correlation is explained primarily by common activity in groups of nearby cells. Thus, M/T-cell correlation principally reflects respiratory modulation and sparse, local network connectivity, with odor identity accounting for a minor component.
Circuit Properties Generating Gamma Oscillations in a Network Model of the Olfactory Bulb
Journal of Neurophysiology, 2005
Bathellier, Brice, Samuel Lagier, Philippe Faure, and Pierre-Marie Lledo. Circuit properties generating gamma oscillations in a network model of the olfactory bulb. . The study of the neural basis of olfaction is important both for understanding the sense of smell and for understanding the mechanisms of neural computation. In the olfactory bulb (OB), the spatial patterning of both sensory inputs and synaptic interactions is crucial for processing odor information, although this patterning alone is not sufficient. Recent studies have suggested that representations of odor may already be distributed and dynamic in the first olfactory relay. The growing evidence demonstrating a functional role for the temporal structure of bulbar neuronal activity supports this assumption. However, the detailed mechanisms underlying this temporal structure have never been thoroughly studied. Our study focused on gamma (40 -100 Hz) network oscillations in the mammalian OB, which is a form of temporal patterning in bulbar activity elicited by olfactory stimuli. We used computational modeling combined with electrophysiological recordings to investigate the basic synaptic organization necessary and sufficient to generate sustained gamma rhythms. We found that features of gamma oscillations obtained in vitro were identical to those of a model based on lateral inhibition as the coupling modality (i.e., low irregular firing rate and high oscillation stability). In contrast, they differed substantially from those of a model based on lateral excitatory coupling (i.e., high regular firing rate and instable oscillations). Therefore we could precisely tune the oscillation frequency by changing the kinetics of inhibitory events supporting the lateral inhibition. Moreover, gradually decreasing GABAergic synaptic transmission decreased the degree of relay neuron synchronization in response to sensory inputs, both theoretically and experimentally. Thus we have shown that lateral inhibition provides a mechanism by which the dynamic processing of odor information might be finely tuned within the OB circuit. * B. Bathellier a nd S. Lagier contributed equally to this work. Address for reprint requests and other correspondence: P.-M. Lledo, Laboratory of Perception and Memory, CNRS URA 2182, 25 rue du Dr. Roux,
Burst firing versus synchrony in a gap junction connected olfactory bulb mitral cell network model
Frontiers in Computational Neuroscience, 2012
A key player in olfactory processing is the olfactory bulb (OB) mitral cell (MC). We have used dual whole-cell patch-clamp recordings from the apical dendrite and cell soma of MCs to develop a passive compartmental model based on detailed morphological reconstructions of the same cells. Matching the model to traces recorded in experiments we find: C m = 1.91 ± 0.20 μF cm −2 , R m = 3547 ± 1934 cm 2 and R i = 173 ± 99 cm. We have constructed a six MC gap-junction (GJ) network model of morphologically accurate MCs. These passive parameters (PPs) were then incorporated into the model with Na + , Kdr, and KA conductances and GJs from Migliore et al. (2005). The GJs were placed in the apical dendrite tuft (ADT) and their conductance adjusted to give a coupling ratio between MCs consistent with experimental findings (∼0.04). Firing at ∼50 Hz was induced in all six MCs with continuous current injections (0.05-0.07 nA) at 20 locations to the ADT of two of the MCs. It was found that MCs in the network synchronized better when they shared identical PPs rather than using their own PPs for the fit suggesting that the OB may have populations of MCs tuned for synchrony. The addition of calcium-activated potassium channels (iKCa) and L-type calcium channels (iCa(L)) (Bhalla and Bower, 1993) to the model enabled MCs to generate burst firing. However, the GJ coupling was no longer sufficient to synchronize firing. When cells were stimulated by a continuous current injection there was an initial period of asynchronous burst firing followed after ∼120 ms by synchronous repetitive firing. This occurred as intracellular calcium fell due to reduced iCa(L) activity. The kinetics of one of the iCa(L) gate variables, which had a long activation time constant (τ ∼ range 18-150 ms), was responsible for this fall in iCa(L). The model makes predictions about the nature of the kinetics of the calcium current that will need experimental verification.
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2017
Rhythmic neuronal activity of multiple frequency bands has been described in many brain areas and attributed to numerous brain functions. Among these, little is known about the mechanism and role of infra-slow oscillations, which have been demonstrated recently in the mouse accessory olfactory bulb (AOB). Along with prolonged responses to stimuli and distinct network connectivity, they inexplicably affect the AOB processing of social relevant stimuli. Here, we show that assemblies of AOB mitral cells are synchronized by lateral interactions through chemical and electrical synapses. Using a network model, we demonstrate that the synchronous oscillations in these assemblies emerge from interplay between intrinsic membrane properties and network connectivity. As a consequence, the AOB network topology, in which each mitral cell receives input from multiple glomeruli, enables integration of chemosensory stimuli over extended time scales by interglomerular synchrony of infra-slow burstin...
Dynamics of Input Patterns Modulate the Behavior of a Model of Olfactory Bulb Function
Journal of Neurophysiology, 2009
Input patterns to the olfactory bulb are dynamic and change in an odor-specific manner as measured by selective calcium imaging of olfactory bulb input. To our knowledge, none of the published models of olfactory bulb function uses dynamic input patterns. Therefore we tested how dynamic input alters the behavior of a simple model consisting of two layers. The membrane potential of the first-layer neurons, integrate-and-fire neurons corresponding to mitral cells, was modulated with a subthreshold oscillation at respiration frequency. The membrane potential of the second-layer neurons was used to discriminate input patterns. We implemented oscillating input with amplitudes and latencies different for each mitral cell. Not only varying the input amplitudes but also de-synchronizing the input, and varying the relation between latency and input amplitude, individually changed the model's performance significantly. The discrimination time was affected more easily than the number of se...
Responses of single neurons and neuronal ensembles in frog first- and second-order olfactory neurons
Brain Research, 2013
A major challenge in sensory neuroscience is to elucidate the coding and processing of stimulus representations in successive populations of neurons. Here we recorded the spiking activity of receptor neurons (RNs) and mitral/tufted cells (MCs) in the frog olfactory epithelium and olfactory bulb respectively, in response to four odorants applied at precisely controlled concentrations. We compared how RN responses are translated in MCs. We examined the time course of the instantaneous firing frequency before and after stimulation in neuron ensembles and the dependency on odorant concentration of the number of action potentials fired in a preselected 5-s time window (dose-response curves) in both single neurons and neuron ensembles. In RNs and MCs, the dose-response curves typically increase then decrease and are well described by alpha functions. We established the main quantitative properties of these curves, including the distributions of concentrations at threshold and maximum responses. We showed that the main transformations occurring in the transition from RNs to MCs is the lowering of the firing threshold and a large decrease in the total number of spikes fired. We also found that the number of action potentials fired by recorded neurons and hence their energy consumption is independent of odorant concentration, and that this is a consequence of their time-and concentrationdependent activities.
2020
In the vertebrate olfactory bulb (OB), axonless granule cells (GC) mediate self- and lateral inhibitory interactions between mitral/tufted cells via reciprocal dendrodendritic synapses. Locally triggered release of GABA from the large reciprocal GC spines occurs on both fast and slow time scales, possibly enabling parallel processing during olfactory perception. Here we investigate local mechanisms for asynchronous spine output.To reveal the temporal and spatial characteristics of postsynaptic ion transients, we imaged spine and adjacent dendrite Ca2+- and Na+-signals with minimal exogenous buffering by the respective fluorescent indicator dyes upon two-photon uncaging of DNI-glutamate in OB slices from juvenile rats. Both postsynaptic fluorescence signals decayed slowly, with average half durations in the spine head of t1/2_Δ[Ca2+]i ~500 ms and t1/2_Δ[Na+]i ~1000 ms. We also analysed the kinetics of already existing data of postsynaptic spine Ca2+-signals in response to glomerular ...
Characterization of the Synaptic Properties of Olfactory Bulb Projections
Chemical Senses, 2004
The olfactory bulb directly projects to several diverse telencephalic structures, but, to date, few studies have investigated the physiological characteristics of most of these areas. As an initial step towards understanding the odor processing functions of these secondary olfactory structures, we recorded evoked field potentials in response to lateral olfactory tract stimulation in vivo in urethane-anesthetized Sprague-Dawley rats in the following brain structures: anterior olfactory nucleus, ventral and dorsal tenia tecta, olfactory tubercle, anterior and posterior piriform cortex, the anterior cortical nucleus of the amygdala, and lateral entorhinal cortex. Using paired-pulse stimulation with interpulse intervals of 25-1000 ms, we observed facilitation of the response to the second pulse in every structure examined, although the degree of facilitation varied among the target structures. Additionally, pulse train stimulation at three different frequencies (40, 10 and 2 Hz) produced facilitation of evoked field potentials that also varied among target structures. We discuss the potential utility of such short-term facilitation in olfactory processing.
Coincidence Detection within the Excitable Rat Olfactory Bulb Granule Cell Spines
The Journal of Neuroscience, 2019
In the mammalian olfactory bulb, the inhibitory axonless granule cells (GCs) feature reciprocal synapses that interconnect them with the principal neurons of the bulb, mitral, and tufted cells. These synapses are located within large excitable spines that can generate local action potentials (APs) upon synaptic input ("spine spike"). Moreover, GCs can fire global APs that propagate throughout the dendrite. Strikingly, local postsynaptic Ca 2ϩ entry summates mostly linearly with Ca 2ϩ entry due to coincident global APs generated by glomerular stimulation, although some underlying conductances should be inactivated. We investigated this phenomenon by constructing a compartmental GC model to simulate the pairing of local and global signals as a function of their temporal separation ⌬t. These simulations yield strongly sublinear summation of spine Ca 2ϩ entry for the case of perfect coincidence ⌬t ϭ 0 ms. Summation efficiency (SE) sharply rises for both positive and negative ⌬t. The SE reduction for coincident signals depends on the presence of voltage-gated Na ϩ channels in the spine head, while NMDARs are not essential. We experimentally validated the simulated SE in slices of juvenile rat brain (both sexes) by pairing two-photon uncaging of glutamate at spines and APs evoked by somatic current injection at various intervals ⌬t while imaging spine Ca 2ϩ signals. Finally, the latencies of synaptically evoked global APs and EPSPs were found to correspond to ⌬t Ϸ 10 ms, explaining the observed approximately linear summation of synaptic local and global signals. Our results provide additional evidence for the existence of the GC spine spike.
Interneurons in the olfactory bulb are key elements of odor processing but their roles have not yet being fully understood. Two types of inhibitory interneurons, periglomerular and granule cells, act at two different levels within the olfactory bulb and may have different roles in coordinating the spiking of mitral cells, which are the principal output neurons of the olfactory bulb. In this work we introduce a reduced compartmental model of the periglomerular cell and use it to investigate its role on mitral cell spiking in a model of an elementary cell triad composed of these two cell types plus a granule cell. Our simulation results show that the periglomerular cell is more effective in inhibiting the mitral cell than the granule cell. Based on our results we predict that periglomerular and granule cells have different roles in the control of mitral cell spiking. The periglomerular cell would be the only one capable of completely inhibiting the mitral cell, and the activity decrease of the mitral cell through this inhibitory action would occur in a stepwise fashion depending on parameters of the periglomerular and granule cells as well as on the relative times of arrival of external stimuli to the three cells. The major role of the granule cell would be to facilitate the inhibitory action of the periglomerular cell by enlarging the range of parameters of the periglomerular cell which correspond to complete inhibition of the mitral cell. The combined action of the two interneurons would thus provide an efficient way of controling the instantaneous value of the firing rate of the mitral cell.