Most olfactory receptor neurons (ORNs) express a single type of olfactory receptor that is differentially sensitive to a wide variety of odorant molecules. The diversity of possible odorant-receptor interactions raises challenging problems for the coding of complex mixtures of many odorants, which make up the vast majority of real world odors. Pure competition, the simplest kind of interaction, arises when two or more agonists can bind to the main receptor site, which triggers receptor activation, although only one can be bound at a time. Noncompetitive effects may result from various mechanisms, including agonist binding to another site, which modifies the receptor properties at the main binding site. Here, we investigated the electrophysiological responses of rat ORNs in vivo to odorant agonists and their binary mixtures and interpreted them in the framework of a quantitative model of competitive interaction between odorants. We found that this model accounts for all concentration-response curves obtained with single odorants and for about half of those obtained with binary mixtures. In the other half, the shifts of curves along the concentration axis and the changes of maximal responses with respect to model predictions, indicate that noncompetitive interactions occur and can modulate olfactory receptors. We conclude that, because of their high frequency, the noncompetitive interactions play a major role in the neural coding of natural odorant mixtures. This finding implies that the CNS activity caused by mixtures will not be easily analyzed into components, and that mixture responses will be difficult to generalize across concentration.
Taste receptors play a crucial role in detecting the presence of bitter compounds such as alkaloids, and help to prevent the ingestion of toxic food. In Drosophila, we show for the first time that several taste sensilla on the prothoracic legs detect bitter compounds both through the activation of specific taste neurons but also through inhibition of taste neurons activated by sugars and water. Each sensillum usually houses a cluster of four taste neurons classified according to their best stimulus (S for sugar, W for Water, L1 and L2 for salts). Using a new statistical approach based on the analysis of interspike intervals, we show that bitter compounds activate the L2 cell. Bitter-activated L2 cells were excited with a latency of at least 50 ms. Their sensitivity to bitter compounds was different between sensilla, suggesting that specific receptors to bitter compounds are differentially expressed among L2 cells. When presented in mixtures, bitter compounds inhibited the responses of S and W, but not the L1 cell. The inhibition was effective even in sensilla where bitter compounds did not activate the L2 cell, indicating that bitter compounds directly interact with the S and W cells. Interestingly, this inhibition occurred with latencies similar to the excitation of bitter-activated L2 cells. It suggests that the inhibition in the W and S cells shares similar transduction pathways with the excitation in the L2 cells. Combined with molecular approaches, the results presented here should provide a physiological basis to understand how bitter compounds are detected and discriminated.
Antennal lobes of adult male and female Manduca sexta were compared in order to investigate the nature and extent of sexual dimorphism of the primary olfactory center of this lepidopteran species. Complete identification of the glomeruli led to the conclusion that all female glomeruli have homologous male counterparts. Thus, there is no sex-specific glomerulus present in one sex and absent in the other. Sexual dimorphism (i.e. glomeruli present but morphologically different in males and females), however, does occur in the three glomeruli composing the male macroglomerular complex. The female homologs of this complex consist of two previously identified 'large female glomeruli' and one newly identified normal-sized glomerulus. The lateral and medial large female glomeruli are interpreted to be homologous to the first two macroglomerular-complex glomeruli-the cumulus and toroid 1. The third male component, the toroid 2, was tentatively identified with a normal-sized spheroidal glomerulus of the female, called here the 'small female glomerulus'. The 60 'ordinary' glomeruli that make up the rest of the glomerular neuropil were found to be homologous in males and females, with the exception of two anomalous (or uncertain) glomeruli. Some variations in relative position and size observed among those glomeruli suggest a diffuse, quantitative kind of sexual dimorphism.
The glomerular organization of the antennal lobes was analyzed in the moth Mamestra brassicae and comparatively in the butterfly Pieris brassicae. The invariance of the lobes in number, position, and size of the glomeruli was verified quantitatively in the moth for all the glomeruli in individuals of the same sex (67 in males, 68 in females) and for 56 sex-invariant glomeruli which can be identified in all individuals whatever their sex. In the butterfly, the positional variability is greater than in the moth and hinders identification. The most conspicuous sex-variant glomeruli are two adjoining macroglomeruli in the male moth which have homologs of very small size in the female. No such dimorphism was observed in Pieris, a species in which males are attracted to female by visual stimuli and not by a sex pheromone as in Mamestra. There are other sex-variant glomeruli in Mamestra: four varying in location, three subdivided in the female, two found only in the male, and three found only in the female. Consequently, differing olfactory sensitivity related to species and sex could correlate with detectable modifications in the glomerular organization. A hypothesis on the function of glomeruli is discussed in which most of the glomeruli are viewed as "olfactory generalists" giving rise collectively to proposed "across-glomeruli patterns."
The spiking activity of receptor neurons was recorded extracellularly in the frog olfactory epithelium in response to four odourants applied at precisely controlled concentrations. A set of criteria was formulated to define the spikes in the response. Four variables - latency, duration, number of interspike intervals and frequency - were determined to quantify the responses. They were studied at the single neuron, neuron population and ciliary membrane levels. The dose-response curves were determined using specific functions and their characteristics were evaluated. The characteristic molar concentrations at threshold or at maximum duration and the characteristics of variables, e.g. minimum latency or maximum frequency, have asymmetric histograms with peaks close to the origin and long tails. Dynamic ranges have even more asymmetric histograms, so that a significant fraction of neurons presents a much wider range than their one-decade peak. From these histograms, response properties of the whole neuron population can be inferred. In general, location along the concentration axis (thresholds), width (dynamic ranges) and heights of dose-response curves are independent, which explains the diversity of curves, prevents their global categorization and supports the qualitative coding of odourants. No evidence for odourant-independent types of neurons was found. Finally, receptor activation and ciliary membrane conductance were reconstructed in the framework of a model based on firing data, known mucus biochemical and neuron morpho-electrical characteristics. It is in agreement with independent determinations of Kd of odourant-receptor interaction and of conductance characteristics, and describes their statistical distributions in the neuron population.
Computer-assisted neuroanatomical methods have been used to demonstrate unique identities of the glomeruli of the antennal lobes (ALs) in males of the sphinx moth Manduca sexta. The glomerular neuropil consists of the male-specific macroglomerular complex, which comprises two closely apposed bulky subunits, and 64 +/- 1 "ordinary" glomeruli arrayed in a shell around a central region of coarse neuropil. Computer-generated maps show the exact locations of all glomeruli and adjacent groups of neuronal somata in a constant Cartesian coordinate system, such that these can be accurately identified in any individual. The glomeruli belong to three classes according to the number and type of identification criteria they satisfy. The larger class comprises glomeruli (n = 44) identified only in the computer-generated maps on the basis of their relative positions. The other two classes include glomeruli that were also identified in sections, either directly from their proximity to readily identifiable structures and their shape and size (n = 10, including the labial-palp-pit-organ (LPO) glomerulus), or indirectly from their positions relative to the former (n = 9). Two very small glomeruli were present in only one AL, demonstrating the existence of anomalous glomeruli, whereas another glomerulus had no homologue in both ALs of one individual. The true number of ordinary glomeruli (per male AL) was thus estimated to be 64. The uncertainty in delineating some glomeruli might affect this number without implying modification of the homologies proposed. The locations of tracts and cell groups, both within and near the AL, are also invariant with respect to glomeruli, as shown in the computer maps. The methods employed are general and might be useful to researchers in related fields. The results obtained call for more attention to the precise geometry of neural structures.
A biophysical model of receptor potential generation in the male moth olfactory receptor neuron is presented. It takes into account all pre-effector processes—the translocation of pheromone molecules from air to sensillum lymph, their deactivation and interaction with the receptors, and the G-protein and effector enzyme activation—and focuses on the main post-effector processes. These processes involve the production and degradation of second messengers (IP3 and DAG), the opening and closing of a series of ionic channels (IP3-gated Ca2+ channel, DAG-gated cationic channel, Ca2+-gated Cl− channel, and Ca2+- and voltage-gated K+ channel), and Ca2+ extrusion mechanisms. The whole network is regulated by modulators (protein kinase C and Ca2+-calmodulin) that exert feedback inhibition on the effector and channels. The evolution in time of these linked chemical species and currents and the resulting membrane potentials in response to single pulse stimulation of various intensities were simulated. The unknown parameter values were fitted by comparison to the amplitude and temporal characteristics (rising and falling times) of the experimentally measured receptor potential at various pheromone doses. The model obtained captures the main features of the dose–response curves: the wide dynamic range of six decades with the same amplitudes as the experimental data, the short rising time, and the long falling time. It also reproduces the second messenger kinetics. It suggests that the two main types of depolarizing ionic channels play different roles at low and high pheromone concentrations; the DAG-gated cationic channel plays the major role for depolarization at low concentrations, and the Ca2+-gated Cl− channel plays the major role for depolarization at middle and high concentrations. Several testable predictions are proposed, and future developments are discussed.
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