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C D Derby

Publications and source records attributed to C D Derby.

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Responses of olfactory receptor cells of spiny lobsters to binary mixtures. II. Pattern mixture interactions.

1. The effect of mixture interactions in individual olfactory receptor cells of the spiny lobster on neural coding of odorant quality of binary mixtures and their components is examined in this paper. Extracellular responses of 98 olfactory receptor cells in the antennules of spiny lobsters to seven compounds [adenosine-5'-monophosphate (AMP), betaine (Bet), L-cysteine (Cys), L-glutamate (Glu), ammonium chloride (NH4), DL-succinate (Suc), taurine (Tau)] and their binary mixtures were recorded, and mixture interactions in individual olfactory receptor cells were identified. 2. Coding of odorant quality was evaluated by examining across neuron patterns (ANPs)--the relative response magnitudes across neuronal populations. ANPs are a feature of the neuronal population response and are a possible concentration-independent code of odorant quality in this system, as indicated by previous studies and present results. 3. For most binary mixtures the diversity of types and degrees of mixture interactions across the individual cells of a population of cells resulted in ANPs for each mixture to be different from the ANPs for the components of the mixture and different from the ANP predicted for the mixture from the responses to the components (Figs. 2-10). These effects are called pattern mixture interactions (PMIs). PMIs occurred for most binary mixtures, even those that did not produce statistically significant intensity mixture interactions (IMIs) for this same population of cells. 4. The results suggest that PMIs can influence coding of stimulus quality, in some cases by causing an improvement of the contrast between the quality of mixtures and some of their components.

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Peripheral mechanisms of olfactory discrimination of complex mixtures by the spiny lobster: no cell types for mixtures but different contributions of the cells to the across neuron patterns.

Toward understanding mechanisms of olfactory discrimination, we have examined the existence of cell types and the role of cells in the coding of odorant quality in the olfactory organ of the spiny lobster. The results consisted of responses of 30 antennular chemoreceptor cells to 8 behaviorally discriminable complex stimuli--4 natural extracts and 4 artificial mixtures, each at 3 concentrations. Multidimensional scaling and cluster analysis failed to identify unequivocal cell types, but rather suggested a continuum of cellular response profiles. The lack of cell types suggests that the code for the quality of natural odorants in this system is a population code. The distribution of cells along the response continuum was based on any of many features of their response profiles. The most effective stimulus (= best stimulus) and the least effective stimulus (= least stimulus), two features of the response profiles, could only partially explain the differences in response profiles of cells. Nonetheless, cells with different response profiles were shown to have different functions in odorant coding. Most cells contribute to some degree to the discrimination of any two stimuli, but a cell's contribution to the discrimination of two stimuli is usually disproportionally robust when those two stimuli produce very different responses in that cell.

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Independent components of the neural population response for discrimination of quality and intensity of chemical stimuli.

The responses of a population of 30 olfactory receptor cells from spiny lobsters to 8 behaviorally relevant complex types of stimuli at 0.005, 0.05 and 0.5 mM were analyzed using multidimensional scaling to evaluate their potential for coding quality and intensity. A discrimination index was derived from the resulting stimulus coordinates, which takes into account the response similarities within type/concentration and the response dissimilarities between types/concentrations. The results indicate that quality and intensity can be discriminated by separate components of the response of the population of neurons: quality by the pattern of responses produced across the neuronal population, and intensity by the absolute response magnitude.

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Morphological and physiological characterization of individual olfactory interneurons connecting the brain and eyestalk ganglia of the crayfish.

1. In order to understand the functional organization of the crustacean olfactory system, we are using intracellular recording and staining techniques to correlate the structure and function of single, odorant-sensitive interneurons in the brain of the crayfish Procambarus clarkii. We describe here the anatomy and physiology of interneurons that connect the brain with the medullae terminales or other eyestalk ganglia. 2. All of the interneurons in our study are at least third-order olfactory neurons (second-order olfactory interneurons) because they respond to chemostimulation of the olfactory organ (the antennules) but do not branch in the olfactory lobe (the neuropil to which primary olfactory receptor cells of the antennules project). 3. Much of the central nervous system, including the three main divisions of the brain (protocerebrum, deuterocerebrum, tritocerebrum) and the medullae terminales, are involved in integrating olfactory or multimodal (including olfactory) information, since these areas contain neurites of olfactory interneurons. Previous studies have indicated that regions involved in such processing include the olfactory lobes and accessory lobes of the deuterocerebrum, and regions I, II, IV, and VII (in some species) of the medullae terminales. Our results show that also prominent among regions involved in olfactory or multimodal (including olfactory) integration are the anterior and posterior optic neuropils of the protocerebrum, the lateral and medial antennular neuropils of the deuterocerebrum, the tegumentary neuropils and the antennal neuropils of the tritocerebrum, and neuropils III, VI, XII of the medullae terminales. 4. These olfactory interneurons were sensitive to chemostimulation (unimodal), chemo- and mechanostimulation (bimodal), or chemo-, mechano-, and photostimulation (trimodal). Responses could be excitatory or inhibitory, even for a given neuron. Morphologically complex interneurons (those having bilateral branching) were more likely to have complex response characteristics (trimodal sensitivity) than were morphologically simpler interneurons (those having unilateral branching). Olfactory interneurons with a soma in the medulla terminalis showed the most complex response profiles: they were trimodal, and were exicted by odorants but were inhibited by touch and/or light. This finding suggests that these are complex, high order interneurons. 5. Our studies reveal that olfactory and other sensory information is transmitted between the brain and the medullae terminales (and possibly other eyestalk ganglia) by a coactivated, parallel array of structurally and functionally diverse neurons.

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Physiology of chemoreceptor cells in the legs of the freshwater prawn, Macrobrachium rosenbergii.

1. Chemoreceptor cells in the first pereiopods (legs) of the freshwater prawn, Macrobrachium rosenbergii, were investigated using single-unit, extracellular electrophysiological recording techniques on an isolated, perfused leg preparation. 2. The cells were responsive to aqueous extracts of food (shrimp, mullet, trout chow), a salt mixture (artificial sea-water), amino acids (L-arginine HCl, taurine), a quaternary ammonium compound (betaine HCl) and ammonium chloride. 3. The response specificity of individual cells ranged from narrow to broad, but on average was broad, being more similar to chemoreceptor cells of freshwater crayfish than of marine spiny or clawed lobsters. 4. Responses were generally excitatory. However, some responses were inhibitory, the first such demonstration in aquatic crustaceans. 5. These electrophysiological results highly correlate with results of feeding behavioral assays carried out on M. rosenbergii.

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Differential associative conditioning and olfactory discrimination in the spiny lobster Panulirus argus.

A differential aversive associative conditioning paradigm was used to assess the ability of the spiny lobster Panulirus argus both to associatively learn not to respond to the odorant stimulus to which it was conditioned and to discriminate between odorants. The paradigm consisted of pairing an aversive stimulus (pseudopredator) with a conditioned chemical stimulus (shrimp mixture). Four artificial mixtures (crab, mullet, oyster, and shrimp), each at 0.05 and 0.5 mM, were presented to the animals prior to, during, and following conditioning to both concentrations of the shrimp mixture. Pre- vs postconditioning changes in three types of behavioral responses (and an index based on a composite of these three behaviors) were used as indicators of learned aversions. Olfactory discrimination abilities were determined by comparing the aversion to the conditioned mixture with the aversions to the three nonconditioned mixtures. A high degree of associative learning was attained after 10 pairings of the pseudopredator with the shrimp mixture over a period of 5 test days. According to the aversion index, animals conditioned to shrimp mixture perceived crab mixture as being more similar to shrimp mixture than were mullet and oyster mixtures, but all three nonconditioned mixtures were perceived as being significantly different from the shrimp mixture. These results are in concordance with results of a cluster analysis based on the mixture compositions, which indicates that shrimp and crab mixtures are compositionally similar, while mullet and oyster mixtures are compositionally distinct from the shrimp mixture.

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Neural coding of quality of complex olfactory stimuli in lobsters.

1. Extracellular responses to complex biologically relevant stimuli were recorded from 30 primary olfactory cells from excised antennules of spiny lobsters. The stimulus types were natural extracts of crab, mullet, oyster, and shrimp and artificial mixtures of crab, mullet, oyster and shrimp based on the chemical composition of the related extracts. All stimulus types were presented at the following three concentrations: 0.005, 0.05, and 0.5 mM. 2. The responses were expressed as number of spikes per 5 s. Response magnitude increased significantly as a function of concentration. It was significantly greater for the natural extracts than for the related artificial mixtures but was not significantly different among stimulus types within either natural extracts or artificial mixtures. 3. The cells were broadly tuned to all stimuli. Tuning slightly, but significantly, broadened as a function of stimulus concentration. 4. Multidimensional scaling (MDS) was used to evaluate similarities and dissimilarities among stimuli based on population responses. The artificial mixtures and the natural extracts were analyzed separately. Dimensionality of spatial configuration was based on the following three criteria: stress values, squared correlation values, and relevance to quality coding. 5. When applied to the original data, MDS distributed the stimuli in a two-dimensional space where the location of each stimulus was based mainly on stimulus concentration. The results of a simple standardization procedure showed that this distribution resulted mostly from the significant effect of concentration on one of the two features of population responses, which is the absolute magnitude. This standardization procedure equalized the three concentrations in terms of absolute magnitude of evoked response. Consequently, the neural population responses of the 12 stimuli (4 types X 3 concentrations) could be compared based only on their across-neuron patterns (ANPs) (relative amount of activity across neurons). 6. When stress and squared correlation values were used as criteria for dimensionality, the configuration of the artificial mixtures space was best derived from dimensions 1, 2, and 3 of the three-dimensional resolution. When relevance to quality coding was used, the configuration of the artificial mixtures space was best derived from dimensions 1, 3, and 4 of the four-dimensional resolution. Whether stress and squared correlation values or relevance to quality coding were used, the four types of stimuli occupied nonoverlapping spaces.(ABSTRACT TRUNCATED AT 400 WORDS)

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Purinergic modulation in the brain of the spiny lobster.

Earlier studies identified purinergic chemoreceptors in the olfactory organ of the spiny lobster, Panulirus argus. In this study, electrophysiological experiments demonstrate that purinergic substances can modulate both the spontaneous activity and the evoked responses of neurons within the brain of this animal. Perfusion of the brain with 100 microM adenosine 5'-monophosphate (AMP) modulated the spontaneous activity of 71% of the brain interneurons that were monitored. AMP also modulated the electrically or chemically evoked activity of 25% of the monitored interneurons. The effects were dose-dependent (down to 1 microM) and reversible. The modulatory effects of adenosine were similar to those of AMP, and were antagonized by the adenosine receptor antagonist 1,3-dipropyl-8-p-sulfophenylxanthine. The modulation by AMP or adenosine was depressive in most but not all neurons, as is the case with purinergic effects in the brain of vertebrates. We believe this is the first demonstration of modulatory effects of purinergic substances in the nervous system of any invertebrate.

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Processing of olfactory information at three neuronal levels in the spiny lobster.

Odor quality coding was analyzed at three neuronal levels, receptor cells and two levels of chemosensory interneurons, in the olfactory system of the spiny lobster Panulirus argus . Responses to three of the most stimulatory compounds for this animal - taurine, glutamate and betaine - were recorded at each level in order to compare basic neuronal response properties, single cell and population response spectra, and across-neuron patterns. Mean response specificity increased for cells at each successive neuronal level. The increase in breadth of tuning between receptor cells and low-order interneurons was paralleled by an increase in interstimulus across-neuron correlations. However, in high-order interneurons, there was a relative decline in across-neuron correlations, indicating that the more broadly-tuned high-order interneurons are better able to discriminate between any two compounds than are the more narrowly-tuned low-order interneurons. Although stimulus quality appears to be coded by interneurons as an across-fiber pattern, the fact that some low-order and high-order interneurons retained the narrow specificity of receptor cells suggests that labeled lines may have an important function in coding throughout the olfactory pathway of the spiny lobster.

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Quality coding of a complex odorant in an invertebrate.

Mechanisms whereby the olfactory system of the spiny lobster codes food odors were quantitatively analyzed. A 23-component chemical mixture, with a composition based on a tissue extract from a known food of lobsters, and 8 of the mixture's components were used to describe responses of single cells at two neural levels: a) olfactory receptor cells and b) low-order interneurons projecting from the main olfactory center of the brain. Cluster analysis identified six classes of narrowly tuned receptor cells. Interneurons, on the other hand, were significantly more broadly tuned than receptor cells and could not be grouped into a small number of discrete, highly correlated cell types. Nonetheless, some chemosensory interneurons (unimodal interneurons) had specificities as narrow as receptor cells. Across-neuron correlations between stimuli showed that the increase in neuronal breadth of responsiveness from the level of receptors to the level of interneurons was paralleled by an increase in similarity in across-neuron patterns and, therefore, a decline in ability to discriminate between any two compounds. Across-neuron correlations between concentrations of a given compound showed that stimulus quality had a much stronger effect on across-neuron patterns than did stimulus quantity and, hence, stimulus qualities could be distinguished in spite of concurrent changes in stimulus quantity. Coding of odor quality could be accomplished at the receptor level by a labeled-lines code. At the interneuronal level, odor quality appears to be coded by across-fiber patterns. However, the finding that unimodal interneurons were as narrowly tuned as receptor cells indicates that specific channels for some food-odor components (e.g., taurine and glycine) are conserved even at higher neuronal levels. These narrow-spectrum interneurons may have a special function in quality coding either by dominating the interneuronal across-fiber pattern for that stimulus or by being processed independently of the broad-spectrum interneurons and thereby transferring information about certain components by way of specific channels to even higher neuronal levels.

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Learning from spiny lobsters about chemosensory coding of mixtures.

Studies of the peripheral olfactory system of the Caribbean spiny lobster Panulirus argus and related decapod crustaceans have helped us understand mechanisms of coding of mixtures, some of which are discussed in this review. Although the number of cells in the lobster's olfactory system is much lower than in vertebrate olfactory systems, it is a highly complex system. The receptor neurons (RNs) of this olfactory system are complex processors that cannot be categorized into discrete cell types, but rather have a diversity of response profiles. Each RN can have different types of receptor proteins, second messengers, and/or ion channels, which undoubtedly contributes to the functional diversity of these neurons and makes them complex peripheral integrators. The RNs probably encode information about the quality of mixtures as a distributed or population code, providing a basis for behavioral discrimination of natural food stimuli. Analysis of distributed codes for a series of blend ratios of binary mixtures reveals that the qualities of individual compounds are probably not lost when mixed. Such peripheral processing allows spiny lobsters to perceive complex odors as a set of elemental cues if the salience of the components is sufficiently high.

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