Central nervous processing of behaviourally relevant odours in solitary and gregarious fifth instar locusts, Schistocerca gregaria (original) (raw)
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Journal of Comparative Physiology A, 1996
Olfactory receptor neurons present in two morphological sensillum types on the male Schistocerca gregaria antenna were for the first time investigated physiologically when stimulated with behaviourally relevant odours. Neurons present in trichoid/basiconic sensilla showed clear excitatory responses to compounds present in the male-produced aggregation pheromone and also to a plant produced compound. Sensilla could be categorised physiologically according to the responses of their receptor neurons to the tested stimuli. Also receptor neurons present in sensilla coeloconica responded to aggregation pheromone components, but always in an inhibitory fashion. These neurons could, however, be excited by a plant produced compound and by some acids present in the nymphal odour. The antennal lobe of the male S. gregaria was observed to contain about 1000 very small glomerular structures. Single receptor neurons were stained from the antenna to the antennal lobe using a cobalt lysine technique. These stainings revealed a multi glomerular axonal branching pattern of antennal receptor neurons. Key words Antennal lobe projection 9 Single sensillum 9 Locust -Receptor neuron 9 Electrophysiology Abbreviations AN antennal nerve 9 AL antennal lobe. RN receptor neuron B. S. Hansson (~:~3)' S. A. Ochieng' 9 S. Anton
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 1998
Stimulation of the antenna of the male moth, Manduca sexta, with a key component of the female's sex pheromone and a mimic of the second key component evokes responses in projection neurons in the sexually dimorphic macroglomerular complex of the antennal lobe. Using intracellular recording and staining techniques, we studied the antennal receptive ®elds of 149 such projection neurons. An antennal¯agellum was stimulated in six regions along its proximo-distal axis with one or both of the pheromone-related compounds while activity was recorded in projection neurons. These neurons fell mainly into two groups, based on their responses to the two-component blend: neurons with broad receptive ®elds that were excited when any region of the¯agellum was stimulated, and neurons selectively excited by stimulation of the proximal region of thē agellum. Projection neurons that were depolarized by stimulation of one antennal region were not inhibited by stimulation of other regions, suggesting absence of antennotopic center-surround organization. In most projection neurons, the receptive ®eld was determined by aerent input evoked by only one of the two components. Dierent receptive-®eld properties of projection neurons may be related to the roles of these neurons in sensory control of the various phases of pheromonemodulated behavior of male moths. Key words Antenna á CNS á Glomerulus á Insect á Olfaction Abbreviations AL antennal lobe á Bal bombykal á C15 (E,Z)-11,13-pentadecadienal á IPSP inhibitory postsynaptic potential á MGC macroglomerular complex á PN projection neuron
Neuron, 2001
The Salk Institute independently of any temporal patterning in the olfac-Computational Neurobiology Laboratory tory input. It rather results from the intrinsic dynamics La Jolla, California 92037 of interacting excitatory PNs and inhibitory local neurons 2 California Institute of Technology (LNs). Unpatterned electrical stimulation of the olfactory Biology Division, 139-74 afferent axon tract evoked different temporal response Pasadena, California 91125 patterns in simultaneously recorded PNs (Wehr and 3 Institute for Nonlinear Science Laurent, 1999). In addition, activation of spatially differ-University of California, San Diego ent groups of afferents with otherwise identical electrical La Jolla, California 92093 stimuli produced different response patterns in individ-4 Department of Physics and Marine ual PNs. The complex synaptic organization of the an-Physical Laboratory tennal lobe network must therefore, by itself, provide Scripps Institution of Oceanography the mechanisms underlying odor-specific slow temporal University of California, San Diego patterning. In a recent theoretical study, it was shown La Jolla, California 92093 that heteroclinic structures in the phase space of a dy-5 Department of Biology namical system representing the antennal lobe network University of California, San Diego can underlie patterns of PN activity that resemble those La Jolla, California 92093 observed in vivo (Laurent et al., 2001). The specific mechanisms underlying these slow temporal structures, however, remain unknown. This issue is explored here. Summary The dynamical properties of a network consisting of interacting excitatory and inhibitory neurons depend, in Locust antennal lobe (AL) projection neurons (PNs) part at least, on the dynamics of synaptic transmission respond to olfactory stimuli with sequences of depobetween its elements. Previous pharmacological experilarizing and hyperpolarizing epochs, each lasting hunments with the locust antennal lobe showed that fast dreds of milliseconds. A computer simulation of an AL inhibition mediated by LNs can be blocked by applicanetwork was used to test the hypothesis that slow tion of the GABA-activated chloride channel blocker picinhibitory connections between local neurons (LNs) rotoxin (MacLeod and Laurent, 1996; MacLeod et al., and PNs are responsible for temporal patterning. Acti-1998; Stopfer et al., 1997). Picrotoxin blocks fast IPSPs, vation of slow inhibitory receptors on PNs by the same thereby desynchronizing PNs and thus the antennal lobe GABAergic synapses that underlie fast oscillatory synoutput. Remarkably, however, this manipulation spared chronization of PNs was sufficient to shape slow rethe slow patterning of individual PN responses to odors sponse modulations. This slow stimulus-and neuron-(MacLeod and Laurent, 1996; MacLeod et al., 1998; specific patterning of AL activity was resistant to Stopfer et al., 1997). In particular, picrotoxin did not blockade of fast inhibition. Fast and slow inhibitory block the slow phases of inhibition observed in PNs mechanisms at synapses between LNs and PNs can before, between, or following bursts of odor-evoked acthus form dynamical PN assemblies whose elements tivity. Pharmacological blockers of the vertebrate GABA B synchronize transiently and oscillate collectively, as receptor did not affect this slow inhibition (K. MacLeod observed not only in the locust AL, but also in the and G.L., unpublished data). This pharmacological analvertebrate olfactory bulb. ysis, however, does not exclude the possible presence of metabotropic GABA receptors, for insect and verte-Introduction brate receptor/channel pharmacology can differ significantly. Bicuculline, for example, fails to block fast and Odor stimulation evokes complex temporal patterns of picrotoxin sensitive GABA-mediated inhibition in most activity in the mitral cells of the vertebrate olfactory bulb insects. These experimental results simply indicate the (Kauer, 1974; Kauer and Shepherd, 1977; Chaput and existence of slow inhibitory mechanisms, whose action Holley, 1980; Meredith, 1986, 1992) and projection neumay be to shape the slow evolution of antennal lobe rons (PNs) of the insect antennal lobe (Burrows et al., dynamics. These slow mechanisms must be synaptic 1982; Christensen and Hildebrand, 1987; Laurent and because long-lasting PN inhibition can occur in the ab-Davidowitz, 1994). These patterns, recently charactersence of any preceding spiking by the inhibited neuron ized in locust, consist of alternating epochs of excitation (e.g., see Figure 1; Laurent et al. , 1996). Thus, AHP-(characterized by Na ϩ spikes), inhibition (PN activity is type mechanisms as well as reciprocal inhibition can be reduced or subthreshold), and quiescence. Different excluded as necessary functional features. odors can evoke different temporal patterns in one PN, Our goal here is to build on our previous model of the antennal lobe, initially designed to investigate the fine temporal structure of spike synchronization during ol-6
Olfactory signalling in antennal receptor neurones of the locust (Locusta migratoria)
Journal of Insect Physiology, 1993
The electrical properties of isolated antenna1 neurones from Locusta mipatoria were investigated using patch clamp techniques. The neurones displayed a resting potential of -26 f 11 mV (n = 38) and an input resistance between l-6 Ga. Upon application of depolarizing voltage steps a noninactivating non-specific inward current and a calcium-dependent outward potassium current were identified. Some neurones responded to stimulation by the grass odour hexenoic acid (l-100 p M) with an increase in ion channel activity in cell-attached recordings. This channel was identified as a calcium-activated potassium channel belonging to the maxi-K+-channel types. Odour-stimulation of antenna1 tissue and antenna1 cells using a fast quench device leads to a rapid generation of inositol 1,4,9trisphosphate, supporting the idea that this substance acts as second messenger in insect olfaction. The odour-induced increase in inositol trisphosphate concentration may initiate a rise in intracellular calcium controlling the activity of calcium-dependent ion channels.
Neuron, 2002
Here we apply this novel experimental strategy to obtain direct images of a series of representational intermediates in an intact neural network, the antennal lobe of the fruit fly, Drosophila melanogaster. Our experi-Summary ments rely on the capacity of natural odors to activate physiologically relevant neural ensembles in this sen-Three classes of neurons form synapses in the antensory network and take advantage of the lobe's small nal lobe of Drosophila, the insect counterpart of the scale and our ability to discern its principal neuronal vertebrate olfactory bulb: olfactory receptor neurons, elements genetically. We visualize odor-specific ensemprojection neurons, and inhibitory local interneurons.
Origin and morphogenesis of sensory neurons in an insect antenna
Developmental Biology, 1976
Each antenna1 flagellum of the moth, Manduca sexta, contains about 2.5 x lo" primary sensory neurons. The neurons are components of small sensory organs (sensilla) and send axons through antenna1 nerves to the brain. The neurons, sensilla, and nerves differentiate as the antenna develops, during the 18 days of metamorphosis from pupa to adult. Neurons arise from divisions of epidermal cells between 25 and 60 hr after pupal ecdysis and elaborate axons and dendrites soon thereafter. Neurons have the bipolar form, ciliated dendrite, and glial sheath characteristic of the adult within a few days of their birth. The axons grow along small pupal nerves to form the adult antenna1 nerves, and the dendrites grow beyond the apical margin of the epidermis, where they are enveloped by a growing process of the sensilla's trichogen cell. Cuticle secreted by the trichogen cell forms the seta or sensory hair of the sensillum. Later, the neuronal somata migrate from the basal to the apical margin of the epidermis. Finally, the cytoplasm withdraws from the seta, leaving the dendrites imprisoned in a cylinder of cuticle. All of the neurons in the flagellum differentiate nearly synchronously, facilitating correlation of morphogenetic results presented here with biochemical and electrophysiological analyses of the developing neurons. 300 Copyright G 19% by Acadeinic Press, Inc. All rights of reproduction in any form reserved.
Chemical senses, 1996
Based on anatomical and physiological data pertaining to several moth species and the cockroach, we propose a neural model for pheromone discrimination in the insect antennal lobe. The model exploits the variety of neuronal response patterns observed in the macroglomerulus, and predicts how these complex patterns of excitation and inhibition can participate in the discrimination of the species-specific pheromone blend. The model also allows us to investigate the relationship between the distribution of observed response patterns and the neural organization from which these patterns emerge.
Local and Intersegmental Interneurons with Chemosensory Inputs from the Locust Ovipositor
2015
Sensory afferents from the ovipositors influence the behaviour of locusts before and during egg-laying. Contact chemoreceptors, known as basiconic sensilla in insects, occur dispersed and crowded in fields between mechanosensory receptors on the ovipositor of the female desert locust Schistocerca gregaria and serve to control the chemical features of the substrate before and during oviposition. Responses of contact chemoreceptors to aqueous solutions of salts (NaCl), sugars (glucose), acids (citric acid), oviposition aggregation pheromones (veratrole and acetophenone), alkaloids (quinine and tomatine), and phenolic compounds (salicin) were seen. Higher order processing occurs in local and ascending interneurones of the terminal abdominal ganglion. We focussed on a cluster of interneurons extending in the anterolateral region of the eighth abdominal neuromere. Several have ascending collaterals to more anterior abdominal ganglia. The physiological and morphological differences betwee...
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 1997
Responses of antennal lobe neurons to dierent amounts of the female-produced pheromone blend and to its individual components were investigated in Agrotis segetum males using intracellular recording methods. We identi®ed three physiological types of antennal lobe neurons, categorized according to their response thresholds to single pheromone components and to the blend: generalist neurons, component-speci®c neurons and blend-speci®c neurons. Response and spe-ci®city of antennal lobe neurons were largely dose dependent. In most cases speci®c responses occurred only at low stimulus amounts, while increasing concentrations often resulted in an increase of the number of pheromone stimuli to which the neuron responded. Dose-response relationships often diered between different stimuli activating a neuron.