Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta

Keil, Thomas A.

doi:10.1016/0040-8166(89)90028-1

Cited by 88 publications

(58 citation statements)

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“…Specificity of the olfactory receptor neurons and behavioural aspects As described previously (Dolzer et al, 2001;Kalinová et al, 2001), but in contrast to other studies in M. sexta (Kaissling et al, 1989;Marion-Poll and Tobin, 1992), two classes of action potentials, which can probably be assigned to the two ORNs in each sensillum (Keil, 1989), could be distinguished by their amplitude in most of the recordings. Our experiments showed that in M. sexta, as in other moth species investigated, the ORN that fires the action potentials with the larger amplitude responds to the main component of the conspecific pheromone blend (Bombyx mori, Kaissling et al, 1978;Antheraea polyphemus and A. pernyi, Zack, 1979; Mamestra suasa, Lucas and Renou, 1989; Mamestra brassicae, Renou and Lucas, 1994).…”

Section: Discussionmentioning

confidence: 58%

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Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta

Dolzer

Fischer

Stengl

2003

Journal of Experimental Biology

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While the transduction cascade of pheromone-sensitive olfactory receptor neurons (ORNs) in insects has been thoroughly investigated in vitro (Breer et al., 1988Boekhoff et al., 1990Boekhoff et al., , 1993Stengl et al., 1992;Stengl, 1993Stengl, , 1994Wegener et al., 1993Wegener et al., , 1997, little is known about olfactory adaptation and the mechanisms involved. Adaptation is a universal characteristic of receptor cells of all sensory modalities (Burkhardt, 1961). There are different definitions for the term 'adaptation' but implicit in any definition is a decrease in sensitivity due to the influence of a previous (conditioning) stimulus (Zack, 1979).Moths distinguish pheromone mixtures according to the concentration ratios of the different pheromone components. Thus, differentiation of pheromone concentrations is very crucial for recognition of prospective mates. Turbulences and wind velocities determine the structure of the pheromone filaments that stimulate the antenna of a flying moth. Thus, adapting and non-adapting pheromone stimuli of variable concentrations and stimulus durations reach different parts of the antenna at various time intervals. It is still unknown how the moth can recognize relevant pheromone ratios in various states of adaptation. In our study of pheromone-sensitive ORNs, we examine how adapting pheromone stimuli affect the encoding of different pheromone concentrations (quantity coding) in the intact moth. We distinguish the rapidly (within seconds to minutes) reversible reduction of sensitivity due to prior stimulation (short-term adaptation) from the decline in excitation, as seen during a phasic-tonic response to a stimulus of long duration (desensitization; Zufall and Leinders-Zufall, 2000). Thus, we compare quantity coding in response to short (50·ms) and long (1000·ms) pheromone stimuli, as possibly encountered during flight to the calling female. We do not examine the more slowly occurring (within several minutes to hours) reduction of sensitivity due to In extracellular tip recordings from long trichoid sensilla of male Manduca sexta moths, we studied dose-response relationships in response to bombykal stimuli of two different durations in the adapted and the non-adapted state. Bombykal-responsive cells could be distinguished from non-bombykal-sensitive cells in each trichoid sensillum because the bombykal-responsive cell always generated the action potentials of larger initial amplitude. The bombykal cell, which was recorded at a defined location within a distal flagellar annulus, can resolve at least four log 10-units of pheromone concentrations but is apparently unable to encode all stimulus durations tested. Parameters of the amplitudemodulated sensillar potential and the frequencymodulated action potential responses were examined in different states of adaptation. Evidence is presented for the existence of several mechanisms of adaptation, which affect distinct steps of the transduction cascade. After adapting pheromone stimuli, the sensillar potential rises to a lower ampl...

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Section: Discussionmentioning

confidence: 58%

“…Moths detect the pheromones using specialized ORNs, which innervate long multiporous trichoid sensilla on the antenna in pairs (Keil, 1989). It has been shown that in each trichoid sensillum, one of the ORNs (the bombykal cell) responds to bombykal, the main component in the conspecific pheromone blend (Starratt et al, 1979;Tumlinson et al, 1989).…”

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confidence: 99%

Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta

Dolzer

Fischer

Stengl

2003

Journal of Experimental Biology

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“…Type I trichoid hairs (.600 ,um in length) are typical olfactory sensilla, with single walls and pores, and include two ORCs that send their unbranched dendrites through the lumena of the fluid-filled hairs to their tips (51,(55)(56)(57). In most of these sensilla, one of the two male-specific ORCs is highly sensitive and specific to pheromone component A, while the second ORC is tuned to component B (54).…”

Section: Origins Of Olfactory Systemsmentioning

confidence: 99%

“…A male flagellum has -3 x 105 ORCs associated with 0 recognized sensilla, of which '40% are male-specific sensory hairs or sensilla trichodea (51,(53)(54)(55)(56). Type I trichoid hairs (.600 ,um in length) are typical olfactory sensilla, with single walls and pores, and include two ORCs that send their unbranched dendrites through the lumena of the fluid-filled hairs to their tips (51,(55)(56)(57).…”

Section: Origins Of Olfactory Systemsmentioning

confidence: 99%

Analysis of chemical signals by nervous systems.

Hildebrand

1995

Proc. Natl. Acad. Sci. U.S.A.

174

103

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Intraspecific and interspecific communication and recognition depend on olfaction in widely diverse species of animals. Olfaction, an ancient sensory modality, is based on principles of neural organization and function that appear to be remarkably similar throughout the zoosphere.Thus, the "primitives" of olfactory stimuli that determine the input information of olfaction, the kinds of "molecular images" formed at various levels in the olfactory pathway, and the cellular mechanisms that underlie olfactory information processing are comparable in invertebrates and vertebrates alike. A case in point is the male-specific olfactory subsystem in moths, which is specialized to detect and analyze the qualitative, quantitative, and temporal features of the conspecific females' sex-pheromonal chemical signal. This olfactory subsystem can be viewed, and is here presented, as a model in which common principles of organization and function of olfactory systems in general are exaggerated to serve the requirements of a chemical communication system that is crucial for reproductive success.All creatures detect and react to chemicals in the external environment. In metazoans possessing a differentiated nervous system, an important function of that system is to detect, analyze, integrate, and generate responses to chemicals in the environment. Among the substances to which these organisms must respond are chemical signals, including pheromones and kairomones. Pheromones are chemical messengers between individuals of the same species, such as the sex attractants of moths and the alarm pheromone of honey bees. Kairomones are chemical messengers between species and adaptively favorable to the recipient, such as attractants and stimulants for insect oviposition and feeding emitted by a host plant. The importance of such chemical signals for survival and reproductive success is reflected in remarkable chemosensory capacities and specializations in diverse species of animals.After considering the evolutionary origins of the olfactory system and some basic principles of olfaction, this brief review examines one of the most extensively studied examples of neural processing of semiochemical information: the sex pheromone-specific olfactory subsystem in male moths. This malespecific subsystem can be viewed as representing an exaggeration of organizational principles and functional mechanisms that are characteristic of olfactory systems in general. Origins of Olfactory SystemsConsideration of the origins and evolution of chemosensation can help one to begin to understand the themes of olfaction and chemical communication that are common to diverse phyletic groups. This section emphasizes ideas that were propounded with characteristic clarity and elegance by the late Vincent Dethier in his 1990 R. H. Wright Lectures on Olfaction. Because the published version of those lectures (1) may not be widely accessible, some of Dethier's main points are restated here.Origins of Chemoreception. The universal chemoreceptive capacity of living o...

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“…The pheromone-sensitive sensilla are located in large numbers at the leading edge of the antenna and are each innervated by two olfactory receptor neurons (ORNs) (Sanes and Hildebrand, 1976;Keil, 1989;Lee and Strausfeld, 1990). Both ORNs are sensitive to different components of the pheromone blend.…”

Section: Introductionmentioning

confidence: 99%

Perfusion with cGMP analogue adapts the action potential response of pheromone-sensitive sensilla trichoidea of the hawkmoth Manduca sextain a daytime-dependent manner

Flecke

Dolzer

Krannich

et al. 2006

Journal of Experimental Biology

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SUMMARY Pheromone-dependent mate search is under strict circadian control in different moth species. But it remains unknown whether daytime-dependent changes in pheromone sensitivity already occur at the periphery in male moths. Because adapting pheromone stimuli cause rises of cyclic guanosine monophosphate (cGMP) in pheromone-sensitive trichoid sensilla of the night-active hawkmoth Manduca sexta, we wanted to determine whether cGMP decreases pheromone-sensitivity of olfactory receptor neurons in a daytime-dependent manner. Long-term tip recordings from trichoid sensilla were performed at the early day (ZT 1-4), when many moths are still active, and at the middle of the day (ZT 8-11), when moths are resting. A non-adapting pheromone-stimulation protocol combined with perfusion of the sensillum lymph with the membrane-permeable cGMP analogue 8bcGMP adapted the action potential response but not the sensillar potential. Perfusion with 8bcGMP decreased the initial action potential frequency, decreased the numbers of action potentials elicited in the first 100 ms of the pheromone response and attenuated the reduction of action potential amplitude. Furthermore, the decrease in 8bcGMP-dependent action potential frequency was stronger in recordings made at ZT 8-11 than at ZT 1-4. In the control recordings during the course of the day the pheromone responses became increasingly tonic and less phasic. At ZT 8-11 only, this daytime-dependent effect was further enhanced by 8bcGMP application. Thus we hypothesize that during the moths' resting phase,elevated cGMP levels underlie a daytime-dependent decrease in pheromone sensitivity and a decline in the temporal resolution of pheromone pulses.

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Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta

Cited by 88 publications

References 20 publications

Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta

Adaptation in pheromone-sensitive trichoid sensilla of the hawkmoth Manduca sexta

Analysis of chemical signals by nervous systems.

Perfusion with cGMP analogue adapts the action potential response of pheromone-sensitive sensilla trichoidea of the hawkmoth Manduca sextain a daytime-dependent manner

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