Individual Sensilla Research Articles

The contribution of olfactory receptor neurons to the perception of pheromone component ratios in male redbanded leafroller moths.

(Z)-11-tetradecenyl acetate (Z-11, 14:AC) must be in a 100:9 ratio with (E)-11-tetradecenyl acetate (E-11,14:AC) to produce maximal wing fanning and attraction in male redbanded leafrollers. Earlier electrophysiological studies had indicated that mixtures of these pheromone components elicited responses from olfactory receptor neurons that appeared to differ from those expected on the basis of the responses to the individual components. Here we evaluate whether the behavioral sensitivity to particular ratios of Z- and E-11,14:AC has a correlate in the response properties of olfactory receptor neurons. The stimuli included the ratios of Z- and E-11,14:AC used in earlier behavioral work plus several different mixtures of the seven components found in the pheromone blend, and equivalent amounts of the individual components. These stimuli were presented over a range of intensities to individual trichoid sensilla on the male antenna. In common with earlier results, the receptor neuron with the larger amplitude action potential responded most strongly to Z-11,14:AC, whereas the companion receptor neuron in the sensillum responded most strongly to E-11,14:AC. In contrast with earlier results, each receptor neuron responded exclusively to its own most effective stimulus, without regard to the presence of any other compound. They failed to respond uniquely to any of the other five compounds in the female pheromone blend, or to any of the tested combinations of these compounds. These minor components also failed to modulate the responses elicited in receptor neurons by appropriate ratios of Z- and E-11,14:AC. Thus, the responses of the two types of olfactory receptor neurons found in trichoid sensilla failed to show an optimum at the pheromone ratio known to elicit peak behavioral activity.

Electrophysiological responses of olfactory receptor neurons to stimulation with mixtures of individual pheromone components.

Multicomponent pheromone systems are the rule in many species. As our knowledge about the number and kinds of different chemical compounds actually employed in the communication system of a particular species has increased, so too has our appreciation for the level of neurobiological complexity that must underlie these capabilities. The supposition that mixtures are differentially processed in the nervous system arises most easily when biologically relevant materials are evaluated, either singly or in multicomponent blends, with modern behavioral assay techniques. It is becoming increasingly clear that this increase in the chemical and behavioral complexity of a particular communication system must be paralleled by an increase in the efficiency of the physiological mechanisms employed for the neural encoding of behaviorally relevant odor compounds and blends. Here we review several studies that have examined the electrical activity elicited in primary olfactory receptor neurons when they are stimulated with mixtures of odorants. Particular attention is given to the responses elicited in a subset of the individual pheromone-sensitive sensilla on the antennae of male cabbage looper moths (Trichoplusia ni). Electrophysiological responses to single- and multiple-component stimuli, each drawn from among the seven known behaviorally active compounds for this insect, were obtained at several different stimulus intensities. Both (Z)7-dodecenyl acetate and (Z)7-dodecenol were effective stimuli for both of the receptor neurons found in one of the two classes of pheromone-sensitive sensilla, even at relatively low stimulus intensities (0.0005 micrograms). Dodecyl acetate, although behaviorally active, did not significantly excite either of these receptor neurons. However, when mixed with either of the unsaturated components, it significantly enhanced the receptor neuron's response to its appropriate parent compound only in the middle range of stimulus intensities. A mixture of all three components did not show this enhancement and at the middle range of intensities actually elicited reduced responses when compared to those elicited by appropriate amounts of any of the one- and two-component stimuli evaluated. Thus, some blends elicited electrical responses from primary olfactory receptor neurons that were not readily predicted from a knowledge of the receptor neurons' response to individual components.

Insect olfactory receptor responses to components of pheromone blends

Multicomponent pheromone systems are common in many insect species. As our knowledge about the number of different chemical compounds actually involved in a particular communication system increases, so too does the need for an efficient neural mechanism for the encoding of behaviorially relevant odor compounds. Here we consider the electrical activity of olfactory receptor neurons in a subset of the individual pheromone-sensitive sensilla on the antennae of male cabbage looper moths (Trichoplupia ni). Responses to single- and multiple-component stimuli, drawn from seven behaviorally active compounds, were obtained at several different intensities. Some blends elicited electrical responses which were not readily predicted from a knowledge of the receptor neuron's response to individual components.

Functional organization of insect auditory sensilla

1. Electrophysiological recordings from individual auditory sensilla in the tettigoniid (Caedicia simplex) ear (Fig. 1) show that spike potentials of two distinct amplitudes occur in the sensory neuron (Fig. 2). Generally, the smaller of the two classes of spike is observed as an inflection on the rising phase of the larger spike. In cases where the larger spike fails or is blocked, the smaller spike becomes distinct. In the attachment cell of the sensillum, negative-going monophasic, or biphasic spikes are recorded (Fig. 3). In biphasic spikes, the positive phase is of smaller amplitude and always follows the negative phase. 2. Simultaneous recordings from the sensory neuron and from its associated attachment cell, using two electrodes, show that the negative-going spike recorded from the attachment cell corresponds with the smaller spike recorded from the neuron (Fig. 4). The occurrence of a large spike in the neuron causes the positive-going potential in the attachment cell, immediately following the negative spike. 3. Injection of negative current into the attachment cell via a recording electrode elicits spikes in the sensory neuron. If large spikes in the neuron fail or are blocked by hyperpolarization of that cell, the injection of negative current into the attachment cell elicits small spikes in the neuron (Fig. 4). 4. Electrical stimulation of the tympanal nerve induces retrograde spikes in the soma of the sensory neuron. Such spikes show no inflection in the rising phase, indicating the absence of the small spike as a precursor to the retrograde spike (Fig. 6). Recordings from the attachment cell, when retrograde spikes are induced, show only a positive-going potential correlated with each retrograde spike. The positive deflections recorded in the attachment cell, resulting from retrograde spikes, generally are of greater amplitude than those specifically associated with large, orthograde spikes occurring in the sensory neuron. 5. These results confirm previous suggestions that, in insect auditory, chordotonal sensilla, spikes of relatively small amplitude occur at the apex of the sensory dendrite and subsequently, trigger spikes of conventional amplitude at a site more proximal in the dendrite. The occurrence of small spikes in the neuron implies novel equilibrium potentials at the apical dendritic membrane, which may result from the scolopale lumen functioning as a receptor lymph cavity.

Responses to pheromone blends in insect olfactory receptor neurons

1. The electrical activity of the two olfactory receptor neurons in individual pheromone-sensitive sensilla on the antennae of male cabbage looper moths (Trichoplusia ni) was monitored extracellularly. Responses to single and multiple component stimuli containing up to three of the seven behaviorally active compounds for this species were obtained at several different stimulus intensities. 2. Neurons which produced large amplitude action potentials (A neurons) were more responsive to (Z)7-dodecenyl acetate, a major component of the female pheromone gland, than were their companion B receptor neurons. B receptor neurons were more responsive to (Z)7-dodecenol, a behavioral inhibitor of male orientation to calling females. Neither neuron was particularly responsive to stimuli containing only dodecyl acetate, a minor component of female glands, which has powerful synergistic effects on male behavior. 3. Some blends of these three compounds elicited responses which were not readily predicted from a knowledge of the cells' responses to individual components of the blend. 4. The average A receptor neuron was significantly more responsive to the blend containing (Z)7-dodecenyl acetate and 10% dodecyl acetate than it was to either component alone or, for that matter, to the algebraic sum of their individual responses. These enhancements were intensity-dependent, occurring to a significant extent only in the middle portion of a neuron's dose-response function. Although A recpetor neurons are not particularly responsive to either (Z)7-dodecenol or dodecyl acetate, a binary mixture of these components elicited significantly smaller responses than expected. Blends which contained all three compounds elicited responses in A receptor neurons which were also significantly smaller than those expected. These reductions were dose-dependent and occurred most reliably at the middle of the dose-response function. 5. The responses of B receptor neurons to blends were more variable than those obtained simultaneously in A receptor neurons. Although all of the various alterations in discharge magnitude observed in the typical A receptor neuron response to blend stimulation were seen in some fraction of the B receptor neurons sampled, only the trinary blend elicited responses which were significantly different from those expected. These reductions in the response of B receptor neurons were also intensity-dependent because they were more reliably observed in the middle portion of the neurons' dose-response function. 6. The sensory processing of complex chemical signals by the insect olfactory system has been postulated to involve a set of narrowly tuned, highly specific olfactory receptor neurons, one for each of the behaviorally relevant component compounds in the pheromone blend. Here we show that olfactory receptor neurons may also be responsive in unique ways to multiple component stimuli even in cases where an individual behaviorally relevant pheromone component is not processed by a separate class of receptor neuron.

The structure, function and metamorphic reorganization of somatotopically projecting sensory neurons inManduca sexta larvae

1. A set of innervated sensory hairs that cover the abdominal surface ofManduca larvae is described (Fig. 1). 2. Intracellular recordings from intersegmental muscle motorneurons reveal that they receive different inputs from these sensilla, depending upon the location of their target muscle. In general, sensilla on the same side of the body excite, and those on the opposite side inhibit these motorneurons (Figs. 2, 3). Motorneurons receive input from sensilla on several segments. 3. The branching patterns of the sensory neurons within the CNS were revealed by filling individual sensilla with cobalt. There is a strong correlation between the branching pattern of a sensory neuron and the peripheral location of the hair it innervates (Figs. 4–9). 4. This precise topographic map is maintained across various borders on the body surface. Thus anterior sensory neurons in one segment branch in a similar area as afferents from posterior sensilla in the next anterior segment (Fig. 10). Similarly, sensilla on either side of the dorsal and ventral midlines send their axons to the midline of the ganglion, where their processes overlap (Fig. 10). 5. Ten large hairs are identifiable on each segment of the 5th instar larva, and their sensory neurons branch in a characteristic region of the CNS (Fig. 11). These hairs are among only 16 present on each abdominal segment of the 1st instar animal (Fig. 12). 6. During the larval-pupal transition many of the hairs are lost, but a subset of the sensory neurons remain to innervate the pupal gin-trap sensilla. The central processes of these afferents increase in extent during this developmental period (Fig. 13).

Physiology of auditory receptors in two species of Tettigoniidae (Orthoptera: Ensifera)

1. The gross anatomical features of the crista acustica in the tettigoniids Mygalopsis marki and Polichne sp. are compared (Fig. 1). The crista in Polichne sp. was longer and contained 12 more receptors than that in M. marki. Both organs, however, displayed a gradual and even taper from the proximal to the distal end. The size of the attachment cells and the length of the sensory dendrites displayed a similar gradual decrease in size from the proximal to the distal end of the array (Fig. 1). 2. The characeristic sound frequency and roll offs in sensitivity of ascending auditory interneurons in the oesophageal connectives of M. marki did not alter after the leg cuticle covering the crista acustica was removed (Fig. 2). Since such interneurons receive excitatory and possible inhibitory input from several receptors in the crista this result indicated that the tuning of these receptors was not affected by removing this portion of the leg cuticle. 3. Physiological recordings were obtained from the cell bodies of individual receptors in the crista acustica of M. marki and Polichne sp. (Fig. 3 A, B). Receptors in M. marki produced a maximum response to an 80 ms tone pulse of 16 spikes/stimulus, had a dynamic range of approximately 30 dB and a rate of increase in the spike response of 6 spikes/10 dB (Fig. 3C). The maximum response, dynamic range and slope of the intensity-response characteristics of auditory receptors in Polichne sp. were less than that for receptors in M. marki (Fig. 3 D). The slope of the intensity response characteristics, dynamic range and maximum spike response of individual auditory receptors in both M. marki and Polichne sp. did not alter for sound frequencies above and below the characteristic frequency of the individual receptor (Fig. 3 C, D). 4. The tonotopic organisation of the crista acustica in M. marki and Polichne sp. was determined by the injection of Lucifer Yellow into the cell bodies and dendrites (Fig. 4 A) of receptors for which the frequency-threshold characteristics had been obtained (Fig. 4B). The characteristic frequencies of adjacent receptors in the crista acustica of M. marki were seperated by irregular amounts with receptor 6 tuned to 7 kHz, receptor 7 to 14 kHz, receptor 8 to 17 kHz and receptors 10 and 11 tuned to 20 kHz (Fig. 6). Although adjacent receptors in Polichne sp. were seperated by approximately 1 kHz, the crista acustica of the species contains four receptors tuned to 20 kHz (Fig. 7). 5. The discontinuities in the tonotopic organisation of the crista acustica of M. marki and Polichne sp. are incompatable with the notion that mechanical resonances within the receptor array could be responsible for the frequency selectivity of these auditory receptors. It is therefore proposed that these receptors are tuned as a result of electrical and/or mechanical resonance intrinsic to the individual sensilla.

The Exoskeleton and Insect Proprioception

ABSTRACT Mechanical stimulation of individual tibial campaniform sensilla produces specific reflex effects upon motoneurones to leg muscles. The reflex effects of a campaniform sensillum depend upon the orientation of its cuticular cap. The proximal sensilla, oriented perpendicular to the long axis of the tibia, excite slow motoneurones to the extensor tibiae and extensor trochanteris muscles and inhibit slow motoneurones to the flexor tibiae and flexor trochanteris muscles. The distal sensilla, oriented parallel to the tibia, exhibit reflexes of opposite sign, inhibiting the extensors and exciting the flexors. These reflexes constitute a negative feedback system. Individual sensilla specifically excite motoneurones which innervate muscles whose resultant tensions decrease the firing of those sensilla. It is postulated that individual campaniform sensilla can detect loading of the leg in various postures and can excite appropriate motoneurones in compensation. These receptors can also detect strains caused by large, resisted contractions of the antagonist muscles and inhibit the corresponding motoneurones.

The Exoskeleton and Insect Proprioception. I. Responses of Tibial Campaniform Sensilla to External and Muscle-Generated Forces in the American Cockroach, Periplaneta Americana

ABSTRACT The tibial campaniform sensilla are a group of mechanoreceptors in the cockroach leg that respond to cuticular strain. Each sensillum consists of a single bipolar neurone whose dendrite inserts into an ovoid cuticular cap embedded in the exoskeleton. The tibial campaniform sensilla are consistently separable into two subgroups with mutually perpendicular cap orientation: the long axis of the caps of proximal subgroups are oriented perpendicular to the tibial long axis; caps of the distal subgroup are parallel to the tibia. The responses of individual, identified sensilla from both subgroups were tested to the following forces: bending forces (perpendicular to the leg long axis), axial forces (parallel to the leg axis), torques (twisting about the leg long axis) and forces generated by the tibial muscles. The tibial campaniform sensilla respond vigorously to bending forces imposed in the plane of movement of the adjacent femorotibial joint. Individual sensilla exhibit orientation-dependent directional sensitivity in their response: the proximal sensilla respond only to dorsal bending; the distal sensilla respond only to ventral bending. Sensilla respond less vigorously to bending forces in other planes. Responses are weak but directionally sensitive to axial forces: the proximal sensilla fire upon axial compression; the distal sensilla fire upon axial tension. Both subgroups respond simultaneously but weakly to imposed torques. Contractions of the tibial muscles produce strong orientationdependent responses: the proximal sensilla respond only to flexor muscle contractions; the distal sensilla respond only to extensor muscle contractions. These responses are accurately predicted from a simple model in which the tibia behaves as a cylinder under stress. The tibial campaniform sensilla respond as directionally sensitive strain gauges. Each individual sensillum responds only to compressions perpendicular to the long axis of its cuticular cap. Tibial campaniform sensilla respond best to those forces that the animal can most effectively control.

The role of distributed viscoelastic coupling in sensory adaptation in an insect mechanoreceptor

1. Time-dependent mechanical coupling in proprioceptive campaniform sensilla of the cockroach leg was investigated by measuring the compliance of the sensillar cap with punctate, sinusoidal mechanical stimuli at forcing frequencies ranging 3 mHz (0.003 Hz) to 100 Hz. Coupling was described in terms of linear transfer functions for cap compliance and for sensory discharge sensitivity to both cap indentation and applied force. 2. Most sensilla stiffened viscoelastically as a power of frequency, with median power coefficient −0.058 for compliance, and with indentation lagging force by a constant phase angle, median −8.4°. This behavior indicates broadly distributed viscoelastic rate constants in individual sensilla. The extent of viscoelasticity also varied among sensilla; about a third were purely elastic, with constant compliance and zero phase angle. 3. Discharge sensitivity increased with forcing frequency, usually as a power function, and the sinusoidally modulated discharge peaked sooner than both indentation and force by essentially constant phase angles. Median power coefficients were 0.51 for indentation sensitivity and 0.38 for force sensitivity; corresponding phase angles were somewhat smaller than for a power law, respective medians 39° and 30°. Purely elastic caps gave identical values for indentation and force. 4. This means all sensilla adapted, and all were rate sensitive; but in viscoelastic ones these effects were greater for indentation than for force. 5. Discharge sensitivity for a few sensilla deviated systematically from a power law in that power coefficients and phase angles increased somewhat with forcing frequency. 6. Computed responses for viscoelastic caps showed creep under constant force, and stress relaxation under constant indentation, with faster and greater sensory adaptation for indentation than for force. 7. We conclude cap compliance exerts a mild filtering action throughout the entire time course of adaptation in viscoelastic sensilla, but has no role in the adaptation of purely elastic ones.

Single cell responses from olfactory receptors of small ermine moths to sex-attractants

Morphological classification of the nine European representatives of small ermine moths yields four distinct species and a complex of five closely related forms. In four forms of the complex and one distinct species receptor and action potentials were recorded from the outer dendritic segments of the olfactory cells in individual antennal sensilla trichodea during stimulation with sex-attractants. Two types of cells were activated. The response spectra of these cells in males for the sex-attractants differed characteristically among the various Yponomeuta tested. This indicates that the composition of the respective female sex pheromones may differ. The activity of two cell types suggests that multi-component sex pheromone systems are utilized.

Compliance and sensitivity of a mechanoreceptor of the insect exoskeleton

1. The compliance (indentation per unit force) of the caps of proprioceptive campaniform sensilla of Group 6 of the cockroach leg has been measured in terms of the stimulating force generated per volt of input to a piezoelectric punctate stimulating device. The median compliance value at cap center in 19 preparations, using punctate forces which were modulated sinusoidally at 3 Hz, was 2.1 nm/ΜN (mm N−1), inner quartile range 1.5–3.7 nm/ΜN. 2. Sensitivity to punctate force (impulse frequency modulation per unit force) was meassured simultaneously with compliance. Median force sensitivity in 18 preparations was 3.2 Hz/ΜN (MHz N−1), inner quartile range 2.3–5.1 Hz/ΜN. 3. Sensitivity to indentation (impulse frequency modulation per unit indentation) was determined as force sensitivity divided by compliance. Median indentation sensitivity in 18 preparations was 1.7 Hz/nm (GHz m−1), inner quartile range 1.2–2.0 Hz/nm. Thus the magnitude of cap indentation associated with moderately brisk discharge frequencies of the order of 100 Hz, well within the range of linear encoding, is of the order of a few tens of nanometers. 4. The precision of the method in individual determinations, estimated as the propagated standard error, gave median values of 7.6% for cap compliance, of 5.8% for force sensitivity, and 9.8% for indentation sensitivity. The method was sufficiently precise to resolve variability of repeated measurements on the same sensillum. 5. The reproducibility of repeated measurements on individual sensilla, expressed as median coefficient of variation, gave values of 27% for cap compliance, 25% for force sensitivity, and 32% for indentation sensitivity. Analysis of variance indicated the method was sufficiently reproducible to resolve variability among the individual receptors comprising this study. 6. Cap compliance and indentation are discussed in terms of the structure of the sensillum. The measured compliance values agree quantitatively with simple models based on known mechanical properties of insect cuticle.

Changes in Chemoreceptor Sensilla on the Maxillary Palps of Locusta Migratoria in Relation to Feeding

ABSTRACT The electrical resistance across the tips of the maxillary palps of Locusta migratoria is high immediately after a feed, but falls to a steady level in about 2 h after feeding. Only a small proportion of the individual sensilla on the domes of the palps respond to chemical stimulation immediately after feeding, but this proportion increases with the period of food deprivation. Gentle manipulation of the tips of non-responsive sensilla causes them to respond. It is suggested that the terminal pores of the sensilla can open and close and that the resistance across the tips of the palps varies inversely with the number of open sensilla. The possible significance of the changes is discussed.

Fine structure of the antennal sensory appendix in the larva of Ctenicera destructor (Brown) (Elateridae: Coleoptera).

The antennal sensory appendix of Ctenicera destructor (Brown) appears to be a compound sensillum basiconicum formed by a union of about 12 individual sensilla. It is innervated by about 36 bipolar sense cells of type I, which occur usually in 12 groups of three neurons each. The sensory cuticle is large, cone-shaped, and abundantly perforated by a slit-tubule system. The dendrites of each group of neurons are enclosed distally by a single tubular cuticular sheath attached to the base of the cone by a suspensory fiber system. The ensheathed portion of the dendrites lies in a receptor-lymph cavity formed by the tormogen and accessory trophic cells. Distal dendritic branches pass below and occasionally enter inner pockets in the sensory cuticle, but no connections were seen between the slit-tubule system and the dendritic surfaces. About 12 of each of four types of cells are associated with the neurons in this sensillum: tormogen, trichogen, accessory trophic, and neurilemma. The ultrastructure and probable function of each type is described. A central, complex junction body region divides each dendrite into morphologically distinct distal and proximal region. All the cells associated with the sensillum are in a compact bundle, which is separated from adjacent sensilla within the antenna by a membranous septum. It is suggested that this sense organ has an olfactory function.