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Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, Arizona 85721-0077
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Christensen, Thomas A. and John G. Hildebrand. Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. J. Neurophysiol. 77: 775-781, 1997. Male moths must detect and resolve temporal discontinuities in the sex pheromonal odor signal emitted by a conspecific female moth to orient to and locate the odor source. We asked how sensory information about two key components of the pheromone influences the ability of certain sexually dimorphic projection (output) neurons in the primary olfactory center of the male moth's brain to encode the frequency and duration of discrete pulses of pheromone blends. Most of the male-specific projection neurons examined gave mixed postsynaptic responses, consisting of an early suppressive phase followed by activation of firing, to stimulation of the ipsilateral antenna with a blend of the two behaviorally essential pheromone components. Of 39 neurons tested, 33 were excited by the principal (most abundant) pheromone component but inhibited by another, less abundant but nevertheless essential component of the blend. We tested the ability of each neuron to encode intermittent pheromonal stimuli by delivering trains of 50-ms pulses of the two-component blend at progressively higher rates from 1 to 10 per second. There was a strong correlation between 1) the amplitude of the early inhibitory postsynaptic potential evoked by the second pheromone component and 2) the maximal rate of odor pulses that neuron could resolve (r = 0.92). Projection neurons receiving stronger inhibitory input encoded the temporal pattern of the stimulus with higher fidelity. With the principal, excitatory component of the pheromone alone as the stimulus, the dynamic range for encoding stimulus intermittency was reduced in nearly 60% of the neurons tested. The greatest reductions were observed in those neurons that could be shown to receive the strongest inhibitory input from the second behaviorally essential component of the blend. We also tested the ability of these neurons to encode stimulus duration. Again there was a strong correlation between the strength of the inhibitory input to a neuron mediated by the second pheromone component and that neuron's ability to encode stimulus duration. Neurons that were strongly inhibited by the second component could accurately encode pulses of the blend from 50 to 500 ms in duration (r = 0.94), but that ability was reduced in neurons receiving little or no inhibitory input (r = 0.23). This study confirms that certain olfactory projection neurons respond optimally to a particular odor blend rather than to the individual components of the blend. The key components activate opposing synaptic inputs that enable this subset of central neurons to copy the duration and frequency of intermittent odor pulses that are a fundamental feature of airborne olfactory stimuli.
Time-coding circuits in the auditory systems of birds and mammals and in the electrosensory systems of electric fish provide elegant examples of different strategies for extracting temporal information from the environment. Certain animals use interaural time differences to locate sources of sound (Carr 1993 Adult male Manduca sexta, 2-3 days posteclosion, were used for all experiments. In preparation for intracellular recording, the head capsule was opened and the brain was exposed by removing the labial palps, cibarial pump, and antennal muscles. After the AL had been desheathed with fine forceps, the preparation was superfused with physiological saline (composition in mM: 150 NaCl, 3 CaCl2, 3 KCl, 10 N-tris(hydroxymethyl)methyl-2-aminoethanesulfonic acid buffer, and 25 sucrose, pH 6.9 at 25°C). Sharp glass electrodes (60-80 M All neurons characterized in this study had apparent resting potentials between
Responses to varying odor pulse frequency
Trains of 50-ms pulses of the pheromone components at progressively smaller intervals were used to determine the dynamic range for temporal coding in each neuron (n = 39). First the two-component pheromone blend was used as the stimulus, and then each component was presented separately (see METHODS). In 33 of 39 MGC-PNs, each component evoked a different phase of the "mixed" response to the blend: component A was excitatory and component B was inhibitory (both inputs are probably polysynaptic) Fig. 1B; (Christensen et al. 1993
Responses to varying stimulus duration
In nature, odor molecules form discrete "filaments" of odor interspersed with clean air (Murlis et al. 1990
Our physiological observations are consistent with behavioral evidence from several species of moths, indicating that essential components of the pheromone blend must arrive at the antenna simultaneously to ensure optimal upwind progress toward the source (Vickers and Baker 1992
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Konishi and Volman 1994; Neuweiler 1994; Simmons 1979), and electric fish measure changes in the nearly sinusoidal pattern of their self-generated electric fields to detect nearby objects and to communicate with conspecific animals (Heiligenberg 1994). In crickets, certain auditory interneurons function as sensory filters that copy the temporal pattern of the chirps characteristic of the conspecific calling song (reviewed in Schildberger 1994). In many other species of insects, reproductive behavior is triggered and/or modulated by olfactory cues, and a growing body of evidence indicates that odor plumes, which form downwind from an odor source, possess discontinuous spatiotemporal structural features that are important for the behavior of recipients in response to the odor (Christensen et al. 1996; Murlis et al. 1990). Indeed, "calling" females of certain species of moths release their sex pheromone discontinuously by means of rhythmic extrusion of the pheromone gland, thus imposing on the odor signal a pulsatile pattern (Conner et al. 1980, 1985). Both terrestrial and aquatic organisms are believed to extract information about such spatiotemporal features of odor signals and to use them as aids in locating the odor source (Atema 1995; Mafra-Neto and Cardé 1994; Moore 1994; Vickers and Baker 1992, 1994).
; Schneider 1992). In Manduca sexta in particular, about one third of the ~3 × 105 olfactory receptor cells (ORCs) in each antenna are narrowly and sensitively tuned to specific components of the conspecific female moth's sex pheromone (Homberg et al. 1989; Kaissling et al. 1989). The axons of antennal ORCs project to the ipsilateral antennal lobe (AL) of the brain, where the axons of the pheromone specialist ORCs converge on the macroglomerular complex (MGC), a characteristically organized cluster of specialized glomeruli that also contains the arborizations of male-specific AL local neurons and projection neurons (PNs) that are dedicated to processing of sex pheromonal information (Christensen and Hildebrand 1987; Christensen et al. 1993, 1995; Hansson et al. 1991; Homberg et al. 1988; Kanzaki et al. 1989; Lee and Strausfeld 1990).
). In M. sexta, a mixture of two of the eight aliphatic aldehydes present in the sex pheromone is the minimal blend necessary and sufficient to elicit the characteristic sequence of male reproductive behaviors (Starratt et al. 1979; Tumlinson et al. 1989, 1994). Moreover, PNs in the MGC respond selectively to these two aldehydes, but not specifically to any of the remaining six components (Christensen et al. 1989a). The two components of the pheromone essential for maleattraction are (E,Z)-10,12-hexadecadienal (E10,Z1216:AL, "component A") and (E,E,Z)-10,12,14-hexadecatrienal, a relatively unstable substance for which a morestable chemical mimic, (E,Z)-11,13-pentadecadienal(E11,Z13-15:AL, "component B"), can be substituted (Kaissling et al. 1989). Information about these two key aldehydes is transmitted from the antenna via two functionally distinct primary afferent input channels, each comprising ORCs tuned to one of the key components, to two morphologically distinct glomeruli in the MGC (Christensen et al. 1995; Hansson et al. 1991).
; Baker et al. 1988; Kaissling 1986; Marion-Poll and Tobin 1992; Rumbo and Kaissling 1989). Limiting that ability, however, are physical and biochemical processes that underlie olfactory reception in the periphery and contribute to receptor adaptation and disadaptation (Moore 1994; Stengl et al. 1992). Nevertheless, both the signal-to-noise ratio and the accuracy of stimulus-response phase locking are improved considerably through the convergence of thousands of ORC axons onto a much smaller population of first-order interneurons in the brain (Boeckh and Tolbert 1993; Christensen and Hildebrand 1988, 1994).
; Homberg et al. 1988, 1989). We previously reported that a specific subset of MGC-PNs can encode the temporal pattern of a discontinuous pheromonal stimulus received by the antenna (Christensen and Hildebrand 1988, 1990; Christensen et al. 1989b). When stimulated with repetitive, brief puffs of pheromone blend, these MGC-PNs encode each stimulus pulse with a discrete burst of action potentials (Christensen and Hildebrand 1988). A small percentage of these MGC-PNs can follow pulse frequencies of up to 10 per second with considerable accuracy. One question that has arisen from these studies is what physiological mechanisms distinguish MGC neurons that can encode these rapid temporal changes from neurons that cannot.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
) were filled with 2 M potassium acetate. Signals were amplified (Axoclamp 2A, Axon Instruments), monitored with an oscilloscope, and stored on FM tape for off-line analysis. Recordings were analyzed with customized ASYST scientific software (Keithly Instruments, Rochester, NY).
). Pulses of air from a constant air stream were diverted through a glass syringe containing a piece of filter paper impregnated with a known quantity of the pheromone component or blend. The odor stimulus could be pulsed repetitively by means of a solenoid-activated valve controlled by a computer running customized ASYST stimulation programs. In every experiment, the outlet of the stimulus syringe was positioned ~2 cm from and orthogonal to the center of the antennal flagellum. A synthetic mixture of equal 25-ng amounts of pheromone components A (E10,Z12-16:AL) and B (E11,Z13-15:AL, the stable mimic of the essential trienal component) was found in previous studies to evoke a response in MGC-PNs that was qualitatively and quantitatively similar to the response evoked by the amount of pheromone typically produced by one female (Christensen and Hildebrand 1987, 1988, 1990; Christensen et al. 1989a). Natural pheromone was thus obtained by rinsing a single female moth's pheromone gland with n-hexane. Although the threshold for activation to a one-female-equivalent stimulus loading varies from cell to cell, this amount falls within the dynamic range of all cells examined to date.
), starting at a frequency of one per second. Each neuron was then challenged with a successively greater frequency of pheromone blend pulses until the maximum following frequency was found. This was defined as the maximum frequency at which each stimulus evoked a discrete, phase-locked burst of spikes, and every response burst was separated by a gap of 
50 ms. Next, pheromone components A and B were tested separately to determine which phases of the response were driven by each odorant. Thereafter, if the penetration remained stable, other tests, such as examining responses to different stimulus durations and blend ratios, were performed.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
50 and 55 mV. MGC-PNs were identified by their characteristic response to orthodromic electrical stimulation of the antennal nerve (Fig. 1A) (Christensen et al. 1993): a fast hyperpolarizing potential, followed by a membrane depolarization with associated firing of action potentials and finally a prolonged hyperpolarization that far outlasted the stimulus. Several lines of evidence have suggested that the initial fast hyperpolarization is a Cl
-mediated inhibitory postsynaptic potential (IPSP) elicited by GABAergic local interneurons (Christensen et al. 1993; Waldrop et al. 1987). Similar patterns of postsynaptic activity were evoked by pheromonal stimulation, except that the amplitude of the fast IPSP evoked by one female equivalent of the blend varied considerably from cell to cell (seebelow).
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FIG. 1.
A: in the macroglomerular complex (MGC), a projection neuron (PN) is readily distinguished from a local interneuron (LN) by orthodromic stimulation of the antennal nerve ( 
). Most local interneurons respond with a short-latency depolarization characteristic of monosynaptic input, whereas PNs typically give a more complex response consisting of an inhibitory postsynaptic potential (IPSP) (I) followed by an excitatory postsynaptic potential (E) and spiking activity. Local interneuron spikes typically are broader than PN spikes (Christensen et al. 1993). B and C: intracellularly recorded responses of MGC-PNs to pulsatile stimulation of the antenna with blends of sex pheromone components A and B. The timing and duration of stimuli are indicated beneath the records in B and C. B: responses of a MGC-PN to an optimal blend (1A:1B) as well as to each component. C: responses to a less effective blend ratio (1A:2B). Bi: ipsilateral antenna was stimulated with a train of 5 pulses of the blend delivered at 2 per s. Note that each pulse evoked a membrane depolarization and a discrete burst of action potentials; each response burst occurred with a similar delay from the onset of the corresponding odor pulse (indicated by vertical dashed lines), and each burst was separated from the next by a period of inactivity. Bii: stimulation with component A also evoked a depolarization, but it was greatly prolonged, eliminating the period of inactivity between the 1st and 2nd pulses of odor. This neuron was therefore incapable of encoding intermittent stimulation at this frequency with component A alone. Biii: stimulation with component B alone evoked a membrane hyperpolarization and cessation of spiking activity. C: another MGC-PN followed repetitive stimulation at a faster rate (250-ms interstimulus interval) with the 1:1 blend of components A and B, but could not follow when the blend ratio was 1A:2B. The elevated concentration of the odorant mediating inhibitory input (component B) resulted in a prolonged level of hyperpolarization, such that the excitatory postsynaptic potentials evoked by the 2nd-5th puffs did not reach threshold.
). In the other six neurons, component A was excitatory but component B had no detectable influence on the membrane potential. In addition to these characteristics, marked differences were also noted in the temporal dynamics of responses throughout the population. Some neurons could follow odor pulses only up to ~1 per second, whereas others could encode rapid changes up to ~10 per second (Christensen and Hildebrand 1988).
11.2 mV in amplitude. As shown in Fig. 2, regression analysis revealed a linear relationship between the amplitude of the hyperpolarization evoked by component B and the maximal odor pulse frequency resolvable by the neuron [F(1,34) = 189.9; r2 = 0.85; P < 0.001; regression equation, y = 1.44 + 0.5x]. Most MGC-PNs could encode stimulus rates up to ~2-3 per second (n = 20), whereas others receiving stronger inhibitory input could encode a broader range, displaying "cutoffs" between 4 and 10 pulses per second(n = 13). Neurons that gave no detectable response to component B could not follow pulses more frequent than one or two per second (n = 6).
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FIG. 2.
MGC-PNs are inhibited to different degrees by pheromone component B. The relationship between temporal coding properties and the amplitude of the IPSP evoked by component B is plotted for the pheromone blend as the stimulus ( 
) and component A alone (
). The frequency of blend pulses was increased until the neuron failed to encode every pulse with a discrete burst of action potentials, as shown in Fig. 1B. The ability of an MGC-PN to track intermittent stimuli is strongly correlated with inhibitory input to the neuron, as revealed by a type II regression analysis. Most neurons could encode pheromone blend pulses in the range 1-5 per s (n = 35), whereas 4 neurons with particularly strong inhibitory synaptic input could follow up to 10 stimulus pulses per s. In many neurons receiving strong inhibitory synaptic input from component B, input from component A alone was insufficient to match the rate of pulse coding achieved with the pheromone blend.
6.2 ± 2.2 mV), with a resultant block in spiking activity (Fig. 1Biii). In many MGC-PNs, therefore, excitatory input from the component A input channel alone was insufficient to sustain optimal coding of the pulsatile stimulus (Fig. 2, ). Component B evoked a pronounced hyperpolarization in these neurons, and this level of inhibitory input was apparently necessary to repolarize the cell after each burst of spikes evoked by excitatory input from the component A pathway. This was especially apparent at the highest stimulus rates, between 5 and 10 pulses per second. By contrast, in the 14 remaining MGC-PNs, the amplitude of the inhibitory input due to component B was considerably smaller (1.8 ± 1.3 mV). Component A input alone was sufficient to encode the same rate as with the blend, but the maximal rate encoded in all but one of these neurons was only three pulses per second (Fig. 2).
), and as a male moth flies through a pheromone plume, his antennae encounter filaments of different sizes that activate antennal receptors for different lengths of time. There is evidence, moreover, that the pattern of filaments in a plume changes with distance, and thus a temporal fluctuation in signal strength may serve as an indicator of distance from the pheromone source (Murlis et al. 1990). We therefore wanted to know whether MGC-PNs could encode single pheromone pulses of varying duration. As shown in Fig. 3, we again observed functional differences among MGC-PNs that appeared to be related to the strength of the inhibitory synaptic connections to these neurons. Stimulus duration was encoded with considerable precision by MGC-PNs that received inhibitory input to offset the excitatory input (n = 4; Fig. 3B), but duration was poorly encoded by those neurons that received little or no inhibitory input from component B(n = 5; Fig. 3A). Neurons that integrated excitatory and inhibitory synaptic input were also able to encode a train of stimuli consisting of a random series of pheromone pulses of various durations and interpulse intervals (n = 5; Fig. 3C).
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FIG. 3.
Some MGC-PNs can also encode stimulus duration with a discrete burst of action potentials. A, top and B, top: examples of intracellular recordings from 2 types of MGC-PNs to the 1:1 blend of pheromone components A and B. The neuron in A exhibited no detectable IPSP at the onset of the response and could not follow a series of 50-ms pulses at an interstimulus interval of 330 ms. In contrast, the neuron in B exhibited a 10.2-mV IPSP and could follow repetitive stimulation up to 10 pulses per s. Each neuron was then challenged with a random presentation of blend pulses ranging from 50 to 500 ms in duration. The duration of the train of action potentials evoked by each odor pulse is plotted as a function of stimulus duration in the graph below each record. A: neuron that exhibited excitatory input and little or no inhibitory input could not discriminate different durations of blend pulses. B: neuron that showed strong inhibitory input along with the excitatory input could encode the duration of blend pulses with great accuracy. C: another neuron that integrated excitatory and inhibitory synaptic input could encode a random sequence of pheromone blend pulses of varied durations and interpulse intervals.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). Wind tunnel studies have also revealed that male M. sexta will not take flight unless the two essential pheromone components are presented simultaneously (Tumlinson et al. 1989), again stressing the importance of blends in controlling behaviors based on olfaction. Behavioral studies combined with in-flight electroantennogram recordings also show conclusively that some moths can respond reiteratively to repeated pulses of pheromone with response latencies <1 s (Vickers and Baker 1994). Although similar behavioral experiments have yet to be performed with M. sexta, we now have evidence that at least some AL output neurons can follow such rapid odor pulses, and the accuracy of frequency coding improves in some neurons if the inputs from the two parallel input pathways are synchronized. These neurons therefore perform a type of coincidence detection in the olfactory system. Although they are not comparing signals from different locations in space, their function is operationally equivalent to the coincidence detectors that are key elements in timing circuits in other systems (Carr 1993; Heiligenberg 1994; Konishi and Volman 1994; Neuweiler 1994; Simmons 1979) in that their response is optimal when they receive simultaneous inputs. These MGC-PNs furthermore perform the olfactory equivalent of contrast enhancement. Through the integration of excitatory and inhibitory synaptic currents that permit rapid fluctuations of the membrane potential above and below spike threshold, these neurons can encode the moment-to-moment changes that occur in the pattern of the odor stimulus as the male moth flies through the pheromone plume. Each synaptic input is mediated by its own input channel, each comprising antennal ORCs tuned to one key pheromone component, and the axons of each channel terminate in a distinct glomerulus in the MGC (Christensen et al. 1995; Hansson et al. 1991; Kaissling et al. 1989). Thus frequency coding in these MGC-PNs depends not only on the coincident activation of two different odor input channels, but also on lateral synaptic interactions between the adjacent glomeruli that receive this information from the two antennal channels. Experiments are under way to investigate possible relations between temporal response properties and dendritic arborizations of individual MGC-PNs (Heinbockel et al. 1994; T. Heinbockel, T. A. Christensen, and J. G. Hildebrand, unpublished observations).
-aminobutyric acid (GABA)-containing interneurons, the periglomerular and granule cells, are believed to be largely responsible for shaping the temporal response patterns of mitral/tufted cells, and thus the output from the bulb (reviewed in Duchamp-Viret and Duchamp 1993). In insects, it appears that excitability in AL output neurons is also regulated largely through the actions of GABAergic local interneurons (Boeckh et al. 1990; Christensen et al. 1993; Hoskins et al. 1986; Waldrop et al. 1987). In M. sexta, several lines of evidence indicate that the IPSP evoked by sex pheromone component B is mediated by GABAergic synaptic input from a population of spiking local interneurons (Christensen et al. 1993; Hoskins et al. 1986; Waldrop et al. 1987). Currently we are exploring the possibility that aminergic modulation of the inhibitory input mediated by GABAergic local interneurons may be an adaptive mechanism for adjusting the temporal filtering characteristics of MGC-PNs in the insect AL (Kloppenberg and Hildebrand 1995; Mercer et al. 1995).
; Murlis et al. 1990), and recent behavioral evidence indicates that spatiotemporal features of a sex pheromone plume may be used by male moths to locate a female moth releasing pheromone (Mafra-Neto and Cardé 1994; Vickers and Baker 1994). In studying the pheromone-processing circuits in the brain of male M. sexta, we have recognized a simple integrative mechanism for filtering this temporal information from a natural, discontinuous odor stimulus. Several recent computational models of MGC circuits offer further insight into how information about odor blends may be processed (Av-Ron 1994; Linster et al. 1993, 1994), and their results agree with the findings presented here. That is, these models can faithfully reproduce many of the physiological response patterns of MGC-PNs, and in particular can predict the effects of altering pheromone component ratios on the temporal response properties of those particular neurons that integrate information from a binary blend like the M. sexta pheromone. Given the remarkable similarities between the odor-driven responses of MGC-PNs and the analogous processing units in the vertebrate olfactory bulb (mitral/tufted cells) (Getchell and Shepherd 1975; Hamilton and Kauer 1988, 1989; Mori 1987; Mori and Shepherd 1994; Wellis et al. 1989; Yokoi et al. 1995), we believe that the coincident activation of two opposing synaptic inputs could represent a general coding strategy for enhancing the discrimination of odor signals in widely divergent species.
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ACKNOWLEDGEMENTS |
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We are very grateful to Dr. Brian Waldrop and T. Heinbockel for many helpful discussions and comments on the manuscript, to Dr. James Tumlinson for supplying purified pheromone components, and to C. Hedgcock, R.B.P., for photographic assistance.
This work was supported by National Institute of Allergy and Infectious Diseases Grant AI-23253 to J. G. Hildebrand.
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FOOTNOTES |
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Address for reprint requests: T. A. Christensen, ARL Div. of Neurobiology, University of Arizona, P.O. Box 210077, Tucson, AZ 85721-0077.
Received 19 July 1996; accepted in final form 3 October 1996.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli.
J. Comp. Physiol. A Sens. Neural Behav. Physiol.
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H. Lei and B. S. Hansson Central Processing of Pulsed Pheromone Signals by Antennal Lobe Neurons in the Male Moth Agrotis segetum J Neurophysiol, March 1, 1999; 81(3): 1113 - 1122. [Abstract] [Full Text] [PDF]
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