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The Journal of Neuroscience, September 15, 2002, 22(18):8324-8333
Gustatory Processing in Thoracic Local Circuits of Locusts
Stephen M. Rogers and Philip L. Newland Centre for Neuroscience, School of Biological Sciences, University of Southampton, Southampton SO16 7PX, United Kingdom
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Recent reviews highlight a longstanding controversy about how different taste qualities are coded in the CNS. To address this issue, we have analyzed gustatory coding in the relatively simple and accessible nervous system of the locust, in which neural responses and gustatory elicited behavior are readily comparable. The intracellular responses of a population of spiking local interneurons in the metathoracic ganglion that receive monosynaptic inputs from chemosensory afferents were analyzed in response to stimulation with droplets of four behaviorally relevant chemicals: sodium chloride, sucrose, lysine glutamate, and nicotine hydrogen tartrate. There was a significant positive correlation between chemical concentration and response duration and the number of spikes evoked in 81% of interneurons sampled. The threshold of sensitivity to different chemicals varied but was consistent between all interneurons tested, being most sensitive to nicotine hydrogen tartrate and least sensitive to sucrose. Each interneuron responded similarly to specific chemicals at single concentrations. Interneurons that responded phasically to one chemical responded similarly to others, whereas interneurons that responded phasotonically to one stimulus also did so to others. Hindleg motor neurons also responded in a concentration-dependent manner to all test chemicals. Therefore, we found no interneurons or motor neurons that responded only to specific chemicals. We discuss the responses of the local circuit neurons in relation to the known chemically evoked behavioral responses of locusts and suggest that the aversiveness of a chemical, rather than its identity, is encoded directly in the local circuits.
Key words: chemosensory processing; taste; local circuits; spiking local interneuron; motor neuron; withdrawal reflex; grasshopper
INTRODUCTION
The sense of taste has a vital role in the selection of appropriate foods, in the decision to ingest food, and in regulating dietary intake (Scott and Verhagen, 2000
; Spector, 2000
Studies at peripheral and central levels have shown that gustatory neurons in general lack strong stimulus specificity (Pfaffmann, 1959
In vertebrates, neurons in the nucleus of the solitary tract (NST) are broadly tuned to more than one stimulus quality and represent the initial stage in the central coding and processing of taste signals (Smith and Travers, 1979
MATERIALS AND METHODS
Adult desert locusts, Schistocerca gregaria (Forskål), of both sexes were taken from a colony maintained at the University of Southampton. Animals were secured ventral side uppermost in modeling clay to prevent movement. The right hindleg was positioned laterally and restrained securely with the anterior surface uppermost and accessible. The mesothoracic and metathoracic ganglia were exposed by removing a window of cuticle in the ventral thorax and overlying air sacs. The abdominal connectives were severed, and a small platform, made from a wax-coated chloridated silver wire, was inserted underneath the ganglia for support. In most experiments, all peripheral nerves were cut except nerve 5 of the metathoracic ganglion that contains axons of sensory neurons innervating receptors on and in the hindleg. The ganglion sheath was softened by direct application of a protease (Sigma type XIV) for 45-60 sec, and thereafter the thorax was continuously superperfused with locust saline at 20-25°C. A more detailed description of this procedure has been described by Burrows et al. (1989)
Recording. Intracellular recordings were made from the somata of leg motor neurons and midline spiking local interneurons of local circuits producing and controlling hindleg movements (Fig. 1A) using glass microelectrodes filled with 2 M potassium acetate and with direct current resistance of 50-80 M
. Recordings were made with either an Axoclamp 2A amplifier (Axon Instruments, Foster City, CA) or an amplifier designed and built at the University of Cambridge (Cambridge, UK). For motor neuron recordings, a pair of insulated 50 µm copper wires, exposed only at their tips, was implanted in the tibial extensor muscle of the hindleg and used to stimulate the muscle to induce antidromic spikes in the fast extensor tibia motor neuron (FETi). Flexor tibia motor neurons, which occur in three groups, each consisting of a fast, intermediate, and slow neuron, were identified according to a number of criteria as detailed by Burrows et al. (1989)
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Figure 1. Spiking local interneurons and hindleg motor neurons receive convergent mechanosensory and chemosensory inputs. A, Summary of the basic organization of chemosensory and mechanosensory processing pathways in local circuits. Cell types recorded are shown in black. B, Simultaneous dual recording of a midline spiking local interneuron and a posterior flexor tibia motor neuron. Gently deflecting receptors on a hindleg with a paint brush elicited a sustained depolarization and spikes in an interneuron and depolarizing potentials in a flexor tibia motor neuron. C, Applying a droplet of 100 mM NaCl to the leg also elicited a sustained depolarization and spikes in the same interneuron and a long-lasting depolarization in the same flexor tibia motor neuron. D, A droplet of water applied to the same site on the hindleg evoked briefer depolarizing responses in both neurons. All recordings are from the same pair of neurons. Arrows indicate onset of droplets. In this and subsequent figures of intracellular recordings, the dotted lines represent the membrane potential before stimulation. Flexor, Flexor tibia motor neuron; interneuron, spiking local interneuron of a ventral midline population.
Test protocol. Chemical stimuli were applied as droplets of aqueous solutions to taste receptors, or basiconic sensilla, with Pasteur pipettes in a region of the leg identified as having the strongest mechanosensory input onto sampled spiking local interneurons. It has been established previously that the mechanosensory and chemosensory receptive fields are coincident for most spiking local interneurons (Newland, 1999
The concentration ranges used varied for each chemical and were determined from the data obtained by Rogers and Newland (2000)
The number of spikes elicited, the duration of the depolarization/hyperpolarization, and its peak amplitude in response to chemical stimulation were determined for all neural responses. The duration of response was calculated as the time from the onset of depolarization/hyperpolarization to a recovery of two-thirds the peak amplitude of depolarization/hyperpolarization.
Chemosensory receptors within the basiconic sensilla on a leg adapt rapidly to repeated stimulation with most chemicals (White and Chapman, 1990
RESULTS
Responses of spiking local interneurons to gustatory stimulation
Local circuits producing and controlling movements of the leg of locusts have been well studied, and we now know much about their general organization (Fig. 1A). Spiking local interneurons from the midline population receive convergent mechanosensory and chemosensory inputs from receptors on a hindleg (Fig. 1A). Touching hairs and basiconic sensilla with a fine brush evoked depolarizations and spikes in spiking local interneurons (Fig. 1B). The majority of spiking local interneurons that received exteroceptive inputs also received chemosensory inputs (see below). For example, a droplet of 100 mM NaCl applied to the hindleg evoked a long-lasting depolarization and spikes in the same interneuron that received mechanosensory inputs (Fig. 1C). The duration of the response to droplets containing chemicals was always longer than to droplets containing water only (Fig. 1C,D). Activity in the spiking local interneuron was rapidly followed by activity in a flexor tibia motor neuron, the amplitude of which paralleled that of inputs to the spiking local interneuron for both mechanosensory (Fig. 1B) and chemosensory (Fig. 1C) stimulation.
Concentration-dependent responses
Forty-five spiking local interneurons were tested with one of four test chemicals, each in a range of concentrations. Droplets of chemicals were applied to regions of a hindleg that were found to provide the strongest mechanosensory input to the recorded local interneuron. We measured the duration, amplitude, and number of spikes evoked in an interneuron by chemosensory stimulation. Thirty-six of the interneurons showed a statistically significant increase in the strength of the response with increasing chemical concentration (Table 1; Figs. 2, 3, and 4). The response characteristics most frequently correlated with chemical concentration were the duration of depolarization and the number of spikes evoked by chemical stimulation (Table 1). Response amplitude, however, was less reliably correlated with chemical concentration, reflecting the difficulty in measuring the amplitude of the underlying depolarization in a spiking neuron and vulnerability to variation in recording quality over the course of the experiments.
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Table 1. Correlation coefficients of chemical concentration and the duration, amplitude, and spike frequency of response for midline spiking local interneurons tested with four different chemicals
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Figure 2. Responses of midline spiking local interneurons to chemosensory stimulation. A, Responses to NaCl. B, Responses to sucrose. C, Responses to NHT. D, Responses to lysine glutamate. Recordings from four different spiking local interneurons showing their responses to repeated applications of increasing concentrations of the four test chemicals. The greater the chemical concentration, the greater the response in an interneuron. Chemical droplets were applied once every 2 min in an ascending concentration series; each application was followed by water, and the entire sequence was repeated.
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Figure 3. Relationship between chemical concentration and response in interneurons. Summaries of the mean duration of depolarization evoked in response to a concentration series of four test chemicals are shown. A, Responses to NaCl. B, Responses to sucrose. C, Responses to NHT. D, Responses to lysine glutamate. In general, the greater the concentration of a test chemical, the greater the duration of response elicited in an interneuron. Each line represents data from a different interneuron, with solid lines indicating significant correlations. Data detailing the number of droplets applied and the significance of the correlations between concentration and duration of response are given for each interneuron in Table 1. Arrows indicate responses to water alone.
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Figure 4. Relationship between chemical concentration and interneuron spike number. Summaries of the number of spikes evoked by different concentrations of the test chemicals applied to the leg are shown. A, Responses to NaCl. B, Responses to sucrose. C, Responses to NHT. D, Responses to lysine glutamate. Each line represents data from a different interneuron, with solid lines indicating significant correlations. In general, the greater the concentration of a chemical, the greater number of spikes evoked in an interneuron. Arrows indicate responses to water alone. Neuron identities are the same as in Figure 3 and Table 1.
Ten of 13 spiking local interneurons tested with droplets of NaCl showed statistically significant correlations (Spearman's
) between the concentration of the chemical in the droplet and the duration (Figs. 2A, 3A) and/or the number of spikes (Fig. 4A) evoked in response to the stimulation (Table 1). Another 13 spiking local interneurons were tested with sucrose, and of these 11 showed significant correlations between concentration and neural response, either duration and/or the number of spikes evoked (Table 1; Figs. 2B, 3B, 4B). All eight neurons tested with NHT (Table 1; Figs. 2C, 3C, 4C) and 7 of 11 neurons tested with lysine glutamate (Table 1; Figs. 2D, 3D, 4D) had responses that were significantly correlated with chemical concentration. We found no neurons exhibiting significantly smaller responses with increasing concentration for any of the test chemicals. Moreover, there were no significant correlations between interneuron response and the pH of the test chemicals.
The responses of individual spiking local interneurons were clearly dose dependent, but there was considerable variation in their absolute excitability. This is reflected in the control response to water, in which the duration of the depolarization after stimulation of the leg ranged from ~0.1 to 1 sec or from 0.2 to >5 sec for the highest concentrations of stimulating chemicals (Fig. 3). This variability is clearly seen in the representative traces of recordings from interneurons shown in Figure 2. The responses of the interneuron in Figure 2B were very short to all droplets but nevertheless increased in amplitude with chemical concentration, whereas the interneuron in Figure 2D exhibited considerably more prolonged responses. The interneurons shown in Figure 2A and C are typical of interneurons with response durations intermediate to these two extremes. The chemical used had no consistent effect on excitability; responses ranging from extremely rapid to long lasting were found in interneurons tested with any one of the four chemicals (Fig. 3).
In summary, 81% of spiking local interneurons tested with one of the four test chemicals showed a significant relationship between chemical concentration and duration of response, which varied from phasic to phasotonic.
Evidence for the convergence of chemosensory inputs onto spiking local interneurons
Many studies have shown that the different sensory neurons within a single basiconic sensillum encode a wide range of different chemicals (Blaney, 1975
Our results show that there is a high probability of any sampled spiking local interneuron responding in a dose-dependent manner to increasing concentrations of any of the test chemicals. This suggests that each of these interneurons may be sensitive to a large number of different chemical stimuli. It is not clear, however, whether an interneuron giving long-lasting phasotonic responses to one chemical concentration series would respond similarly to a different test chemical or whether it could respond more phasically. If this were so, different chemical identities could be encoded in the ensemble response of several different neurons. To test whether individual interneurons showed different response characteristics to different chemicals, experiments were performed on spiking local interneurons in which the leg was tested with single concentrations of three different chemicals and water. To balance between the need to sample several different chemicals and to ensure that each chemical could be applied repeatedly during the course of a single recording, not all of the test chemicals were used. Two solutions, water and 250 mM sucrose, were chosen because they led to comparatively weak responses and two more, 250 mM NaCl and 5 mM NHT, were chosen because they evoked relatively strong responses (Figs. 2, 3). Thirteen interneurons were tested repeatedly with each of these solutions. Statistically significant differences in response duration were found in 8 of the 13 interneurons (Kruskal-Wallis tests; significance taken at p < 0.05) (Fig. 5A). For each interneuron, the responses to 250 mM NaCl and 5 mM NHT were stronger than to 250 mM sucrose and water; there were no sugar-best interneurons (Fig. 5A). As with the previous experiments, there were considerable differences in the absolute excitability of different recorded neurons, but we found that interneurons that responded phasically to 250 mM NaCl also did so to 5 mM NHT and similarly when interneurons that responded phasotonically to one stimulus also did so to the other (Fig. 5A,B). The relative strength of response correlates with the response expected to particular chemicals based on concentration series experiments (Fig. 3). Whether the interneurons show a concentration-dependent response or an apparent sensitivity to particular chemicals, however, depends entirely on experimental design, because the actual response of any one of the interneurons depends on both chemical concentration (Fig. 3) and identity (Fig. 5).
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Figure 5. Individual spiking local interneurons respond to stimulation with different chemicals. The response characteristics of different local interneurons were all similar when tested with different chemicals at fixed concentrations. Neurons were repeatedly tested with single concentrations of four different chemicals at 2 min intervals. A, In experiments where significant differences in response duration occurred, interneurons always responded most strongly to 5 mM NHT and 250 mM NaCl than to 250 mM sucrose and water. Each symbol/line represents data from a different interneuron. B, Typical recordings of the responses obtained during an experiment showing the longer-duration responses to NHT and NaCl. Five responses to each test chemical are superimposed. Note the consistency of the responses to each test chemical.
Additional evidence that individual interneurons respond in a similar manner to different chemicals of similar behavioral effectiveness is shown in Figure 6, in which a spiking local interneuron responded in a similar phasic manner to a concentration series of both NaCl and sucrose.
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Figure 6. Responses of spiking local interneurons to concentration series of two different chemicals. For both NaCl and sucrose, increasing the test concentration resulted in an increase in response duration. Three traces are superimposed for each chemical concentration. The durations of the response for any test concentration were similar.
In summary, the results suggest that spiking local interneurons in the midline population receive inputs from chemosensory neurons sensitive to many, if not all, test chemicals, and that the response durations of these neurons are a function of both chemical concentration and identity. The data suggest that any individual interneuron will respond with similar relative duration to an input of similar behavioral effectiveness (Rogers and Newland, 2000
Responses of leg motor neurons to gustatory stimulation
The responses of flexor tibia motor neurons resembled those of spiking local interneurons to the same four test chemicals. The amplitude and duration of responses in flexor tibia neurons after stimulation of the hind tibia and tarsus with droplets of chemical increased with concentration for all of the four test chemicals (Figs. 7A-D, 8A-D). The mean duration of depolarization increased from ~200 msec after stimulation with water to 600-750 msec after stimulation with 2000 mM sucrose or 250 mM NaCl (Fig. 8). Flexor motor neurons occur in three distinct groups, each containing slow, intermediate, and fast members (Burrows, 1996
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Figure 7. Responses of flexor tibia motor neurons to chemosensory stimulation. Recording from a single posterior flexor tibia motor neuron showing responses to repeated applications of concentration series of each test chemical. A, Responses to NaCl. B, Responses to sucrose. C, Responses to NHT. D, Responses to lysine glutamate. The responses of the flexor tibia motor neuron showed a dose-dependent relationship with chemical concentration, with higher chemical concentrations evoking larger responses in the motor neuron. Droplets of chemical solutions were applied to the dorsal tibia and tarsus in ascending concentration at 3 min intervals. All recordings are from the same motor neuron tested with each chemical concentration at least five times. Three traces at each concentration are superimposed.
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Figure 8. Mean dose-response relationships of flexor tibia motor neurons. A, Responses to NaCl. B, Responses to sucrose. C, Responses to NHT. D, Responses to lysine glutamate. Mean ± SEM response durations of flexor tibia motor neurons to concentration series of each of the test chemicals are shown. Response duration increased with higher concentrations of each test chemical. Data are from nine recordings each of motor neurons tested with NaCl and sucrose, six tested with NHT, and four tested with lysine glutamate. Arrows indicate responses to water alone.
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Figure 9. Chemosensitivity of flexor tibia motor neurons. All flexor tibia motor neurons tested in the three motor pools responded in a similar dose-dependent manner. Paired simultaneous recording of flexor tibia motor neurons showed responses to ascending concentrations of NaCl and NHT. A, A motor neuron from each of the lateral and posterior groups responds in a similar manner to each concentration of NaCl. B, The fast and slow flexor tibia motor neurons of the posterior group respond in a similar manner to a concentration series of NHT. Three traces, one at each concentration, are superimposed. Arrows indicate responses to the concentrations shown.
Other motor neurons controlling leg movement also exhibited dose-dependent responses after stimulation of basiconic sensilla on the leg with chemical solutions. The fast extensor tibia was depolarized after applications of droplets to the distal dorsal tibia (n = 3 animals), the duration and amplitude of which increased with greater concentrations of NaCl (Fig. 10A). Compared with flexor tibia motor neurons, however, the depolarizations were both smaller and of shorter duration. For example, the duration of the response to 100 mM NaCl lasted for only 166 ± 15.9 msec (mean and SEM) compared with 640 ± 60 msec for the flexor tibia motor neurons. The slow depressor tarsus motor neuron, which receives inhibitory inputs from midline spiking local interneurons, was hyperpolarized after stimulation of the ventral tibia with droplets containing NaCl (n = 4) (Fig. 10B,C). As with the flexor and extensor motor neurons, the duration of the response increased with increasing NaCl concentration.
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Figure 10. Chemosensory responses of other hindleg motor neurons. A, Intracellular recording from a FETi showing superimposed traces of responses of increasing duration to higher concentrations of NaCl. Three traces at each concentration are superimposed. B, C, Paired recording of a lateral flexor tibia and the slow depressor tarsus motor neuron. Both neurons display longer-duration responses to the higher concentration of NaCl (C), but in this case, the depressor tarsus motor neuron is hyperpolarized by the chemosensory input.
DISCUSSION
Both spiking local interneurons and motor neurons receive synaptic inputs during stimulation with five chemicals that represent nutrient through to toxic qualities, but there is a consistent variation in the sensitivity of these neurons to the different chemicals. The duration of these inputs is significantly correlated with chemical concentration for neurons tested with any one chemical and is sufficiently large to give rise to action potentials whose frequencies are also related to chemical concentration and identity.
Overall, 81% of spiking local interneurons tested with one of the test chemicals showed a significant correlation between concentration and response. The high probability of any local interneuron receiving a chemosensory input from any one of the different test chemicals suggests that there is a convergence of a large number of taste qualities onto the same interneurons, either from many sensory neurons responding to a range of chemical qualities or from fewer, more broadly tuned sensory neurons. In addition, interneurons that responded phasically to one chemical responded phasically to all others tested, whereas interneurons that responded phasotonically to one chemical also did so to others. Although members of the same population of spiking local interneurons differed in their somatosensory receptive fields (Burrows and Siegler, 1984
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Figure 11. The response durations of spiking local interneurons correspond closely with the behavioral effectiveness of different chemical stimuli at different concentrations. The filled symbols show the mean ± SEM response durations (left ordinate) of spiking local interneurons to each of the test chemical stimuli at different concentrations (abscissa). Data were normalized so as to give the same mean response to water to minimize the variability associated with the different phasotonic response characteristics of individual neurons (Fig. 2). The behavioral effectiveness (right ordinate), as measured by the frequency of locusts withdrawing their legs from droplets of chemical stimuli at different concentrations, are shown by the open symbols (mean ± SEM) (data from Rogers and Newland, 2000
Locust chemosensory afferents appear to lack a strict segregation into distinct classes of chemical sensitivity (Blaney, 1975
Spiking local interneurons are broadly tuned to many different chemical stimuli in a manner consistent with across-fiber pattern coding. Rodent peripheral taste fibers that converge on brainstem neurons in the NST are similarly broadly tuned and lack a high degree of stimulus specificity (Smith and Travers, 1979
These results suggest that local circuits of the metathoracic ganglion may not have separate chemosensory processing pathways for different chemicals or classes of chemical. How then could this system, broadly tuned but with all neurons apparently having the same range of sensitivity, be used to make effective behavioral decisions about chemicals in the environment? Clearly this kind of coding is inconsistent with a system that is concerned with establishing chemical identity, because a similar strength of response in an interneuron can be evoked by a weak solution of NaCl or a strong solution of sucrose. Instead, our results suggest that the duration of response to different chemicals provides a direct measure of a perceived quality, that of aversiveness, because the relative size of the neuronal response of spiking local interneurons and motor neurons correlates strongly with behavioral withdrawal responses (Fig. 11). Our previous experiments (Rogers and Newland, 2000
It is readily understandable why locusts should be highly sensitive to and withdraw their legs from the toxic secondary plant compound NHT, but their aversion to high concentrations of nutrient chemicals is also consistent with recent models of the role of taste in dietary regulation in locusts and other animals (Simpson and Raubenheimer, 1996
FOOTNOTES Received April 25, 2002; revised June 26, 2002; accepted July 8, 2002.
This work was supported by an Advanced Fellowship from the Biotechnology and Biological Sciences Research Council (Swindon, UK) (P.L.N.). We thank Dr. Hans Schuppe for numerous discussions about this work and Tom Matheson, David Parker, and Hans Schuppe for their helpful comments on this manuscript.
Correspondence should be addressed to P. L. Newland, Centre for Neuroscience, School of Biological Sciences, Biomedical Sciences Building, University of Southampton, Bassett Crescent East, Southampton SO16 7PX, UK. E-mail: pln{at}soton.ac.uk.
S. M. Rogers' present address: Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.
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