Behavioral evidence for chemosensory and thermosensory pathway convergence in the caenorhabditis elegans nervous system.
Keywords: Caenorhabditis elegans, neurobiology, chemosensory, thermosensory.
As organisms interact successfully with their surroundings, certain environmental cues generate specific and appropriate behaviors. Sensory neurons detect environmental changes, encode the information, and pass this information into neural circuits where it is integrated and ultimately produces an appropriate behavioral response. Details of the mechanisms by which this is accomplished have been poorly understood. However, recent studies using the model Caenorhabditis elegans nervous system have begun to shed light on the ways that innate, "hard wired" neural circuits generate predictable behavioral responses (1).
For a number of reasons the nematode Caenorhabditis elegans has become a favored laboratory model for neurobiological studies. It is the only organism for which the entire nervous system, consisting of 302 neurons, has been completely mapped by serial section electron microscopy, elucidating the various chemical synapses and gap junction connections (2). C. elegans also exhibits a simple behavioral repertoire consisting primarily of forward
movements (backward waves), backward movements (reversals), and omega waves, which produce 1800 changes in direction (3, 4). These behavioral elements can be monitored to distinguish between chemical attractants and repellents. Rutherford and Croll (5) found reversal activity to increase in repellent chemicals (D-tryptophan) and to decrease in attractant chemicals (NaCI) making it possible to distinguish between attractant and repellent chemicals by the behaviors they elicit. It was also observed that D-tryptophan had no effect on thermal orientation in a gradient or on is othermal tracking in which a worm moves circularly in a radial gradient at its preferred temperature, suggesting that chemical and thermal stimulation operate through separate, nonconvergent pathways.
Chemosensation in C. elegans exhibits both gustatory and olfactory components associated with the amphid sensilla. Phasmid and inner labial sensilla do not appear to be essential for chemotaxis. Water-soluble chemicals are detected by a group of amphid neurons (ASE, ADF, ASG, ASI, and ASK), in which ciliated endings are exposed to the external environment via the amphid channel and comprise the "gustatory" sensory mechanism of the nematode (6). Another pair of chemosensory amphid neurons (AWA and AWC) does not have exposed dendritic endings and comprise an "olfactory" mechanism sensitive to volatile organic attractants. Similarly, the AWB amphid neuron is part of the olfactory mechanism but senses volatile organic repellents instead (4, 1). The thermosensory neurons, AFD, of the amphids also have no exposed dendritic endings (8). The chemosensory AWA, AWB, and AWC neurons and the thermosensory AFD neurons all show strong connections to the AIY and AIZ interneurons, representing an anatomical convergence betw een olfactory and thermosensory pathways (2, 4).
Laser ablation studies, along with mutant isolation and genetic analysis, have begun to reveal the functions of many of these neurons and their associated circuits (9, 10, 11, 12, 1,13). It has also been demonstrated that interactions exist between chemosensory and thermosensory mechanisms within the C. eiegans nervous system. Dusenberry and Barr (14) tested thermophilic (EH61 and EH71) and cyrophilic (EH65 and EH67) mutants and found them to be abnormal in some of their water-soluble chemical responses suggesting some overlap in chemosensory and thermosensory mechanisms. Komatsu, et al., (9) found that thermotaxis deficient mutants (tax-4) also failed to respond to AWC sensed odorants. Since behavioral and genetic similarities apparently exist between the mechanisms for chemotaxis and thermotaxis, shared cellular and molecular components have been suggested (10). In fact, Mon and Oshima (11) proposed a model neural circuit to explain cryophilic, "down gradient" movement, thermophilic, "up gradient" movement , and isothermal movement where the nematode remains at its culture temperature. Their model demonstrated that the interneurons AIY and AIZ respectively were primarily responsible for "up" and "down" gradient movements. A thermosensory neuron, AFD, inputs directly to AIY, but its cryophilic counterpart, connecting to AIZ, remains unidentified.
Temporal changes in C. elegan's behavioral parameters that occur in response to volatile chemical and/or thermal stimulation can be monitored and quantified through video image capture and computer tracking technology (15). By integrating computer tracking technology with controlled chemosensory and thermosensory neuron stimulation, it is possible to explore the interactions between these two neural pathways as the nematode reacts to changes in these environmental parameters.
MATERIALS AND METHODS
Nematode Culture and Collection
Caenorhabditis elegans, provided by the Caenorhabditis Genetics Center (University of Minnesota, St. Paul, MN 55108), was cultured on NGM plates seeded with a lawn of OP50 Escherichia coli, (16). Worms for testing were removed from the culture plates by washing with deionized water. Since C. elegans chemotaxes strongly to its bacterial food source, recovered nematodes were rinsed 3X in deionized water to remove adherent bacteria prior to testing. Because the nematode reacclimatizes to changed temperature within four hours (17), isolation and testing were completed within one hour of removal from culture temperature. Three culture temperatures were selected: 16[degrees]C, 20[degrees]C and 24[degrees]C, to remain within the temperature viability range of the nematode yet provide a separation of acclimation temperatures. All testing was done at 20[degrees]C ([+ or -]0.5[degrees]C).
Since worms acclimated at all three culture temperatures were tested at 20[degrees]C, the 16[degrees]C and 24[degrees]C worms were thermally stimulated by being tested either above or below their eccritic temperatures. The 20[degrees]C worms were isothermal controls. This technique allowed for assessing responses to various combinations of chemical and thermal stimulation.
Behavioral responses were monitored and quantified by a modification of the technique developed by Dusenberry (15). This procedure allows the simultaneous monitoring of up to 100 individual target subjects each second during the observation interval. Test worms placed on a 2% agar pad within a transparent chamber were illuminated by a low-heat, red LED light source focused by a Fresnel lens so that shadows of the moving worms fell on the focal plane of a CCD video camera. Video output from the camera was captured at one-second intervals by a Power Macintosh computer equipped with a Scion LG-3 image capture board. Computer software tracked each moving worm every second of exposure and recorded the number of subjects moving, the number of reversals of movement direction, total combined movement of all test subjects, and net movement in both Y axis directions. Pixels traversed per second for each subject tracked were summed algebraically to determine net movement for each test group. Positive net movement values showed movement toward the stimulus source (upstream) and negative values reflected movement away (downstream) from the stimulus source.
Knowing that AWA and AWC chemosensory neurons connect strongly with the thermosensory interneurons, AIY and AIZ, this point of convergence was selected for study. Since diacetyl is detected primarily by the AWA amphid neurons and benzaldehyde by the AWC neurons (7), use of these two volatile attractants allowed for the separation of these two chemosensory pathways and the assessment of their interactions with the thermosensory circuits. Aqueous dilutions of these two volatiles were adjusted in sparging bottles to levels previously determined by Bargmann, et al (7) to yield an approximate chemotaxis index with C. elegans of 0.8 + or -]0.1. Diacetyl was tested at a concentration of 1 x [10.sup.-5]M and Benzaldehyde, a weaker stimulus, was diluted to 1 x [10.sup.-2]M. For each experimental assay, medically clean air was passed at a flow rate of 4 ml/s through two sparging bottles; one with stimulus chemical dissolved in water and a control containing only deionized water. Airflows from these two bottles were mat ched at 4 ml/s and alternately passed across the test worms for 50 seconds. Thus a complete chemical stimulation cycle consisted of two 50-second phases alternating between stimulus off and stimulus on. An experiment consisted of 10 complete cycles (pseudoreplicates) repeated with each group of test worms. Pseudoreplicate data were summed algebraically to complete each behavioral assay. Each assay situation was repeated from four to eight times with different, fresh worms (true replicates). Data from true replicate experiments were averaged to establish data points for statistical comparisons of different stimulus situations.
Since the test chamber was approximately 40 ml in volume, a flow rate of 4 ml/s required 10 seconds to completely replace the chamber air each time the stimulus/control flows were switched. Consequently, in data analysis the first 10 seconds of each cycle phase were disregarded in determining the response of the test worms. Reversals and total movement data were consolidated and expressed as a reversal/movement ratio. Based on changes in this ratio, which peaked within 15 seconds after the chamber air was completely replaced, the time interval between 10 and 25 seconds into each phase of the cycle was determined to be the response interval. Normalization of all data was accomplished by dividing all raw data values by the number of subjects moving at each one-second interval of data collection prior to plotting. Means of true replicate data points for each second during this 15-second interval were computed and plotted. Since individual data points among the 15 one second intervals are not independent, regres sion lines were fitted to all data points in each 15 second response interval. The slopes of these lines were used to represent the intensity of response to a given experimental treatment and were compared statistically for significant differences by the procedures described below.
Visual examination of the residuals of the fitted regression equations indicated that the assumption of normality of the residuals was reasonable. Consequently the estimated slopes of the regression equations, [[beta].sub.i], are normally distributed. In testing the equality of slopes from two regression equations, we test the hypotheses [H.sub.o]: [[beta].sub.i] = [[beta].sub.j] versus [H.sub.1]: [[beta].sub.i] [not equal to] [[beta].sub.j]. Because of the normality of the [[beta].sub.i] the appropriate statistic for testing the above hypotheses is the usual t statistic t = [[beta].sub.i]-[[beta].sub.i]/[square root of][SE.sup.2.sub.i]+[SE.sup.2.sub.j], where [SE.sub.i] is the estimated standard error of [[beta].sup.i]. Under the null hypothesis, this test statistic has Student's t distribution with [n.sub.i] + [n.sub.j] - 4 degrees of freedom, where [n.sub.i] and [n.sub.j] are the number of points used in fitting the regression equations. In this case, [n.sub.i] = [n.sub.j ] = 15 for all stimulus conditions (18).
The above test statistic has the usual robustness of the t statistic against departures from normality. When the number of points used to fit the two regression equations is the same, the t statistic is also robust to violations of the requirement of equal error variance in the two regression populations. Because of these properties of the t statistic, we proceeded to test the equality of slopes of two regression equations using the t test with 15 + 15 - 4 = 26 degrees of freedom.
Within each culture temperature-chemical stimulus combination, equality of the slopes for the stimulus on and stimulus off conditions was tested. The null hypothesis Ho: [[beta].sub.on] = [[beta].sub.off] was tested versus [H.sub.1]: [[beta].sub.on] [not equal to] [[beta].sup.off], where [[beta].sub.on] and [[beta].sub.off] represent the slopes of the regression lines for the stimulus on and stimulus off conditions. There were nine such hypothesis tests. If each of the tests was done at the traditional significance level of [alpha] = 0.05, an upper limit for the overall significance level of the analysis consisting of all nine tests is 1 - (0.95) (9) n 0.37. To maintain a significance level of no more than [alpha] = 0.05 for all nine tests, Bonferroni's method was used. In Bonferroni's method, each hypothesis test is conducted using a significance level of [[alpha].sup.*] = 0.05/m, where m is the number of tests being done. In this case, m = 0, and the significance level used for each hypothesis test was [[alpha].sup.*] = 0.05/9 [approximately equal to] 0.0056.
Figure 1 shows data from worms receiving no chemical stimulation in which both sparging bottles contained deionized water. Reversal/movement ratios were virtually flat in both phases of the stimulus cycle, which is typical of no chemical stimulation. Had an attractant been present, worms would have slowed in movement and increased reversal behavior in the stimulus off phase of the cycle increasing the reversal/movement ratio during this phase as they sample their immediate vicinity for detectable volatiles. However, the net movement slopes from the same experiments suggested the existence of a slight thermal gradient as evidenced by the increasingly positive slopes of the 16[degrees]C worms in both phases of the cycle. Apparently, the "upstream" portion of the agar pad was cooler as a possible result of evaporative cooling in the airflow. The warmer acclimated 20[degrees]C and 24[degrees]C worms consistently migrated downstream toward the warmer areas as evidenced by the increasingly negative net movement ov er the response intervals. Unfortunately, the gradient was too slight to be measurable but did not vary significantly between the two phases of the cycle confirming the closely matched flow rates between the two sparging bottles.
The virtually flat slopes of the reversal/movement ratios of all three temperature acclimation groups demonstrated the lack of attraction or repulsion to the experimental conditions during both phases of the cycle. More importantly, these data confirmed the lack of contaminant chemical stimulants in the test system. Statistical comparisons (see Table 1) of the Y-axis movement slopes for each temperature group during the stimulus off and stimulus on phases of the cycles showed no differences. Essentially, these experiments reflected pure thermal responses in the absence of chemical stimulation.
Figure 2 illustrates the responses to the weak attractant, benzaldehyde, in different thermal environments. Reversal/movement ratios showed an increase in the stimulus off phase of the cycle followed by a decrease in the presence of benzaldehyde. Since reversals decreased and movement increased in the presence of an attractant, this data represents a typical response to a chemical attractant. The responses of worms from all three acclimation temperatures were similar in this regard. However, there were important differences in their net Y-axis movements. The 16[degrees]C and 20[degrees]C worms showed positive net movement trends upstream toward the chemical stimulus during the stimulus on phase of the cycle. Although the 24[degrees]C worms detected benzaldehyde as an attractant as evidenced by the reversal/movement ratios, they were apparently unable to orient and move toward the source. Slopes of the 16[degrees]C worm's net Y axis movements were significantly different when the two phases of chemical stimul ation were compared (Table I), whereas, the 20[degrees]C and 24[degrees]C slopes were not different. Since benzaldehyde is a weak attractant, the 20[degrees]C response probably was not strong enough to be significant even though a definite upstream movement was apparent from the data in the presence of the attractant.
Figure 3 depicts the responses to the strong attractant, diacetyl, in different thermal environments. Reversal/movement ratios showed the characteristic pattern for an attractant in which the ratio increased with the stimulus off and declined with the stimulus on. Net Y-axis movements in this instance were much stronger and showed an aberrant response with the 16[degrees]C acclimated worms instead of the 24[degrees]C group that appeared disoriented with benzaldehyde stimulation. Statistical comparisons of the Y-axis slopes were unambiguous, as expected with a strong stimulus like diacetyl. The 20[degrees]C and 24[degrees]C worms moved significantly upstream toward the diacetyl source during the stimulus on phase of the cycle (Table I). However in this case, the 16[degrees]C worms appeared unable to orient toward the stimulus source even though they reacted with reversal behavior as if exposed to a normal attractant. The net Y-axis slopes for the 16[degrees]C worms in the two cycle phases were not statistical ly different, confirming the suppression of Y-axis directional movement in these worms.
Essentially, the combined chemical and thermal stimulation showed different effects with worms of different culture temperatures. Benzaldehyde seemed to neutralize the responses to both temperature and the chemical in 24[degrees]C acclimated worms producing a relatively flat Y-axis response. Diacetyl had the same effect in flattening the Y-axis response curve to both stimuli, but with the 16[degrees]C acclimated worms in this case.
Temperature stimuli elicit different responses in C. elegans depending upon the conditions of exposure. If exposed to a temperature within their viability range for about four hours with adequate nutrition, they become acclimated to that temperature. Such thermally acclimated worms migrate toward this preferred (eccritic) temperature (thermotaxis) in a thermal gradient (17). This acclimation is presumed to involve a neural mechanism rather than a metabolic event since different acclimation temperatures did not affect oxygen consumption (18). Alternatively, exposure to potentially injurious high temperature extremes elicited a thermal avoidance response involving a rapid withdrawal from the noxious temperature source (20). Since mutants defective in the thermosensory pathway neurons AFD, AIY and AIZ still showed normal thermal avoidance responses, the thermal avoidance mechanism was presumed to involve a separate pathway from thermotaxis. Since temperatures employed in this study were within 4[degrees]C of cu lture temperature and well within the viability range for the nematode, the observed responses should not involve thermal avoidance mechanisms.
For purposes of discussion, the terms "up gradient" (thermophilic) and "down gradient" (cryophilic) respectively refer to the neural circuits involved in movement toward warmer or colder temperatures. The designations "upstream" (positive net Y-axis trend) and "downstream" (negative Y-axis trend) refer to Y-axis orientation in the air stream of the test apparatus. For example, 24[degrees]C worms tested at 20[degrees]C move "down stream" away from the air flow by activating "up gradient" pathways. Conversely, 16[degrees]C acclimated worms move "up stream" in the Y-axis by activating "down gradient" circuitry.
Hypothetically, worms receiving simultaneous chemical and thermal stimulation might experience conflicting sensory input and should show ambiguous net Y axis responses. The normal tendency would be to move away from a noxious thermal stimulus or upstream toward an attractant chemical odorant. Since both test chemicals were attractants, the nature of the chemical stimulus should not matter. However, the observed behavioral effects were selective with regard to the pattern of chemical and thermal stimulation applied. Diacetyl neutralized the net Y-axis response only with 16[degrees]C worms and benzaldehyde had the same effect, but only with the 24[degrees]C worms. These two affected temperature groups neither moved away from the temperature stimulus or toward the chemical attractants. It appeared that both chemical and thermal responses were neutralized when applied in this pattern of stimulation.
The AWA and AWC neurons comprise the olfactory sensory receptors for attractant volatile organic compounds. Although there appears to be some redundancy in the chemosensory pathways and some overlapping chemosensory abilities among chemosensory neurons, the AWA neuron expresses the primary receptor for diacetyl and the AWC neuron is the primary sensor for benzaldehyde (7). The gene odr-10 codes for a G-protein coupled seven-transmembrane protein receptor that is specific for diacetyl and is expressed in AWA neurons (21, 12). Benzaldehyde is detected by the AWC neuron and a cyclic nucleotide gated channel appears to be involved in this case as well (9). In the assay apparatus, activation of AWA or AWC by diacetyl or benzaldehyde attractants without marked thermal interference resulted in "upstream" movement in the Y-axis toward the chemical source, an expected response to attractants.
Adding the olfactory AWA and AWC connections described by White, et al., (2) to the model proposed by Mori and Oshima (11) reveals that each of these olfactory neurons synapses with both the up and down gradient thermal pathways (interested readers are referred to these papers for details of circuitry). Thus, either chemical should have the potential to activate both thermal pathways. Additionally, the Mori and Oshima model suggests that the activation of one thermal pathway inhibits the other, preventing conflicting sensory input of purely thermal origin. However, chemical and thermal conflicts in sensory input should theoretically be possible.
The present finding that diacetyl flattens the response curve of 16[degrees]C worms to both chemical and thermal stimulation and that benzaldehyde has a similar effect on 24[degrees]C worms suggests that such conflicts in sensory input do occur. Results also suggest that differences exist within the neuronal circuits involving the AWA and AWC neurons even though both show strong synapses with AIY and AIZ (2). Mori and Oshima (11), using laser ablation and thermotaxis assays, developed a model circuit to explain their observed effects of laser "kills" on thermotaxis and isothermal tracking behavior. Basic to their proposed model is that the AIY and AIZ interneurons are the key points that separate thermophilic from cryophilic behavior. Thus, olfactory and thermosensory pathways appear to converge at this point. Thermal activation of AIY occurs via AFD in an environment that is colder than culture temperature and produces an "up gradient" thermotaxis toward warmer temperatures. Conversely, activation of AIZ oc curs in a situation where the environmental temperature is warmer than culture temperature and results in a "down gradient" thermotaxis toward colder temperatures. AIY, when active, is proposed to inhibit AIZ, either directly or indirectly via RIA, to inactivate the alternate thermotaxis pathway. Through alternate activation of these two neural circuits, C. elegans is presumed to be able to move toward a preferred temperature and remain there isothermally.
Assuming the activation of one thermosensory pathway inhibits the other, our observations may be hypothetically explained as conflicting sensory input between chemical and thermal stimuli acting through convergent pathways. If the "up gradient" pathway were active in 24[degrees]C worms and they were exposed to benzaldehyde via AWC, the blocked "down gradient" could be circumvented by synapses through AIA, AIB and ADF to restore "down gradient" activity. Such a situation could cause conflicting sensory information and neutralize the Y-axis movement. With "down gradient" activation, as with 16[degrees]C worms, exposure to diacetyl could cause "up gradient" activity through synapses with AFD and AIY. However, this would require that "up gradient" pathways not be blocked at AIY. Alternatively, a different pathway may exist around AIY. AWA connects by gap junctions to AIA, AIB and ADF. AIB and ADF bypass AIY to synapse strongly with RIA, RIB and RIM possibly accounting for the conflicting sensory input behavior i n these worms.
Although the neural circuit interactions for chemical and thermal pathways described above are highly speculative, the reported data is interesting enough to merit further study of points of convergence between these two complex pathways.
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Table I Statistical Comparisons of Net Movement Response Slopes During the Off and On Phases of Chemical Stimulation Cycles No Stimulus Benzaldehyde Off On P Off On P 16[degrees]C 0.1103 0.0555 0.0649 -0.0935 0.1974 <0.0001 20[degrees]C -0.1492 -0.0488 0.1527 -0.0268 0.1090 0.6328 24[degrees]C -0.1562 -0.0795 0.2471 0.0681 0.0176 0.4373 Diacetyl Off On P 16[degrees]C -0.0084 -0.1105 0.0599 20[degrees]C -0.4115 0.3721 <0.0001 24[degrees]C -0.3584 0.2484 <0.0001
This work was supported by a Faculty Development Grant and a Mentor-Protege Grant from the Georgia Institute of Technology and Kennesaw State University, respectively.
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Bowman O. Davis, Jr. *
* Kennesaw State University, Department of Biological and Physical Sciences, 1000 Chastain Road, Kennesaw, GA 30144-5591; E-mail: email@example.com
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|Author:||Davis, Bowman O., Jr.; VanBrackle, Lewis; Pittard, Darren|
|Publication:||Georgia Journal of Science|
|Date:||Jun 22, 2002|
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