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TRANSLATIONAL PHYSIOLOGY
Department of Neurobiology and Behavioral Sciences, Faculty of Life Sciences, University of Vienna, Vienna, Austria
Submitted 27 February 2006; accepted in final form 25 April 2006
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ABSTRACT |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Caterina and Montell 2005; Cesare et al. 1999; Clapham 2002, 2003; Lee and Caterina 2005; McKemy et al. 2002; Moran et al. 2004; Patapoutain et al. 2003; Voets et al. 2004).
The challenge is to understand the steps interposed between the marked temperature sensitivity of the opening and closing of the TRP cation channel family and the stream of action potentials transmitting temperature information. Extracellular recordings from intact thermoreceptor cells in various vertebrates, insects, ticks, and a spider have shown that the discharge rate peaks when temperature changes. Thereafter, it settles to a level of activity appropriate for the stationary temperature and persists even as the rate of temperature changes approaches zero (Altner and Loftus 1985; Hensel 1974, 1981; Kenshalo 1976; Loftus 1978; Spray 1986; Tichy and Gingl 2001). The continuous discharge reflects the level and duration of the stationary temperature, a characteristic feature of tonic activity. A salient feature of this continuous, tonic response is the regularity of successive intervals obtained in spike trains early in the experimental run and any time thereafter, even when the stimulus temperature is kept constant for periods of >1 h (Hensel and Zotterman 1951; Tichy and Loftus 1987). The incessant nature of the spike activity after reaching a thermal steady state suggests some intrinsic membrane properties to maintain excitation after reaching thermal equilibrium.
Compared with the intact thermoreceptor cells, a continuous tonic discharge at stationary temperatures has not been found in ganglion cultures from mammalian thermosensory neurons. Action potentials occurred only when the temperature was changed. In the cultured neurons of the trigeminal ganglia of snakes innervating the temperature sensors known as pit organs (Pappas et al. 2004), it was even not possible to record action potentials during temperature changes, although in intact preparation action potentials can be elicited by changes in temperature. Pappas et al. supposed that either the rate of temperature change presented to the cultured neurons was too slow to generate action potentials, or that the density of ion channels responsible for temperature detection was not sufficient to produce a depolarization of the membrane potential large enough to elicit action potentials. They also considered the possibility that the role of the molecular events of the transducing process is not to produce fast enough and robust enough depolarization for generating action potentials, but instead modulate an ongoing discharge.
The mechanism by which the continuous discharge of thermoreceptor cells is maintained remains unclear. This paper describes experiments addressing intrinsic membrane properties that underly the generation of the continuous discharge, specifically on the intact warm cells associated with the tiny, air-filled capsule of tarsal organs of the wandering spider Cupiennius salei (Anton and Tichy 1994). Loose-patch recordings revealed that the warm cells persisted in continuous discharge when the capsule was blocked, but in this case, the modulating effect of temperature changes was strongly reduced. Thus the incessant discharge is truly intrinsic to the warm cell and does not require sensory input, suggesting that these cells are their own pacemakers (Bennett et al. 2000; Bond et al. 2005; Feigenspan et al. 1998; Häusser et al. 2004; Ramirez et al. 2004).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Adult female wandering spiders (C. salei Keys., Ctenidae) with a body length of 3–3.5 cm and a leg span of 10–12 cm were used in this study.
Location and structure of the tarsal organ of the spider
The tarsal organ is located on the dorsal side on the tarsus of all walking legs and pedipalps and forms an air-filled capsule in the cuticle (Fig. 1, A and C). This capsule was identified based on its appearance. When the surface hairs were gently removed and the cuticle was viewed from a sharp angle to the light source, the stumps of the removed hairs were visible as dark points on a brick-brown surface. The capsule, on the other hand, appeared as a bright point somewhat larger than the neighboring stumps (Fig. 1A). Histological examinations indicated that the lumen of the capsule (long axis, 18 µm; depth, 12 µm) is connected to the outside by a small elliptical aperture (4 x 7 µm; Fig. 1, B and D). The warm cells are compartmentalized in seven nipple-shaped sensilla that are located on the floor of the capsule and face the aperture. Each sensillum has a single pore at the tip (diameter, 0.7 µm), thus providing access of the sensillum lumen to the external environment. Quite significantly, the dendrites of the warm cells reach right up the lumen to the apical pore (Fig. 1E; for details see Anton and Tichy 1994). Six of the seven sensilla are innervated by three sensory cells, and one by just two cells (Anton and Tichy 1994). Their somata are gathered into a small cluster 40–50 µm beneath the cuticular surface and proximally 70–80 µm from the cavity (Fig. 1, B, D, F, and G). The sensory cells and dendrites traced in microscopic sections are enclosed and surrounded by several accessory cells and covered by a basement membrane (Fig. 1, B and G).
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A leg was autotomized at the coxal-trochanteral joint and placed in a dissecting dish containing Cupiennius saline (223 mM NaCl, 6.8 mM KCL, 8 mM CaCl2, 5.1 mM MgCl2, 10 mM HEPES, pH 7.8; Höger et al. 1997). The tarsus was cut off with a razor blade. Removal of the surface hairs exposed the capsule of the tarsal organ (Fig. 1B). A concave piece of the dorsal cuticle containing the tarsal organ was dissected from the tarsus and pinned dorsal-side-down in the Sylgard-lined recording dish. The preparation was covered by Cupiennius saline. Outlines of the sensory cells associated with the tarsal organ were visible as fusiform structures when bright illumination was provided from above.
Blocking of the sensory input
To study the sensory input and the accompanying discharge of the warm cell in an uncomplicated form, the receptive terminals were either destroyed by piercing the capsule of the tarsal organ with a fine needle or they were poisoned with the cytotoxic Epoxy glue (cyanoacrylates; Loctite). A droplet of Epoxy was picked up by a needle and put onto the opening of the capsule of the tarsal organ. Through capillary action, it penetrated into the lumen of the capsule and solidified almost instantly. Usually, we used this second method of blocking the receptive terminals to show the dependence of the discharge on temperature stimulation.
Recordings
Intracellular recordings were accomplished by means of quartz glass microelectrodes, pulled with a laser-driven horizontal puller (P-2000, Sutter Instruments) and filled with 3 M KCl. Electrode resistances as measured within the bath solution were between 25 and 80 M
. Loose-patch electrodes were pulled from borosilicate glass. Their tips were broken to openings in excess of 50 µm and fire-polished. The resistance was <1 M when filled with spider saline. A silver wire was placed in the microelectrode to improve its performance.
The sensory cells associated with the tarsal organ were identified visually with a Wild M8 dissecting microscope. The microelectrodes were lowered onto the somata of selected cells by a micromanipulator (Leitz, Wetzlar, Germany). A buzzer or gentle tapping of the electrode holder was used to penetrate the cell membrane for intracellular recordings. The action potentials were amplified and band-pass filtered (SEC-05 amplifier, NPI Electronic; Tamm, Germany; Heinecke amplifier, MPI Seewiesen, Germany), passed through a 1401 plus A/D converter (Cambridge Electronic Design) and recorded on-line with the electrical and temperature stimuli on the hard disk of the computer for off-line analysis using Spike 2. Running averages of three consecutive 1-s periods were taken to measure impulse frequency. In a triplet, the mean values of impulse frequency drew on the measured values occurring 1 s before and after them and thereby smoothed the effects of small fluctuations.
Temperature stimulation
The bath solution, flowing from a reservoir to the recording dish, was chosen as stimulus medium. It seemed the most effective way of producing constant temperatures in sensilla located at the floor of an air-filled capsule and thereby protected from contact with the substrate. Bath temperature was measured with a precision of 0.05°C by a small, coated thermistor (Betatherm TP 2802, Galway, Ireland) positioned just at the tarsus. Temperature was termed constant when measurable changes failed to develop in the course of 1 min. Sometimes drift was observed at 0.1°C in 5 min. No systematic attempt was made to determine whether such low rates of temperature change affect the discharge rate of the warm cells. The warm cell definitely reacts to rates of temperature change in the order of 0.01°C/s (Ehn and Tichy 1996), but this is 10 times faster than 0.1°C in 5 min. Changes in stimulus temperature were induced by changing the temperature of the fresh solution flowing into the recording dish. The temperature change at the preparation was relatively slow, between 0.025 and 0.05°C/s.
It should be noted that temperature measurements apply directly to the thermistor, less directly to the bath solution in which it is located, and still less directly to the sensory cells and their receptive terminals. The possibility of assigning instantaneous temperature values to sensory cells or even the bath solution exists when temperature is changing only because the rate of change during these experiments was so slow. Because of these low rates of change, the temperature of both the thermistor and the sensory cells can be considered as locked to that of the bath solution.
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RESULTS |
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50-mV amplitude occurred without electrical stimulation. When injecting a 50-ms current pulse, the frequency of the action potentials increased. Unfortunately, the continuous discharge of action potentials soon disappeared. Although the intracellular recordings were not lost and the cells remained responsive to current pulses, the standard technique of cell penetration (Gingl and French 2003; Gingl et al. 2004) prevented an intracellular study of the continuous discharge. To this end, we used the extracellular loose-patch recording technique. Intact terminal region: responses to stationary temperatures
A microelectrode placed onto the somata of the sensory cells (Fig. 1F) recorded the continuous discharge of single sensory cells (Fig. 2A). Ninety cells (40%) were characterized as warm cells; their discharge rate was increased by warming and decreased by cooling. In 135 (60%) cells, the stationary activity could not be altered by changing temperature. This last category may have included hygroreceptive cells that occur together with the warm cells in the tarsal organ (Ehn and Tichy 1994, 1996).
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Forty-two cells were tested in four or five different overlapping temperature segments of the total temperature range (20–33°C). In nine of these cells, the segment was 6°C and the spacing between stationary temperatures was just >1.5°C (Fig. 2E). This separation was large enough for a tendency to manifest itself in the course of a segment, yet small enough to render very low the probability of a significant but unobserved dip in the general course of the function. The higher values of the tonic frequency were clearly associated with the higher temperatures. The pooled data in Fig. 2E show that impulse frequency based on a 1-s period at the end of the 4-min stimulus rose linearly with increasing values of stationary temperature. The relatively low value of r (0.82), however, does not reflect the deviation of individual points from the regression lines of the individual cells as it does the variation in the slopes of these regression lines. The average slope for a sample of nine warm cells, indicating the mean differential sensitivity to stationary temperature, was 1.1 imp/s/°C. To yield an average rise in tonic impulse frequency by 1 imp/s, stationary temperature must be increased by 0.9°C.
The mean differential sensitivity to stationary temperature described in a previous study (Ehn and Tichy 1996) is almost identical with that found in this study (i.e., 0.8 vs. 1.1 imp/s/°C here). A large difference in sensitivity could raise doubt as to the validity of both the recording and the stimulation methods. Another similarity in the reactions obtained in the two studies is the striking regularity of the discharge throughout the temperature range. A comparison of the interval histograms indicates that with decreasing temperature and discharge rate the mean variance of intervals increased (Fig. 2F). However, there was no indication that the intervals vary in a random manner.
Intact terminal region: lack of responses caused by change in electrode position
The continuous, tonic discharge obtained when contact was made with the somata of the warm cells was never observed when the micropipette was placed onto the terminal region (Fig. 2D). The tonic response resumed, however, on repositioning the micropipette onto the somata. It is therefore extremely unlikely that the tonic discharge originates at the terminal region of the warm cell. All 42 warm cells reacted similarly.
The lack of action potentials from the input region indicates that the warm cell contains two separate parts: one at the distal terminals and specialized for transduction and the other somewhat proximally and endowed with the mechanisms of action potential generation. The question of geometric segregation is important because this study focused on determining whether the warm cell persists in tonic discharge independently from sensory input. If the two processes—transduction and action-potential generation—do coexist at the same membrane patch, the terminal membrane patch could not be blocked by applying the poisonous Epoxy. The process involved in generating action potentials will then be poisoned too.
Blocked terminal region: responses are not affected by temperature stimulation
To block the transduction process, a droplet of Epoxy was put onto the opening of the capsule of the tarsal organ. Under this condition, a continuous discharge of single warm cells was recorded with a micropipette placed onto the somata (Fig. 3A). No warm cell changed its discharge rate during a temperature change to an extent that was sufficient to be interpreted as a response. An obvious explanation for this observation is that the discharge persists independently of temperature input. Another interpretation is that none of these cells are thermoreceptive, so that temperature changes would not modulate the discharge rate even if the sensory input is intact. To establish that the studied cells are indeed warm cells, two successive experiments were required on the same preparation, one on the intact tarsal organ and another on the blocked tarsal organ. In 12 preparations, both experiments were possible. No cells identified as warm cells in the preparation with intact tarsal organ were modulated by temperature changes after blocking the receptive region. They did, however, discharge continuously in the absence of a temperature input.
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Blocked terminal region: responses to electrical stimulation at different temperatures
If indeed intrinsic membrane mechanisms generate the continuous discharge in the warm cell, the frequency should change when the membrane potential changes as a result of electrical stimulation with temperature being constant. The time-course of the electrical stimuli had a square form as generated by conventional method and did not look like the slow changes in temperature, for the chief concern here was not to compare the response patterns during electrical and temperature stimulation but to compare the responses to a particular electrical stimulus at different temperatures.
After an initial phasic response to a depolarizing current pulse (Fig. 4Aa; the electrode outside the cell was negative; current flowed outward across the cell membrane), warm cells with blocked receptive region displayed constant rates of discharge over the remainder of the 3-s depolarizing period (Fig. 4, Ab and Ac). The return from the depolarizing current pulse to zero current slowed down the activity, and zero current applied for 10 s restored the initial discharge rate. A hyperpolarizing current pulse (Fig. 4Aa; the electrode outside the cell was positive; current flowed inward across the cell membrane) reduced the discharge for the 3-s period of hyperpolarization (Fig. 4, Ab and Ac). The above result, that outward current increases the spike discharge rate and inward current decreases it, was obtained from >40 warm cells.
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Intact terminal region: responses to electrical stimulation at different temperatures
All these responses are consistent with the notion that the continuous tonic discharge originates from intrinsic membrane mechanisms and persists without sensory input. When the tarsal organ was blocked, temperature did not affect the responses to current pulses. Therefore an intact terminal region as such must account for the temperature-dependent modulation of the warm cell's response. The evidence is strong, yet circumstantial. Proof would require stimulating the intact tarsal organ with current pulses and shifting the temperature level through the range. If the tonic response to electrical stimulation increases with temperature according to the positive relation between stationary temperature and impulse frequency, then an intrinsic origin of the discharge which is modulated by temperature would be upheld. The stimulus procedure was taken from the experiments on the blocked tarsal organ.
The responses of the single cell shown in Fig. 4C are representative of all 12 warm cells subjected to series of current pulses at different temperature levels. Clearly, a depolarizing current pulse produced a phasic response followed by a decline in the discharge rate to a tonic level of discharge (Fig. 4, Ca and Cb). Terminating the current pulse produced a pause in the discharge, followed by a resumption of the initial frequency. The amplitude of both the phasic and the tonic components of the response were considerably larger in the time histograms obtained at the higher temperature (Fig. 4Cc). Figure 4Bb shows that the tonic response frequency increased in direct proportion to pulse size for pulses between –30 and +100 nA. The relation is less linear in the –100- to –30-nA range. In all 12 warm cells, the temperature level influenced the tonic responses to electrical stimulation, as indicated by the shift of the stimulus–response curves along the frequency axis. Thus when confronted with current pulses, the tonic response increases with temperature. Comparing the parallel running curves in Fig. 4Bb revealed that, at the higher stationary temperature, a –100-nA hyperpolarizing current pulse did not silence activity and that the mean discharge value obtained in the absence of electrical stimulation (i.e., at 0 current) was higher at the higher temperature (as indicated by the points of intersections between the curves and the vertical line at 0 current).
Blocked terminal region: responses to successive, stepwise changes in current amplitude
During a sequence of changes in temperature, the warm cells displayed an initial phasic discharge followed by a tonic level of excitation that depended on the actual temperature (Fig. 2, B and E). In addition, the responses to depolarizing current pulses adapted to a final level of excitation according to pulse size (Fig. 4Bb). This sustained response to stationary depolarization was an invariant property of all warm cells. However, the responses to stationary temperatures (Fig. 2, B and E) cannot be compared directly with those obtained to stationary depolarizations (Fig. 4, Bb and C). For temperature, stimulation consisted of a series of successive upward or downward changes in the temperature level; the current pulses, however, were individual changes from zero current to various higher current levels followed by changes back to zero current before the next current stimulus. The possibility that the direction of change of the depolarizing current might be a parameter was not tested. We therefore studied the influence of the direction of a depolarizing current stimulus by presenting a series of successive upward or downward changes in the depolarizing current level.
Eight warm cells with intact terminal region provided the results. Each cell was subjected to a sequence of constant current stimuli. The sequence always began with zero current and proceeded in three 20-nA depolarizing steps 
60 nA (Fig. 4Da). Then the sequence was reversed; returning from the 60-nA depolarizing level back to zero current constitutes downward steps in the depolarization level. Each depolarization level was maintained for 10 s.
After an initial phasic response to an upward depolarizing current step, the warm cell adapted and displayed constant discharge rates over the remainder of the 10-s period. An example of the response rate over an entire sequence is shown in Fig. 4, Db and Dc. The magnitude of the response was clearly a function of the depolarizing current level. To show this relationship, the impulse frequency that occurred in the last second of each stimulus period was plotted in Fig. 4E (solid line). On reversing the direction of the depolarizing current sequence, i.e., proceeding from 60 to 0 nA, the phasic response was a decrease or short cessation of activity (Fig. 4, Db and Dc). The duration of the suppression increased progressively with the size of the downward depolarizing current level. This suppression of activity was followed by a gradual increase in discharge rate until it seemed to be constant during the remainder of each test period. The dashed line in Fig. 4E shows the responses for the sequence progressing in the zero current depolarization direction. The dashed line clearly revealed a hysteresis of the response over the depolarizing current range. Impulse frequency is not a function of depolarization alone; it also depends on the rate of depolarization. This observation is consistent with the hysteresis of the responses obtained during warming and recooling (Ehn and Tichy 1994, 1996). The hysteresis under electrical and temperature stimulation suggests an important role of the electrical membrane properties during adaptation of the warm cell's discharge.
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DISCUSSION |
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Intracellular recordings
Intracellular microelectrode recordings from intact thermoreceptor cells are known to be difficult. Cell penetration apparently occurred only in the soma region, probably because of the small dendritic and axonal diameter. Most of the time penetration was accompanied by a negative potential shift of 70 mV or less, a few action potentials, the first of which was 50 mV in amplitude with successive one decreasing in amplitude, and no further activity. The negative membrane potential did not decline and electrical stimulation still elicited action potentials. In other words, penetration makes the cell leak without killing it.
This observation is in contrast to the intracellular recordings from cultured mammalian thermosensory neurons, where penetration in the soma region usually revealed action potentials. However, spike activity occurred only when the temperature was changing; there was no discharge after reaching a thermal steady state. In the cultured neurons of the trigeminal ganglia of snakes innervating the pit organs, action potentials did not occur during changes in temperature, let alone when temperature was stationary. Pappas et al. (2004) provided several explanations for this observation, including the possibility that the depolarizing receptor potential will modulate an ongoing discharge of the sensory cell that apparently was not regenerated in the cultured cells.
Action potentials are not generated in the distal most end
We used the extracellular loose patch recording method for showing that the action potentials in the spider warm cells are not generated in the tip region of the dendrite where the transduction process resides. This contrasts with recent studies of the mechanoreceptive slit sensilla of this same spider species where the action potentials are borne close to the dendritic tip region (Gingl et al. 2004). Evidence for action potential generation at the dendritic tip region came also from mechanoreceptive sensilla on the insect antenna (Erler and Thurm 1981; Field and Matheson 1998; Guilett et al. 1980). The thermo- and mechanoreceptors, however, serve different functions. While thermoreceptors are continuously discharging and provide long-term information that at least in indirect form is a prerequisite for thermal regulation, the mechanoreceptors display transient responses and are involved in short-term initiation of behavioral responses.
Equivalent of receptor and injected current in affecting the discharge rate
The nature of the continuous discharge in the spider warm cell remains unknown. Further analysis may proceed from the concept that the receptor potential at the receptive terminal is a depolarization caused by changes in the ionic membrane conductance. The current associated with the receptor potential necessarily spreads from the site of the transducing process onto the region endowed with the generation of the continuous flow of action potentials. The similarity of the tonic response curves obtained by electrical stimulation of warm cells with blocked and unblocked receptive region demonstrates that the mechanisms responsible for the action potentials were not eliminated by the local application of Epoxy glue. The glue apparently selectively poisoned the receptive terminals and prevents conductance changes necessary for the receptor potential. The shift of the tonic response curves along the frequency axis obtained at different temperatures by electrical stimulation of warm cells with unblocked receptive region indicates that the mechanisms underlying the continuous discharge is equally affected by the current application and the receptor membrane conductance change.
Changes of the prevailing discharge rate encode temperature fluctuations
The spider warm cells are highly sensitive to small-amplitude temperature fluctuations (Ehn and Tichy 1996). This ability is conceivable only if its discharge permits high precision. The detection of slight changes in stimulus amplitude will be improved by adding the low-frequency receptor potential caused by the stimulus to a higher frequency carrier signal, a process known as FM. In the warm cell, the unmodulated carrier frequency may correspond with the pacemaking discharge. When the modulating receptor potential is applied, the discharge frequency will swing above and below the carrier frequency according to the amplitude of the modulating receptor potential. Any deviation from the discharge rhythm will signify a change. Threshold is defined not as the occurrence of the discharge, but as a change of the prevailing discharge rate.
Recent studies of mammalian pretectal neurons have underlined the significance of spontaneous pacemaker activity in sensory coding (Prochnow and Schmidt 2004). In neurons that discharge continuously without external drive, the membrane potential is elevated and spike threshold is lower than in neurons that are silent without stimulation. Thus when the same depolarization acts on two neurons—one continuously active and the other not—the threshold voltage is reached sooner in the former than in the latter. This permits high precision at small amounts of depolarization, according to slight changes in temperature. The continuous discharge is thus the "null" condition of a restless active cell, and stimulation, be it artificial or natural, can either increase or decrease the discharge rate. Because the continuous discharge is regular, any departure would signify a temperature change.
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FOOTNOTES |
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Address for reprint requests and other correspondence: H. Tichy, Dept. of Neurobiology and Behavioral Sciences, Faculty of Life Sciences, Univ. of Vienna, 1090 Vienna, Austria (E-mail: harald.tichy{at}univie.ac.at)
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REFERENCES |
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