Gain control in olfactory receptor neurons and the detection of temporal fluctuations in odor concentration.

The ability of the cockroach to locate an odor source in still air suggests that the temporal dynamic of odor concentration in the slowly expanding stationary plume alone is used to infer odor source distance and location. This contradicts with the well-established view that insects use the wind direction as the principle directional cue. This contribution highlights the evidence for, and likely functional relevance of, the capacity of the cockroach's olfactory receptor neurons to detect and process-from one moment to the next-not only a succession of odor concentrations but also the rates at which concentration changes. This presents a challenge for the olfactory system because it must detect and encode the temporal concentration dynamic in a manner that simultaneously allows invariant odor recognition. The challenge is met by a parallel representation of odor identity and concentration changes in a dual pathway that starts from olfactory receptor neurons located in two morphologically distinct types of olfactory sensilla. Parallel processing uses two types of gain control that simultaneously allocate different weight to the instantaneous odor concentration and its rate of change. Robust gain control provides a stable sensitivity for the instantaneous concentration by filtering the information on fluctuations in the rate of change. Variable gain control, in turn, enhances sensitivity for the concentration rate according to variations in the duration of the fluctuation period. This efficiently represents the fluctuation of concentration changes in the environmental context in which such changes occur.

Multielectrode recordings of cockroach antennal lobe neurons in response to temporal dynamics of odor concentrations.

The initial representation of the instantaneous temporal information about food odor concentration in the primary olfactory center, the antennal lobe, was examined by simultaneously recording the activity of antagonistic ON and OFF neurons with 4-channel tetrodes. During presentation of pulse-like concentration changes, ON neurons encode the rapid concentration increase at pulse onset and the pulse duration, and OFF neurons the rapid concentration decrease at pulse offset and the duration of the pulse interval. A group of ON neurons establish a concentration-invariant representation of odor pulses. The responses of ON and OFF neurons to oscillating changes in odor concentration are determined by the rate of change in dependence on the duration of the oscillation period. By adjusting sensitivity for fluctuating concentrations, these neurons improve the representation of the rate of the changing concentration. In other ON and OFF neurons, the response to changing concentrations is invariant to large variations in the rate of change due to variations in the oscillation period, facilitating odor identification in the antennal-lobe. The independent processing of odor identity and the temporal dynamics of odor concentration may speed up processing time and improve behavioral performance associated with plume tracking, especially when the air is not moving.

Developing and testing of an air dilution flow olfactometer with known rates of concentration change.

BACKGROUND: Concentration is a variable aspect of an odor signal and determines the operation range of olfactory receptor neurons (ORNs). A concentration increase is perceived as an odor stimulus. The role that the rate of concentration increase plays thereby has been studied with electrophysiological techniques in ORNs of the cockroach. A key prerequisite for these studies was the development of an air dilution flow olfactometer that allowed testing the same change in concentration at various rates. NEW METHOD: The rate of concentration change was controlled and varied by changing the mixing ratio of odor-saturated and clean air by means of proportional valves. Their input voltages were phase shifted by 180° to hold the mixed air at a particular constant volume flow rate. RESULTS: Using this stimulation technique, we identified, in a morphologically distinct sensillum on the cockroach's antenna, antagonistically responding ON and OFF ORNs which display a high sensitivity for slow changes in odor concentration. COMPARISON WITH EXISTING METHODS: The olfactometer is unique because it enables delivering slowly oscillating concentration changes. By varying the oscillation period, the individual effects of the instantaneous odor concentration and its rate of change on the ORNs' responses can be determined. CONCLUSIONS: The olfactometer provides a new experimental approach in the study of odor coding and opens the door for improved comparative studies on olfactory systems. It would be important to gain insight into the ORNs' ability to detect the rate of concentration change in other insects that use odors for orientation in different contexts.

The Performance of Olfactory Receptor Neurons: The Rate of Concentration Change Indicates Functional Specializations in the Cockroach Peripheral Olfactory System.

Slow and continuous changes in odor concentration were used as a possible easy method for measuring the effect of the instantaneous concentration and the rate of concentration change on the activity of the olfactory receptor neurons (ORNs) of basiconic sensilla on the cockroach antennae. During oscillating concentration changes, impulse frequency increased with rising instantaneous concentration and this increase was stronger the faster concentration rose through the higher concentration values. The effect of the concentration rate on the ORNs responses to the instantaneous concentration was invariant to the duration of the oscillation period: shallow concentration waves provided by long periods elicited the same response to the instantaneous concentration as steep concentration waves at brief periods. Thus, the double dependence remained unchanged when the range of concentration rates varied. This distinguishes the ORNs of basiconic sensilla from those of trichoid sensilla (Tichy and Hellwig, 2018) which adjust their gain of response according to the duration of the oscillating period. The precision of the ORNs to discriminate increments of slowly rising odor concentration was studied by applying gradual ramp-like concentration changes at different rates. While the ORNs of the trichoid sensilla perform better the slower the concentration rate, those of the basiconic sensilla show no preference for a specific rate of concentration increase. This suggests that the two types of sensilla have different functions. The ORNs of the trichoid sensilla may predominately analyze temporal features of the odor signal and the ORNs of the basiconic sensilla may be involved in extracting information on the identity of the odor source instead of mediating the spatial-temporal concentration pattern in an odor plume.

Encoding of Slowly Fluctuating Concentration Changes by Cockroach Olfactory Receptor Neurons Is Invariant to Air Flow Velocity.

The ON and OFF olfactory receptor neurons (ORNs) on the cockroach antenna display a high sensitivity for the rate at which odorant concentration changes. That rate of change acts as a gain control signal that improves the sensitivity of both ORNs for fluctuating concentration changes. By means of extracellular recording techniques, we find in both types of ORNs an increased gain for the rate of concentration change when the duration of the oscillation period increases. During long-period oscillations with slow concentration changes, the high gain for the rate of concentration change improves the ORNs ability to detect low rates of concentration changes when the fluctuations are weak. To be useful in plume tracking, gain control must be invariant to the air flow velocity. We describe that raising the level of the flow rate has no effect on the ON-ORN responses to concentration changes down to rates of 2%/s, but exerts a slight increase on the OFF-ORN response during these extremely low rates. At 4%/s, however, the OFF-ORN response is also unaffected by the flow rate level. The asymmetry corresponds with a generally higher sensitivity of the OFF-ORN to concentration changes. Nevertheless, the gain of both ORNs for the concentration rate change is robust against the air flow velocity. This makes possible an instantaneous analysis of the rate of concentration change for both directions of change by one or the other ORN. Therefore, the ON and OFF ORNs are optimized to encode concentration increments and decrements in a turbulent odorant plume.

Independent processing of increments and decrements in odorant concentration by ON and OFF olfactory receptor neurons.

A salient feature of the insect olfactory system is its ability to detect and interpret simultaneously the identity and concentration of an odorant signal along with the temporal stimulus cues that are essential for accurate odorant tracking. The olfactory system of the cockroach utilizes two parallel pathways for encoding of odorant identity and the moment-to-moment succession of odorant concentrations as well as the rate at which concentration changes. This separation originates at the peripheral level of the ORNs (olfactory receptor neurons) which are localized in basiconic and trichoid sensilla. The graded activity of ORNs in the basiconic sensilla provides the variable for the combinatorial representation of odorant identity. The antagonistically responding ON and OFF ORNs in the trichoid sensilla transmit information about concentration increments and decrements with excitatory signals. Each ON and OFF ORN adjusts its gain for odorant concentration and its rate of change to the temporal dynamics of the odorant signal: as the rate of change diminishes, both ORNs improve their sensitivity for the rate of change at the expense of the sensitivity for the instantaneous concentration. This suggests that the ON and OFF ORNs are optimized to detect minute fluctuations or even creeping changes in odorant concentration.

Revisiting Theories of Humidity Transduction: A Focus on Electrophysiological Data.

Understanding the mechanism of humidity transduction calls for experimental data and a theory to interpret the data and design new experiments. A comprehensive theory of humidity transduction must start with agreement on what humidity parameters are measured by hygroreceptors and processed by the brain. Hygroreceptors have been found in cuticular sensilla of a broad range of insect species. Their structural features are far from uniform. Nevertheless, these sensilla always contain an antagonistic pair of a moist cell and a dry cell combined with a thermoreceptive cold cell. The strategy behind this arrangement remains unclear. Three main models of humidity transduction have been proposed. Hygroreceptors could operate as mechanical hygrometers, psychrometers or evaporation detectors. Each mode of action measures a different humidity parameter. Mechanical hygrometers measure the relative humidity, psychrometers indicate the wet-bulb temperature, and evaporimeters refer to the saturation deficit of the air. Here we assess the validity of the different functions by testing specific predictions drawn from each of the models. The effect of air temperature on the responses to humidity stimulation rules out the mechanical hygrometer function, but it supports the psychrometer function and highlights the action as evaporation rate detector. We suggest testing the effect of the flow rate of the air stream used for humidity stimulation. As the wind speed strongly affects the power of evaporation, experiments with changing saturation deficit at different flow rates would improve our knowledge on humidity transduction.

Rising Background Odor Concentration Reduces Sensitivity of ON and OFF Olfactory Receptor Neurons for Changes in Concentration.

The ON and OFF ORNs on cockroach antennae optimize the detection and transfer of information about concentration increments and decrements by providing excitatory responses for both. It follows that the antagonism of the responses facilitates instantaneous evaluations of the odor plume to help the insect make tracking decisions by signaling "higher concentration than background" and "lower concentration than background". Here we analyzed the effect of the background concentration level of the odor of lemon oil on the responses of the ON and OFF ORNs to jumps and drops of that odor, respectively. Raising the background level decreases both the ON-ORN's response to concentration jumps and the OFF-ORN's response to concentration drops. Impulse frequency of the ON ORN is high when the concentration jump is large, but for a given jump, frequency tends to be higher when the background level is low. Conversely, impulse frequency of the OFF cell is high at large concentration drops, but higher still when the background level is low. Analyses of this double dependence revealed that the activity of both types of ORNs is raised more by increasing the change in concentration than by decreasing the background concentration by the same amount. This effect is greater in the OFF ORN than in the ON ORN, indicating a bias for falling concentrations. Given equal change in concentration, concentration drops evoke stronger responses in the OFF ORN than concentrations jumps in the ON ORN. This suggests that the OFF responses are used as alert information for accurately tracking.

The Rate of Concentration Change and How It Determines the Resolving Power of Olfactory Receptor Neurons.

The response characteristics of olfactory receptor neurons (ORNs) and their corollary, the differential sensitivity and the resolving power, are fundamental to understand olfactory coding and the information extracted from a fluctuating olfactory signal. Previous work has focused on the temporal resolution of odor pulses presented for very brief periods at varying concentrations. The time course of the odor pulses as a stimulus parameter has not been considered. The present study investigated the precision of the ON and OFF ORNs on the antennae of the cockroach to discriminate increments and decrements of continuously rising and falling odor concentrations. Stimulation consisted of ramp-like upward and downward concentration changes in a trapezoid fashion. By varying ramp steepness, we examined the effect of the rate of concentration change. Both ORNs were clearly dependent on continuously rising and falling odor concentrations. As the rate of upward and downward concentration changes increases, differential sensitivity improves. Since the scatter of responses around the stimulus-response functions also increases, the resolving power for concentration increments and decrements deteriorates. Thus, the slower the rate of concentration change, the higher the precision in differentiating small concentration changes. Intuitively, the inverse relationship between the rate of concentration change and the resolving power is not surprising because accuracy requires time. A high degree of precision at slow concentration rates enables the cockroach to use information about the onset and offset slopes of odor pulses in addition to the pulse height to encode the spatial-temporal structure of turbulent odor plumes.

The effect of convection on infrared detection by antennal warm cells in the bloodsucking bug Rhodnius prolixus.

Previous work revealed that bloodsucking bugs can discriminate between oscillating changes in infrared (IR) radiation and air temperature (T) using two types of warm cells located in peg-in-pit sensilla and tapered hairs (Zopf LM, Lazzari CR, Tichy H. J Neurophysiol 111: 1341-1349, 2014). These two stimuli are encoded and discriminated by the response quotient of the two warm cell types. IR radiation stimulates the warm cell in the peg-in-pit sensillum more strongly than that in the tapered hair. T stimuli evoke the reverse responses; they stimulate the latter more strongly than the former. In nature, IR and T cues are always present with certain radiation intensities and air temperatures, here referred to as background IR radiation and background T. In this article, we found that the response quotient permits the discrimination of IR and T oscillations even in the presence of different backgrounds. We show that the two warm cells respond well to IR oscillations if the background T operates by natural convection but poorly at forced convection, even if the background T is higher than at natural convection. Background IR radiation strongly affects the responses to T oscillations: the discharge rates of both warm cells are higher the higher the power of the IR background. We compared the warm cell responses with the T measured inside small model objects shaped like a cylinder, a cone, or a disc. The experiments indicate that passive thermal effects of the sense organs rather than intrinsic properties of the sensory cells are responsible for the observed results.

Infrared detection without specialized infrared receptors in the bloodsucking bug Rhodnius prolixus.

Bloodsucking bugs use infrared radiation (IR) for locating warm-blooded hosts and are able to differentiate between infrared and temperature (T) stimuli. This paper is concerned with the neuronal coding of IR in the bug Rhodnius prolixus. Data obtained are from the warm cells in the peg-in-pit sensilla (PSw cells) and in the tapered hairs (THw cells). Both warm cells responded to oscillating changes in air T and IR with oscillations in their discharge rates. The PSw cells produced stronger responses to T oscillations than the THw cells. Oscillations in IR did the reverse: they stimulated the latter more strongly than the former. The reversal in the relative excitability of the two warm cell types provides a criterion to distinguish between changes in T and IR. The existence of strongly responsive warm cells for one or the other stimulus in a paired comparison is the distinguishing feature of a "combinatory coding" mechanism. This mechanism enables the information provided by the difference or the ratio between the response magnitudes of both cell types to be utilized by the nervous system in the neural code for T and IR. These two coding parameters remained constant, although response strength changed when the oscillation period was altered. To discriminate between changes in T and IR, two things are important: which sensory cell responded to either stimulus and how strong was the response. The label warm or infrared cell may indicate its classification, but the functions are only given in the context of activity produced in parallel sensory cells.

Sensitivity of honeybee hygroreceptors to slow humidity changes and temporal humidity variation detected in high resolution by mobile measurements.

The moist cell and the dry cell on the antenna of the male honeybee were exposed to humidities slowly rising and falling at rates between -1.5%/s and +1.5%/s and at varying amplitudes in the 10 to 90% humidity range. The two cells respond to these slow humidity oscillations with oscillations in impulse frequency which depend not only on instantaneous humidity but also on the rate with which humidity changes. The impulse frequency of each cell was plotted as a function of these two parameters and regression planes were fitted to the data points of single oscillation periods. The regression slopes, which estimate sensitivity, rose with the amplitude of humidity oscillations. During large-amplitude oscillations, moist and dry cell sensitivity for instantaneous humidity and its rate of change was high. During small-amplitude oscillations, their sensitivity for both parameters was low, less exactly reflecting humidity fluctuations. Nothing is known about the spatial and temporal humidity variations a honeybee may encounter when flying through natural environments. Microclimatic parameters (absolute humidity, temperature, wind speed) were measured from an automobile traveling through different landscapes of Lower Austria. Landscape type affected extremes and mean values of humidity. Differences between peaks and troughs of humidity fluctuations were generally smaller in open grassy fields or deciduous forests than in edge habitats or forest openings. Overall, fluctuation amplitudes were small. In this part of the stimulus range, hygroreceptor sensitivity is not optimal for encoding instantaneous humidity and the rate of humidity change. It seems that honeybee's hygroreceptors are specialized for detecting large-amplitude fluctuations that are relevant for a specific behavior, namely, maintaining a sufficiently stable state of water balance. The results suggest that optimal sensitivity of both hygroreceptors is shaped not only by humidity oscillation amplitudes but also according to their impact on behavior.

Differential effects of ambient temperature on warm cell responses to infrared radiation in the bloodsucking bug Rhodnius prolixus.

Thermoreceptors provide animals with background information about the thermal environment, which is at least indirectly a prerequisite for thermoregulation and assists bloodsucking insects in the search for their host. Recordings from peg-in-pit sensilla and tapered hairs on the antennae of the bug Rhodnius prolixus revealed two physiologically different types of warm cells. Both types responded more strongly to temperature pulses produced by switching between two air streams at different constant temperatures than to infrared radiation pulses employed in still air. In addition, both warm cells were better able to discriminate small changes in air temperature than in infrared radiation. As convective and radiant heat determines the discharge, it is impossible for a single warm cell to signal the nature of the stimulus unequivocally. Individual responses are ambiguous, not with regard to temperature change, but with regard to its source. We argue that the bugs use mechanical flow information to differentiate between pulses of convective and radiant heat. However, if pulses of radiant heat occur together with a constant temperature air stream, the mechanical cues would not allow avoiding ambiguity that convective heat introduces into radiant heat stimulation. In this situation, the warm cell in the tapered hairs produced stronger responses than those in the peg-in-pit sensilla. The reversal in the excitability of the two types of warm cells provides a criterion by which to distinguish the combination of convective and radiant heat from the stimuli presented alone.

The evaporative function of cockroach hygroreceptors.

Insect hygroreceptors associate as antagonistic pairs of a moist cell and a dry cell together with a cold cell in small cuticular sensilla on the antennae. The mechanisms by which the atmospheric humidity stimulates the hygroreceptive cells remain elusive. Three models for humidity transduction have been proposed in which hygroreceptors operate either as mechanical hygrometers, evaporation detectors or psychrometers. Mechanical hygrometers are assumed to respond to the relative humidity, evaporation detectors to the saturation deficit and psychrometers to the temperature depression (the difference between wet-bulb and dry-bulb temperatures). The models refer to different ways of expressing humidity. This also means, however, that at different temperatures these different types of hygroreceptors indicate very different humidity conditions. The present study tested the adequacy of the three models on the cockroach's moist and dry cells by determining whether the specific predictions about the temperature-dependence of the humidity responses are indeed observed. While in previous studies stimulation consisted of rapid step-like humidity changes, here we changed humidity slowly and continuously up and down in a sinusoidal fashion. The low rates of change made it possible to measure instantaneous humidity values based on UV-absorption and to assign these values to the hygroreceptive sensillum. The moist cell fitted neither the mechanical hygrometer nor the evaporation detector model: the temperature dependence of its humidity responses could not be attributed to relative humidity or to saturation deficit, respectively. The psychrometer model, however, was verified by the close relationships of the moist cell's response with the wet-bulb temperature and the dry cell's response with the dry-bulb temperature. Thus, the hygroreceptors respond to evaporation and the resulting cooling due to the wetness or dryness of the air. The drier the ambient air (absolutely) and the higher the temperature, the greater the evaporative temperature depression and the power to desiccate.

Adaptation as a mechanism for gain control in cockroach ON and OFF olfactory receptor neurons.

In many sensory systems adaptation acts as a gain control mechanism that optimizes sensory performance by trading increased sensitivity to low stimulus intensity for decreased sensitivity to high stimulus intensity. Adaptation of insect antennal olfactory receptor neurons (ORNs) has been studied for strong odour concentrations, either pulsed or constant. Here, we report that during slowly oscillating changes in the concentration of the odour of lemon oil, the ON and OFF ORNs on the antenna of the cockroach Periplaneta americana adapt to the actual odour concentration and the rate at which concentration changes. When odour concentration oscillates rapidly with brief periods, adaptation improves gain for instantaneous odour concentration and reduces gain for the rate of concentration change. Conversely, when odour concentration oscillates slowly with long periods, adaptation increases gain for the rate of change at the expense of instantaneous concentration. Without this gain control the ON and OFF ORNs would, at brief oscillation periods, soon reach their saturation level and become insensitive to further concentration increments and decrements. At long oscillation periods, on the other hand, the cue would simply be that the discharge begins to change. Because of the high gain for the rate of change, the cockroach will receive creeping changes in odour concentration, even if they persist in one direction. Gain control permits a high degree of precision at small rates when it counts most, without sacrificing the range of detection and without extending the measuring scale.

Functional asymmetries in cockroach ON and OFF olfactory receptor neurons.

The ON and OFF olfactory receptor neurons (ORNs) on the antenna of the American cockroach respond to the same changes in the concentration of the odor of lemon oil, but in the opposite direction. The same jump in concentration raises impulse frequency in the ON and lowers it in the OFF ORN and, conversely, the same concentration drop raises impulse frequency in the OFF and lowers it in the ON ORN. When the new concentration level is maintained, it becomes a background concentration and affects the responses of the ON and OFF ORNs to superimposed changes. Raising the background concentration decreases both the ON-ORN's response to concentration jumps and the OFF-ORN's response to concentration drops. In addition, the slopes of the functions approximating the relationship of impulse frequency to concentration changes become flatter for both types of ORNs as the background concentration rises. The progressively compressed scaling optimizes the detection of concentration changes in the low concentration range. The loss of information caused by the lower differential sensitivity in the high concentration range is partially compensated by the higher discharge rates of the OFF ORNs. The functional asymmetry of the ON and OFF ORNs, which reflects nonlinearity in the detection of changes in the concentration of the lemon oil odor, improves information transfer for decrements in the high concentration range.

Adaptation as a mechanism for gain control in an insect thermoreceptor.

Adaptation controls the gain of the input-function of the cockroach's cold cell during slowly oscillating changes in temperature. When the oscillation period is long, the cold cell improves its gain for the rate of temperature change at the expense of its ability to code instantaneous temperature. When the oscillation period is brief, however, the cold cell reduces this gain and improves its sensitivity for instantaneous temperature. This type of gain control has an important function. When the cockroach ventures from under cover and into moving air, the cold cell is confronted constantly with brief changes in temperature. To be of any use, a limit in the gain for the rate of change seems to be essential. Without such a limit, the cold cell will always indicate temperature change. The decrease in gain for the rate of change involves an increase in gain for instantaneous temperature. Therefore the animal receives precise information about the temperature at which the change occurs and can seek an area of different temperature. If the cockroach ventures back under cover, the rate of change will become slow. In this situation, a high gain improves the ability to signal slow temperature changes. The cockroach receives the early warning of slow fluctuations or even creeping changes in temperature. A comparison of the cold cell's responses with the temperature measured inside of small, cylindrical model objects indicates that coding characteristic rather than passive thermal effects of the structures enclosing the cold cell are responsible for the observed behavior.

Humidity-dependent cold cells on the antenna of the stick insect.

We present the first systematic study of the response of insect "cold cells" to a variation in the partial pressure of water vapor in ambient air. The cold cells on the antenna of the stick insect respond with an increase in activity when either the temperature or the partial pressure of water vapor is suddenly reduced. This double dependency does not in itself constitute bimodality because it could disappear with the proper choice of parameters involving temperature and humidity. In this study, we demonstrate that the evaporation of a small amount of water from the sensillum surface resulting from a drop in the water vapor pressure-leading to a transient drop in temperature and thus to a brief rise in impulse frequency-is the most plausible explanation for this bimodal response. We also show with an order-of-magnitude calculation that this mechanism is plausible and consistent with the amounts of water vapor potentially present on the sensillum. We hypothesize that a film of moisture collects on the hygroscopic sensillum surface at higher humidity and then tends to evaporate when humidity is lowered. The water might even be bound loosely within the cuticular wall, a situation conceivable in a sensillum that contains two hygroreceptive cells in addition to the cold cell.

Olfactory receptors on the cockroach antenna signal odour ON and odour OFF by excitation.

A morphologically identifiable type of olfactory sensillum on the antenna of the American cockroach contains a pair of ON and OFF cells that responds oppositely to changes in the concentration of fruit odours. The odour of lemon oil was used to study the accuracy with which these cells can discriminate between rapid step-like, ramp-like and oscillating changes in odour concentration. The discharge rates of both cells are not only affected by the actual concentration at particular instants in time (instantaneous concentration) but also by the rate at which concentration changes. The impulse frequency of the fruit odour ON cell is high when odour concentration is high, but higher still when odour concentration is also rising. Conversely, the impulse frequency of the fruit odour OFF cell is high when odour concentration is low and higher still when odour concentration is also falling. Thus, the effect of odour concentration on the responses of both cells is reinforced by the rate of change. Sensitivity to the rate of concentration change becomes greater when the rate is low. Because of the high sensitivity to low rates of change, these cells are optimized to detect fluctuations in fruit odour concentration. Whereas the ON cell signals the arrival and presence of fruit odour, the OFF cell detects its termination and absence. These cells provide excitatory responses for both increase and decrease in fruit odour concentration and may therefore reinforce contrast information.

Sensory representation of temperature in mosquito warm and cold cells.

A pair of antagonistic thermoreceptive cells is associated with each of two peg-in-pit sensilla located on the antennal tip of Aedes aegypti. One, the warm cell, responds to rapid warming with a sudden increase in the rate of discharge. The other, a cold cell, responds to rapid cooling with a sudden increase in the discharge rate. When temperature changes are provided by oscillating changes in the convective heat contained in the stimulating air stream, the oscillating discharge rates of both cell types are in advance of the oscillations in temperature and slightly behind the oscillations in the rate of temperature change. Analysis of these phase relationships shows that both cell types respond not only to the actual temperature at particular instance in time (instantaneous temperature) but also to the rate with which temperature changes. Individual responses are therefore ambiguous and signal tendencies rather than precise instantaneous values. When the temperature oscillations are delivered by changes in radiation power, however, the oscillating discharge rates of the warm and cold cells are in step with the oscillations in temperature. Here, individual responses signal instantaneous values of temperature rather than tendencies. The power of radiant heat required to modulate the discharge rates is relatively high, suggesting that infrared radiation is not a significant cue in distant host location.