Harald Tichy

Hygro- and thermoreceptive triad in antennal sensillum of the stick insect,Carausius morosus

SummaryThe receptor cells in a poreless sensillum on the antenna ofCarausius morosus were examined electrophysiologically. Two of the units are antagonistic regarding humidity, one responding with an increase in impulse frequency to rising humidity (moistair unit) and the other to falling humidity (dry-air unit). Another reacts to falling temperature with a rise in impulse frequency (cold unit). In some cases responses from a fourth unit were also present. Its modality is uncertain. A method of marking the sensillum with a cactus needle for subsequent structural examination after recording is described.

Hygroreceptors in insects and a spider: Humidity transduction models

The model most favored in insect hygroreceptors for humidity transduction resembles a mechanical hygrometer. It envisions the humidity-dependent swelling or shrinking of hygroscopic structures belonging to the sensillum as governing dendrite activity. This model, however, is at variance with both the organization and the chemical sensitivity of the hygroreceptive sensilla of Cupiennius salei, a wandering spider. Activity changes in these sensilla fit better into an electrochemical concentration model in which humidity would control the concentration of the electrolytes surrounding the dendrites of the hygroreceptors and thus govern their responses. The situation in Cupiennius, therefore, places models for hygroreception in a broader context and also leads to questions concerning their feasibility elsewhere. I nsect hygroreceptors appear to be restricted mainly to a small number of sensilla on the antennae. There they associate in antagonistic pairs (a moist cell and a dry cell) with a thermoreceptor (for reviews of insects, see [2, 3, 21]). The situation in the tarsal organ of the wandering spider, Cupiennius salei, is somewhat similar [9]. The antagonistic hygroreceptors are present here, too, as are also thermoreceptors. These, however, are not cold receptors as with insects, but warm receptors. Externally the hygro-thermoreceptive sensilla of Cupiennius resemble those of insects. All can be broadly classed as peg-like cuticular protuberances, and most possess an apical pore that is filled with electron-dense material. In insects they tend to be stubby and rather conical with rounded tips, or with caps like mushrooms. To the first group belong sensilla coeloconica (in Carausius morosus, Fig. 1 D [5], also in Locusta migratoria, Fig. 1 C [4]) and s. styloconica (in the moth, Bombyx mori, Fig. 1E [22, 23, 26, 27]; also in the saturniid, Antheraea pernyi [12, 38]; and in the noctuid, Mamestra brassicae [8]). To the second group belong sensilla capitula (in Periplaneta americana, Fig. l A [31, 33]) and s. coelocapitula (in Apis mellifera, Fig. 1 B [34, 36]). In Cupiennius, the hygro-thermoreceptive sensilla in the tarsal organ resemble short, conical nipples (Fig. 1 F). As with insects, these, too, lack the columns of pores in the side walls common to olfactory sensilla. Perhaps quite significantly, the dendritic outer segments of their sensory cells are not only coextensive. In contrast to those of insects, they reach right up the lumen of the sensillum to the apical pore ([6]; for insects, see citations above). There is also a further difference: the hygroreceptors in the sensilla of the tarsal organ can also be stimulated by vapors from several very reactive and volatile substances (ammonia, short-chain aliphatic amines, formic and acetic acids [9]).

Infrared sensitivity of thermoreceptors.

Abstract. This study compares the effects of convective and radiant heat on the discharge rates of the warm cell of a thin hair-like sensillum of the tick and of the cold cells of small peg-shaped sensilla of the locust and the cockroach. The temperature rates imposed by the convective heat contained in the air stream used for stimulation are reflected by the discharge rate of the thermoreceptors. We determined the increment in radiant heat that results in the same change in discharge rate as a given increment in temperature due to convection. The amount of infrared radiation required to produce the same effect as a 1°C change in temperature differs for the sensory cells of the tick, locust and cockroach, respectively, suggesting differences in the ability of the sensilla to take up and transfer radiant heat. The power of radiation required to modulate the discharge rates is very high and outside the biologically meaningful range in all cases. Obviously the adequate stimulus for the examined sensilla is convective heat and not radiant heat.

Hygroreceptor identification and response characteristics in the stick insectCarausius morosus

SummarySimultaneous recordings were made from 3 sensory units in an easily identifiable sensillum on the 12th antennal segment ofCarausius morosus. Impulse frequency (F) of one unit rose sharply when either the temperature (T) or the partial pressure of water vapor (Pw) was suddenly lowered. F of another rose sharply either when T was suddenly lowered or Pw was raised. F of the third was hardly affected by sudden changes in T but rose abruptly when Pw fell (Fig. 1). The reactions of the first may be explained by enthalpic cooling and is considered a cold cell. Those of the second may be attributed to changes in relative humidity (Hr) and is thus termed a moist cell. The third is taken to be the latters antagonist, a dry cell.A 90%-probability that a single moist cell of average differential sensitivity will correctly discriminate between two humidity levels is not reached until the difference between the two is 38% Hr. The dry cell requires a difference of only 7.5% (Table 1). The basis for discrimination is a single presentation of each level.The power to discriminate Hr steps is better in both cell types. For a single moist cell of average differential sensitivity the difference required between the steps for a 90%-probability of correct discrimination is only 6.3% Hr; for the dry cell, 3.5% Hr. Basis for discrimination: a single presentation of each step. Step range: 5% to 55% Hr.

Problems in Hygro- and Thermoreception

Hygroreceptors have been found only in insects and a spider. They associate in antagonistic pairs of a moist and a dry cell in the same sensilla with a thermoreceptor. In insect hygro-thermoreceptive sensilla all of the three cells respond to changes in humidity and two of the three cells respond in addition to changes in temperature. Assigning the individual cells to a particular modality thus becomes a problem. Structural features of thermoreceptors have a bearing on their sensitivity. The size of the dendritic membrane area is related to the sensitivity to slowly changing and steady temperatures. It may determine the number of molecular receptors which in turn sets signal-to-noise ratio. Sensitivity to rapid changes in temperature seems to be increased by positioning the dendritic tips above the surface of the body wall. This is believed to reduce damping of heat transfer. Structural diversity among insect and spider hygro-thermoreceptive sensilla suggests different transduction mechanisms. Three models for hygroreception are discussed. In mechanical hygrometers activity is initiated by swelling or shrinking in hygroscopic sensillum structures, whereas in psychrometers the degree of cooling due to evaporation is used to measure humidity. In electrochemical hygrometers humidity affects electrolyte concentration outside the dendrites.

Olfactory receptor cells on the cockroach antennae: responses to the direction and rate of change in food odour concentration

In insects, information about food odour is encoded by olfactory receptor cells with characteristic response spectra, located in several types of cuticular sensilla. Within short, hair‐like sensilla on the cockroachs antenna, antagonistic pairs of olfactory receptor cells shape information inflow to the CNS by providing excitatory responses for both increases and decreases in food odour concentration. The segregation of food odour information into parallel ON and OFF responses suggests that temporal concentration changes become enhanced in the sensory output. When food odour concentration changes slowly and continuously up and down with smooth transition from one direction to another, the ON and OFF olfactory cells not only signal a succession of odour concentrations but also the rate with which odour concentration happens to be changing. Access to the values of such cues is of great use to an insect orientating to an odour source. With them they may extract concentration gradients from odour plumes.

Hygro- and thermoreceptive tarsal organ in the spider Cupiennius salei

Extracellular recordings were made from moist cells, dry cells and warm cells in the tip pore sensilla of the spider tarsal organ. Stimulation consisted of a rapid shift from an adapting air stream to another one at different levels of partial pressure of water vapor or of temperature. The moist and the dry cells respond antagonistically to sudden changes in humidity. Both hygroreceptors are unusual in being excited in a synergistic manner by pungent vapors of very volatile, polar substances. Presumably, the hygrosensitivity is superimposed on basically chemosensitive receptors. A moist cell at average differential sensitivity is able to discriminate two successive upward steps in humidity when they differ by 11% relative humidity. For a single dry cell, the difference required for a correct discrimination between two downward humidity steps is 10% relative humidity. The moist and the dry cells are unique in that they occur in combination with warm cells. A single warm cell at average differential sensitivity is able to resolve differences in warming steps down to 0.4°C.

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.

Response characteristics of a spider warm cell: temperature sensitivities and structural properties

The sensitivity of a warm cell to temperature stimulation was examined electrophysiologically on the spider Cupiennius salei. The relationship between sensitivity and structure of the warm cell was assessed by comparing both the electrophysiological and electron-microscopic data with those described for insect cold cells. Stimulation of the spider warm cell with slowly oscillating temperature change and steady temperature elicited less sensitive responses than in insect cold cells. These characteristics are reflected in the size of the dendritic membrane area, which is smaller in the spider warm cell compared to the insect cold cells. Rapid step-like temperature change produced in the spider warm cell very sensitive responses when compared with data of insect cold cells. The dendritic tip of the spider warm cell is exposed at a pore on the tip of the sensillum but is covered by the cuticle of the sensillum in the insect cold cells.

Hygro- and thermoreceptors in tip-pore sensilla of the tarsal organ of the spider Cupiennius salei: innervation and central projection

The hygro- and thermoreceptive tarsal organ in the wandering spider Cupiennius salei is located on the tarsus of each walking leg and pedipalp, and consists of a tiny air-filled capsule in the cuticle. This capsule communicates with the outside world through a small aperture and contains seven nipple-shaped sensilla, each with a pore at its tip. In both their external morphology and internal structure, the sensilla are indistinguishable, although one sensillum is innervated by only two sensory cells, whereas the other six sensilla contain three sensory cells. Their dendrites are unbranched and terminate at the tip-pore, where they are enveloped by amorphous material that appears to limit their exposure to the atmosphere. Cobalt fillings reveal that each tarsal organ projects to three different areas within the suboesophageal ganglionic mass: (1) the sensory longitudinal tract 3 and 4; (2) the corresponding pedipalpal or leg ganglion; (3) a structured neuropil (here termed the “Blumenthal neuropil”) beneath the oesophagus. The multiple representation of sensory afferents from each tarsal organ in different regions of the suboesophageal ganglionic mass suggests parallel processing of hygro-/thermoreceptive information.