Insect hygroreceptor responses to continuous changes in humidity and air pressure

Abstract

The most favored model of humidity transduction views the cuticular wall of insect hygroreceptive sensilla as a hygromechanical transducer. Hygroscopic swelling or shrinking alters the geometry of the wall, deforming the dendritic membranes of the moist and dry cells. The small size the sensilla and their position surrounded by elevated structures creates technical difficulties to mechanically stimulate them by direct contact. The present study investigated hygroreceptors on the antennae of the cockroach and the stick insect. Accurately controlled, homogeneous mechanical input was delivered by modulating air pressure. Both the moist and dry cells responded not only to changes in air pressure but also in the opposite direction, as observed during changes in air humidity. The moist cell's excitatory response to increasing humidity and increasing air pressure implies that swelling of the hygroscopic cuticle compresses the dendrites, and the dry cell's excitatory response to decreasing humidity and decreasing air pressure implies that shrinking of the hygroscopic cuticle expands the dendrites. The moist and dry cells of the stick insect are more sensitive to pressure changes than those of the cockroach, but the responses to air pressure are generally weaker than to humidity. Therefore the hygroreceptive sensilla differ in their physical properties and constitutions. Furthermore, the mechanical parameters associated with homogeneous changes in air pressure on the sensillum surface can only partially account for the responses of the moist and dry cells of both species to humidity stimulation.

Fig. 1

A-D: Diagram of the hygroreceptive sensilla on the cockroach and stick insect antenna and proposed effects of changes in humidity and air pressure. A and B: the cuticular processes, cellular associations and lymph cavities in longitudinal section. The main feature common to both insects is a thin-walled sensillum cuticle that lacks a pore system to connect the lumen of the dendritic sheath with outside. The molting pore (m) at the tip is plugged by dense material. Of the three or four sensory cells innervating the sensillum, two possess unbranched outer dendritic segments (d) extending up to the apex of the cuticular peg. The dendritic terminals entering the narrow lumen allow only a small space to separate them from the dendritic sheath and from each other. Dense material accumulates in the space towards the apex of the peg. Farther inside, below the base of the peg, the space opens out to form the small inner receptor lymph cavity (ilc). This cavity encloses the central portion of the dendrites between their inner and outer segments, and is surrounded by sheath cells (shc). Outside the sheath there is a more voluminous space, the outer receptor lymph cavity (olc) (after Tichy and Loftus 1996). C and D: proposed effects of changes in humidity (left side in both diagrams) and changes in air pressure (right side in both diagrams) on the cuticular wall (cw) and the dendritic processes (d) of the moist and dry cell. Swelling or expanding of the sensory cuticle, due to its tendency to take up water, increases the discharge rate of the moist cell and decreases that of the dry cell (Tichy 1987; Fig. 1C); conversely, shrinking or contracting of the cuticular wall, due to its tendency to lose water, increases the discharge rate of the dry cell and decreases that of the moist cell (Fig. 1D). The internal pressure increase during swelling is imitated by increasing air pressure (Fig. 1C), and the internal decrease in pressure during shrinking is imitated by decreasing air pressure (Fig. 1D)

Fig. 2

A-C: Effects of changes in air pressure on the absolute humidity, the temperature and the relative humidity inside the pressure chamber. A: absolute humidity plotted as function of air pressure. B: temperature plotted as function of air pressure. C: relative humidity determined from values in A and B as function of air pressure. Relationships approximated by linear regressions, AH absolute humidity, RH relative humidity, r correlation coefficient, T temperature

Fig. 3

Calculated values of the relative humidity for different water vapor pressures and temperatures

Fig. 4

A and B: Responses of the moist and dry cells to slow and continuous humidity changes. A: cockroach. B: stick insect. a time course of the relative humidity; b time course of the mean frequency (bin width, 0.5 s) of the moist cell (solid line) and the dry cell (dotted line); c extracellular recorded activity. In the cockroach, the moist cell displays larger impulse amplitudes than the dry cell; in the stick insect, impulses from the cold cell tend to be the largest; the moist-cell’s impulses are medium sized and those from the dry cell are the smallest

Fig. 5

A and B: Examples of the responses of the moist and dry cells to puffs of moist and dry air. A: cockroach. B: stick insect. a stimulus: moist air puff; b stimulus: dry air puff. Lines, impulses of moist cells; dots, impulses of dry cells; triangles, impulses of the cold cell. Arrows mark stimulus onset

Fig. 6

A and B: Impulse frequency of the moist and dry cells as function of instantaneous humidity, and as function of both instantaneous humidity and rate of humidity change. A: cockroach. B: stick insect. a impulse frequency of a single moist plotted against instantaneous humidity. b impulse frequency of a single dry cell plotted against instantaneous humidity. Stimulus-response functions approximated by linear regressions (F = a + bRH; where F is the impulse frequency, a the height of the regression line, and b the slope of function indicating the mean change in impulse frequency for each percent change in instantaneous humidity). c impulse frequency of the same moist cell as in a plotted against instantaneous humidity and its rate of change. d impulse frequency of the same moist cell as in b plotted against instantaneous humidity and its rate of change. Multiple regressions which utilize 3-dimensional planes (F = a + bRH + c dRH/dt; where F is the impulse frequency, and a the height of the regression plane) are calculated to determine the simultaneous effects of instantaneous humidity (b-slope) and the rate of humidity change (c-slope) on the response frequencies of both cells. RH relative humidity, r correlation coefficient

Fig. 7

A-D: Examples of the responses of the cockroach’s moist and dry cells to slow and continuous pressure changes. A and B: moist cells from different recordings responding to increasing pressure. C and D: dry cells from different recordings responding to decreasing pressure. a time course of the air pressure; b time course of the mean frequency (bin width, 0.5 s) of the moist cell (solid line) and the dry cell (dotted line); c extracellular recorded activity

Fig. 8

A-D: Examples of the responses of the stick insect’s moist and dry cells to slow and continuous pressure changes. A and B: moist cells from different recordings responding to increasing pressure. C and D: dry cells from different recordings responding to decreasing pressure. a time course of the air pressure; b time course of the mean frequency (bin width, 0.5 ms) of the a moist cell (solid line) and the dry cell (dotted line); c extracellular recorded activity

Fig. 9

A and B: Impulse frequency of the moist and dry cells as function of instantaneous pressure, and as function of both instantaneous pressure and rate of pressure change. A: cockroach. B: stick insect. a impulse frequency of a single moist cell plotted against instantaneous pressure. b impulse frequency of a single dry cell plotted against instantaneous pressure. Stimulus-response functions approximated by linear regressions (F = a + bAP; where F is the impulse frequency, a the height of the regression line, and b the slope of function indicating the mean change in impulse frequency for each percent change in instantaneous pressure). c impulse frequency of the same moist cells as in a plotted against instantaneous pressure and its rate of change. d impulse frequency of the same moist cells as in b plotted against instantaneous pressure and its rate of change. Multiple regressions which utilize 3-dimensional planes (F = a + b AP + c dAP/dt; where F is the impulse frequency, and a the height of the regression plane) are calculated to determine the simultaneous effects of instantaneous pressure (b-slope) and the rate of pressure change (c-slope) on the response frequencies of both cells. AP air pressure, r correlation coefficient