A Temperature Receptor in the Tarsus of the Cockroach, Periplaneta Americana

During the course of experiments on the reactions of the cockroach, Periplaneta americana, to temperature changes (Kerkut & Taylor, 1956) we noted that when the floor of the vessel containing the insect was cooled, the cockroach became more active. The activity later ceased and the animal rested on the floor of the container. After a little while the insect took up a characteristic position with the claws and distal ends of the the tarsi raised from the ground; the insect’s weight resting on the proximal joints of the tarsi (Fig. 1).

This reaction was so consistent that it seemed possible that there might be a temperature receptor in the distal part of the tarsus and that the insect was removing the sense organ from the source of stimulation. It was therefore decided to see what effect cooling the tarsus had on the electrical activity of the nerves in the leg.

The apparatus consisted of a Perspex box fitted with a stainless steel lid. Water or cooling mixture at a specific temperature was drawn through the box by means of a water pump. The temperature of the water was recorded by means of a thermometer and a thermistor placed immediately below the steel lid. The internal volume of the box was low due to the presence of an internal baffle; this facilitated a rapid change in the temperature. Changing the temperature did not lead to any detectable buckling or movement of the part of the steel roof in contact with the insect’s tarsus.

The cockroach leg was removed from the animal and placed so that the distal end of the tarsus rested on the metal surface of the apparatus. A pair of platinum recording electrodes were placed into the tibia as near the leg nerves as possible, and the electrical activity noted. The potentials were amplified in a Leak TL12 amplifier and recorded on a Ferrograph Tape Recorder. The written records were made on an Ediswan Pen Recorder.

In many preparations we found that after a few minutes there was no background activity. In others there was some background activity which increased if the apparatus was tapped. This was clearly due to stimulation of mechanoreceptors and we then adjusted the position of the leg on the apparatus till there was no back-ground activity. Fig. 2 A shows the effect of lowering the temperature. There was no activity before the temperature change, but when the temperature was lowered from 22° to 2° C. there was a sudden burst of activity which lasted approximately 12 sec. Fig. 2B shows the effect of raising the temperature of the same preparation. The temperature was raised from 2° to 22° C. and there was a short burst of activity. In general we found that over the range 0-25° C. the preparations were more sensitive to cooling than to wanning. Preparations maintained below 13° C. were often found to be sensitive to a fall of 1° C., but most preparations required a rise of 5° C. before they became active. It was possible to obtain discharges as a result of increases of 1° C. but this only occurred at high temperatures, i.e. above 30° C. In most cases if we raised the temperature from 10° to 14° C. there was no activity—in fact if the preparation had been discharging as a result of a previous cooling, then warming stopped the discharge.

Preparations have been found which discharged for up to 7 min. after the tarsus had been cooled. The extent and duration of the discharge depended upon the extent to which the temperature was lowered. This is demonstrated in Fig. 3.

Here the preparation was adjusted to 22° C. and the temperature then lowered. The activity of the preparation was recorded and the temperature then returned to 22°°B°; C. for 3 min. The preparation was then cooled once more and then returned to 22° C. In this way the sensitivity of the preparation to different changes of temperature was determined. A fall of 7° C. brought about only slight activity, whilst bigger temperature changes (Δ 11-26° C.) brought about greater activity which also lasted for a longer time.

The sensitivity of the preparations varied slightly from leg to leg and from one region to another of the temperature range over which they were tested. In the experiment illustrated in Fig. 4 there was no activity till the temperature was dropped below 10° C. This preparation became active only above 35° C., a change from 22° to 30° C. having no effect. At the same time it should be noted that there was often a response when it was warmed from 10° to 22° C. ; but in this experiment only changes from 22° C. are considered.

Cooling below 22° C. in general increased the activity, and in most cases if the preparation was warmed whilst the cold discharges were active, the activity then stopped. In some cases, however, warming brought about a sudden increase in activity for a few seconds before it faded away and stopped.

At times the preparations showed some continuous background activity due to the stimulation of proprioceptors and mechanoreceptors. In such preparations lowering the temperature brought in the activity of the cold receptor. This is shown in Fig. 5, where at the arrow the temperature was lowered from 22° to 5° C. At this point large impulses appeared which were easily distinguished from the background activity.

Since the receptor is active when only the pre-tarsus and claw are cooled, it would appear that this is the site of the cold receptor. In addition, it is this part that is raised from the ground when the animal is placed on a very cold surface. The site of the receptor was further localized by placing only part of the limb on the metal surface. There was no response when either the tip of the claw or the side of the claw were cooled. It was necessary for the pad (arolium) to be in contact with the metal before any response could be elicited. Other sensitive sites were found at the base of the first, second, third and fourth tarsal segments (unstippled in Fig. 1).

These are the regions that are unsclerotized and form the tarsal pulvilli. Local application of a cold copper rod confirmed that the arolium and pulvilli were the most sensitive parts of the tarsus. If these were amputated, a response was still obtained to cooling but the potentials were reduced in size. Similarly, if the cut stump of the tibia was cooled it evoked potentials which were, in general, smaller than those found after cooling the intact tarsus.

Gentle pressure on the pulvilli with a warm rod (20° C.) evoked a series of small potentials, but if the rod was cold (0° C.) the potentials were much larger in size. It is possible that the pulvilli have receptors sensitive to both touch and temperature and that cooling stimulated many receptors at the same time and hence brought about large potentials. On the other hand, there may be two types of receptors, one for touch and another for temperature. Histological studies are now being carried out to determine whether there is more than one type of sense organ on the pulvilli. There is some indication that the tactile receptors can respond to temperature since the hairs on the ventral surface of the first tarsal segment can be stimulated when a cold rod (—20° C.) is brought within 1 mm. of them; no contact being made in this case.

The literature on the occurrence and properties of temperature receptors in insects has recently been reviewed by Herter (1953). Most of the previous investigators have been concerned with the reactions of insects to heat and the way in which their behaviour alters if various parts of the body are removed. Herter (1924) brought a hot needle towards various parts of an insect’s body and noted how near the needle had to be before the insect showed a response. The most sensitive part of Blabera fusca proved the labial palps which were sensitive when the needle was some mm. away. The tarsi were sensitive when the needle was 0·5-1 mm. away. In Liogryllus campestris he showed the relative temperature sensitivity was, in order of decreasing sensitivity, labial palps, antennae, cerci and tarsi. Cappe de Bailion (1932) showed the presence of a heat receptor in the antennae of the phasmid Menexenus semiarmatus by removing parts of the antennae and finding when the animal lost its capacity to respond to localized heat. He showed that there was a receptor in the dorsal surface of the 12th antennal segment. Similarly, Herter (1939) and Kahnus (1948) showed a temperature receptor in the 14th segment of Carausius morosus. Wiggles worth & Gillett (1934 a, b) showed that in Rhodnius proUxus the long hairs at the tip of the antennae were most probably temperature receptors. Slifer (1951) showed by extirpation experiments, and by noting the way in which normal and operated animals responded to a hot glass rod, that the antennal crescents and the body fenestrae were temperature receptors in Locusta migratoria migratorioides.

There seems to be very little information concerning either the electrophysiology of the temperature receptors, or the existence of a cold receptor. Barber (1956) has described the electrical reactions of a temperature receptor in the gnathobase of Limulus, and Hodgson & Roeder (1956) have shown that the sensory discharges from the taste receptors in Phormia are sensitive to temperature change, but in both cases only a positive response to an increase in temperature has been described. In neither case does the activity increase when the temperature is decreased. The receptors described here for the tarsus of the cockroach behaves more like the cold receptors described by Dodt & Zottennan (1952) in the cat’s tongue. These receptors become more active when the temperature is lowered. The activity is proportional to the extent to which the temperature is lowered. The activity can last for some time after the receptor has been cooled, in some cases for 7 min. It is interesting to compare the response of the tarsal receptor with the responses found to temperature changes in the central nervous system of the cockroach. In the central nervous system there are several patterns of cell behaviour, some of which are identical with that described for the tarsal receptor. These cells only become active at low temperatures and their activity disappears on warming to approximately 13-28° C. There are other cells in the central nervous system which for a short time become more active when the temperature is lowered, but within a few seconds their activity is considerably reduced (Kerkut & Taylor, 1956).

It is difficult to tell if there are warm receptors in the tarsus. There are two distinct conditions under which warming the tarsus can lead to electrical activity. In the first case the tarsus responds when it is warmed 5° C. in the range from o° to 28° C., but the activity lasts for a short time only. In the second case, the tarsus responds when it is warmed i° C. above 30° C. In this case the activity is prolonged and may show definite bursts of injury potentials. Here the tarsus resembles the cold receptors described by Dodt & Zottennan (1952) in the cat’s tongue, which also showed an anomalous cold discharge at higher temperatures.