INTERNAL FACTORS CONTROLLING THE SUB- OESOPHAGEAL GANGLION NEURO SECRETORY CYCLE IN PERIPLANETA AMERICANA L.
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1 INTERNAL FACTORS CONTROLLING THE SUB- OESOPHAGEAL GANGLION NEURO SECRETORY CYCLE IN PERIPLANETA AMERICANA L. BY JANET E. HARKER Department of Zoology, University of Cambridge {Received 31 August 1959) INTRODUCTION The diurnal locomotory activity rhythm of Periplaneta americana is dependent upon the rhythmic secretion of a hormone from the neurosecretory cells of the suboesophageal ganglion. The phases of this secretory cycle are set by the stimulus of an environmental change from light to darkness (Harker, 1956, 1958 a), the beginning of secretion being coincident with the time of the stimulus. When a rhythmically secreting suboesophageal ganglion is implanted into an arrhythmic animal this animal subsequently follows an activity rhythm in phase with the neurosecretory cycle of the implanted ganglion: that is, the ganglion can maintain its neurosecretory cycle independently. It has been suggested, however, that other processes following 24 hr. rhythms may affect the neurosecretory cycle, particularly in the absence of alternating environmental factors (Harker, 1958a, b). This paper describes the interaction of the neurosecretory cycle and a rhythm associated with the nervous system. EXPERIMENTS The experiments described were designed in an attempt to alter the timing of the phases of the suboesophageal ganglion neurosecretory cycle while leaving unaltered the phases of any other 24 hr. rhythm. CHILLING THE SUBOESOPHAGEAL GANGLION IN SITU When cockroaches have been kept at 3 0 C. for a number of hours the phases of their activity rhythms, after return to room temperature, show a time-lag of a period equivalent to that for which the animals were chilled. A method has been devised (Brown & Harker, i960) by which the neurosecretory cells of the suboesophageal ganglion can be chilled in situ, without the temperature of other parts of the body being lowered. The temperature of the suboesophageal ganglia of five rhythmically active cockroaches was lowered to 3 0 C. for 4 hr.; the ganglia were then dissected out and implanted into arrhythmic animals. All of the implanted animals subsequently showed an activity rhythm in which the phases were delayed by 4 hr. (Fig. 1 b) relative to those of unchilled animals (Fig. 1 a). It is concluded that the neurosecretory cycle is halted by chilling, and starts again when the temperature is raised.
2 Neurosecretory cycle in Periplaneta americana L. 165 The suboesophageal ganglia of another group of animals were chilled for 4 hr. and the ganglia left in their normal positions. The phases of the rhythms of this group showed no delay relative to their previous settings (Fig. 2 a). The ganglia from these animals were removed 24 hr. after shilling and implanted into arrhythmic animals; the phases of the rhythms which subsequently appeared in the implanted animals also remained unchanged in relation to those of unchilled animals (Fig. 2b). The neurosecretory cycle appears to have returned to its previous setting. These results suggest that there is some factor which can reset the neurosecretory cycle, but which in the first experiment had not had time to act before the ganglia were removed. A Hours Fig. 1. Activity of previously arrhythmic cockroach into which had been implanted suboesophageal ganglia taken from: (a) normally rhythmic cockroaches, (6) cockroaches in which the ganglion had been chilled for 4 hr. 1 V.. b V, A., Hours Fig. 2. (a) Activity of cockroaches in which suboesophageal ganglia had been chilled for 4 hr.; (6) activity of previously arrhythmic cockroaches into which the suboesophageal ganglia taken from (a) were implanted Z4 hr. after chilling. These experiments were repeated, the period of chilling being extended to 8 hr. in one group, and 18 hr. in another. The neurosecretory cycle is delayed by 8 or 18 hr. according to the treatment, as can be shown by implantation experiments. When a suboesophageal ganglion is chilled for 8 hr. and left with its normal nervous connexions there is a subsequent time-lag of 8 hr. in the phases of the
3 166 JANET E. HARKER activity rhythm of the animals (Fig. 3^). It appears that whatever factor resets the neurosecretory cycle after it had been delayed by chilling for 4 hr. does not reset the cycle after it has been delayed for 8 hr. When the activity of the animals is measured after the suboesophageal ganglion has been chilled for 18 hr. two peaks of activity appear in the next 24 hr., the larger occurring 18 hr. later than the peak in the control group, and the smaller about an hour before that of the controls (Fig. 3 c). The larger peak appears at the expected time in relation to the delayed neurosecretory cycle. Fig. 3. (a) Activity of normal cockroach; (6) activity of cockroaches after the suboesophageal ganglia had been chilled for 8 hr.; (c) activity of cockroaches after suboesophageal ganglia had been chilled for 18 hr. It has been shown (Harker, i960) that there is a stage in the neurosecretory cycle in which secretion does not normally take place, but when it can be induced by a stimulus ('possible' secretion, Figs. 4-6). It can be seen by reference to Fig. 4 that when thia stage of 'possible' secretion overlaps with the time during which the animals had begun to be active prior to chilling (as it does after 4 or 18 hr. chilling, Fig. 40, c), a peak of activity appears at this time. This represents the only peak after 4 hr. chilling, and the smaller peak after 18 hr. chilling. It is suggested that an internal rhythmical factor, unaffected by chilling of the suboesophageal ganglion, can act as a stimulus on this stage of the cycle. When the neurosecretory cycle has been delayed by 8 hr. the stage of the cycle in which no secretion can take place, even in the presence of a stimulus, coincides with the time at which the animals had been active prior to chilling, and therefore even if a stimulus occurs no peak of activity would be expected to appear (Fig. 46). The results confirm this expectation.
4 Neurosecretory cycle in Periplaneta americana L. 167 EFFECTS OF A CHANGE FROM LIGHT TO DARKNESS WHILE THE SUBOESOPHAGEAL GANGLION IS CHILLED The suboesophageal ganglia of a group of normally rhythmic animals were chilled, beginning 4 hr. before the expected appearance of the activity peak, and continuing for 4 hr. About 15 min. after chilling commenced the compound eyes and ocelli of the animals were blackened with paint. The activity rhythm of the animals was measured after their return to room temperature; the phases showed a 4 hr. timelag (Fig. 5). In the experiment described in the previous section the chining of the Light Onset of darkness 24 Fig. 4. The activity of cockroaches related (Ungrammatically to the neurosecretory cycle after the suboesophageal ganglia had been chilled for (A) 4 hr., (B) for 8 hr., (C) for 18 hr.
5 168 JANET E. HARKER ganglion for 4 hr. was not followed by a delay in the phases of the rhythm; therefore it appears that in the present experiment the new time of onset of darkness had altered the phases of the factor which stimulates neurosecretion. In order to test this supposition further the ganglia of another group of animals were chilled for 8 hr. beginning just before the activity peak was expected. After 4 hr. of the cold treatment the eyes were blackened. Since it is known from previous experiments that the secretory cycle is delayed for 8 hr. by the chilling procedure, the time when the eyes were covered (onset of darkness) coincides with that part of the neurosecretory cycle in which secretion will take place in the presence of a stimulus. The neurosecretory cells having been chilled at the time of onset of darkness are not directly affected by this stimulus, as was confirmed by implantation experiments. The animal, however, shows an activity peak 24 hr. after the onset of darkness which again suggests that a secondary factor, which can stimulate the neurosecretory cells, has had its phases reset by the onset of darkness. Onset of Darkness Fig. 5. The activity of cockroaches related diagrammatically to the neurosecretory cycle after the time of onset of darkness had occurred 4 hr. earlier than normal while the suboesophageal ganglia were being chilled for 4 hr. DISCUSSION The results show that although a light-to-darkness change in the environment immediately sets the phases of the secondary rhythm, it does not directly cause the synchronization of the neurosecretory cycle with the environmental conditions. Observations made on the effect of single environmental perturbations on wellestablished rhythms support this conclusion (Harker, i960). The value to the animal of the control of the activity rhythm by two interacting cycles may lie in the fact that the secondary cycle, although itself immediately reset by any change from light to darkness, can only affect the secretory cycle at a time
6 Neurosecretory cycle in Periplaneta americana L. 169 fairly close to that of the dark period of the preceding days. This allows for the resetting of the activity rhythm by changes in day-length, but not for resetting by light changes at abnormal times of night, unless they recur several times. In view of the small changes in light intensity needed to position the phases of a new rhythm in a previously arrhythmic animal it would appear likely that the change from bright moonlight to darkness would be sufficient to reset the secondary cycle. If the activity rhythm were also reset the animal would soon get out of phase with day and night. Light Onset of darkness 18- Fig. 6. The activity of cockroaches related diagrammatically to the neurosecretory cycle after the time of onset of darkness had occurred 4 hr. later than normal while the suboesophageal ganglia were chilled for 8 hr. SUMMARY 1. Two interacting factors, both following a 24 hr. rhythm, are found to be concerned in the control of the locomotor activity rhythm of Periplaneta americana. 2. When the suboesophageal ganglion is chilled to 3 0 C, the rest of the body being kept at room temperature, the phases of the neurosecretory cycle are delayed for a period equivalent to the period of chilling. 3. A second cycle, which follows a 24 hr. rhythm, can act as a stimulus to the neurosecretory cycle if the latter is at a stage which responds to a stimulus. If the second cycle affects the neurosecretory cycle the phases of the latter are reset by the stimulus. 4. The phases of the second cycle can be reset by a change from light to darkness while the suboesophageal ganglion is in the chilled state. It appears that the second cycle is immediately reset by the onset of darkness, regardless of the time at which this occurs. 5. The value to the animal, in its natural conditions, of the control of the locomotor rhythm by two interacting cycles is discussed.
7 170 JANET E. HARKER This work was supported by a special research grant from the Department of Scientific and Industrial Research, which is gratefully acknowledged. I wish to thank Prof. V. B. Wigglesworth for his encouragement. REFERENCES BROWN, R. H. J. & HARKER, J. E. (i960). A method of controlling the temperature of insect neurosecretory cells in situ. Nature, Lond., 185, 392. HARKER, J. E. (1956). Factors controlling the diurnal rhythm of activity of Periplaneta americana L. J. Exp. Biol. 33, 224. HARKER, J. E. (1958a). Diurnal rhythms in the animal kingdom. Biol. Rev. 33, 1. HARKER, J. E. (19586). Experimental production of midgut tumours in Periplaneta americana L. J. Exp. Biol. 35, 251. HARKER, J. E. (1960). The effect of perturbations in the environmental cycle on the diurnal rhythm of activity of Periplaneta americana L. J. Exp. Biol. 37, 154.
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