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16 décembre 2004
Comp Biochem Physiol
1970; 34; 339-344
Stimulation, control and phylogenetic projection of the teleostean yawn reflex
FH McCutcheon
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia


Psychological features of sighs and yawns in man, including the yawn's "infectious" character (Ganong, 1965), have long been remarked in poetic and psychiatric literature. The function of these impositions on the rhythmic ventilation process remains obscure. The physiological role of sighs has attracted some recent attention with the study of pulmonary surfactants (Clements, 1962) and emphasis on normal alveolar distension, especially in small mammals (McCutcheon, 1953; Agostoni et al., 1959).
The role of yawns has been described in animal behavior as psychological "displacement activity", after yawns became a noteworthy element in the studies of courtship and brooding behavior of birds and especially fishes (Forselius, 1957). The physiological role of yawns appears to have attracted attention, however, only in a few species of fishes, the sea bass (Centropristes striatus) and the pinfish (Lagodon rhomboides) in particular (McCutcheon, 1958, 1966). The yawn reflex has received little attention in any terrestrial animal although yawns do occur in every class of vertebrates. In addition to those represented by the literature already cited, namely Mammalia, Ayes and Teleostij, my personal, observations include yawns in Reptilia (i.e. blacksnake, Coluber constrictor, and chameleon, Anolis carolinensis) and Amphibia (i.e. bullfrog tadpole, Rana catesbiana). This reflex may be absent in modern adult amphibians. More than 5000 frogs, toads and salamanders, including about fifteen species, have been used in our laboratories for various physiological experiments among which some yawns should have been noted or recorded if, in fact, the reflex existed in these animals. Not a single instance of yawns has been observed.
The overt features of the yawn reflex in fishes are like those in man, dog or cat; there is wide mouth gaping, body tensing and often isometric stretching or extension of appendages. Yawns can be triggered in fishes by direct manipulation of the swimbladder volume through a syringe and needle, or indirectly by manipulation of the ambient pressure (McCutcheon, 1958, 1966). The specific receptors and stimulus characteristics are not known. Yawns are correlated with the processes of swimbladder volume adjustment; that is, with the secretion-absorption and, most immediately, compression of gas. These processes can respond to less than 10 cm H20 pressure in the pinfish (McCutcheon, 1966). They compensate for volume changes which are persistent with reference to a control or "fix" level of buoyancy. However, yawns also occur in exceptional species of fishes which lack a swimbladder. Some local sea mullet or southern whiting (Menticirrhus americanus) recently added to our laboratory stock have provided our first example, and Magnuson & Prescott (1966) reported yawns in the Pacific bonito (Sarda chiliensis). Yawns in such fishes may involve the buoyancy effect of gases normally present in the intestine (Scholander, 1954), but no data are available on this subject.
Confirmation is here reported for earlier observations about the stimulating effect of imposed negative pressure on the yawn reflex in pinfish (McCutcheon, 1966). Also, evidence is provided from electrical stimulation of the pinfish brain for an extra-medullary "yawn center".
Materials and methods
Ambient pressure stimulation
The Philadelphia Aquarama provided the means to study two species of physocistous marine fishes which are typically very large (18,000 vs. 100 g) and unavailable in-shore when compared to the pinfish and sea bass previously reported. One display tank at the Aquarama, holding about 21,000 l of sea water, contained five jewfish (Promicrops itaiara), which were 74-76 cm standard length and weighed an estimated 16-18 kg, and two red snappers (Lutianus aya), which were 59-61 cm in length and weighed 11-13 kg. Two gray snappers (Lutianus griseus) and a schoolmaster (Lutianus apodus) completed the display of teleosts in the tank; these were enough like the red snappers to require no separate mention. All of these fishes were habituated to the aquarium where they had been maintained in the same tank more than 2 years. The control depth of water in the tank was 122 cm. The normal water circulation and filtering system allowed this depth to be readily altered and restored for our test purposes. It was reduced 12 cm in 5 min when a stimulus for the yawn reflex was required.
Electrical stimulation
A stanchion-like restraint and holder were made to secure the head of a pinfish in a fixed position. This provided for stereotaxic placement of a stimulating electrode the brain for a survey using conventional neurophysiological technique. The fish's brain was exposed under O 2% urethane anesthesia. The fish breathed normally in slightly urethanized aerated sea water during brain preparation and preliminary stimulation. Aeration was stpped when depressed respiration was required. A stainless wire, 0,02 cm in diameter served as a unipolar stimulating electrode. An electronic research stimulator provided current in a circuit calibrated and monitored with a cathode-ray oscilloscope.current in a circuit calibrated and monitored with a cathode-ray oscilloscope.
Twenty pinfish, 14,1-15,5 cm standard length, were examined. Stimuli of 0,5 msec duration, 20-60/sec frequency and 0-3-1 5-0 V were used. Various sites were stimulated, following a grid pattern, at successive 0,1 mm depths in each brain. Histological methods for post-mortem identification of the electrode path were not used in these exploratory studies. As the stimulation sites were tested moving posteriorly from the forebrain, unitary responses of various effectors, including upper jaw, lower jaw, operculum, eye and fin muscles, were elicited with 0,9-1,5 V, until the cerebellum was reached. Here a very low threshold, massive, lateral flick or thrusting movement of the body and tail was induced by as little as 0,3 V single shocks, a threshold one-third or less of the previous responses. Eventually, in some experiments of long duration in which respiration failed, the flick became depressed. Its threshold increased so that stimuli of O,5-2V no longer elicited a flick, but other responses which had been precluded by the flick began to appear. A site was found under these conditions in which massive yawns were induced by a stimulus of 1,6 V.This region (Fig. 1) was then explored in five fish, during a period without aeration of the sea water.
Ambient pressure stimulation
The control behavior and pressure-sensitive reactions of the jewfish and snappers were like those of the sea bass and pinfish. They each had a specific territorial site. This included the same "fix0 position" feature identified in pinfish studies; that is, a discrete place occupied with remarkable precision (less than 2 min variation in pinfish) when critical buoyancy test-adjust activity was in progress. In this vicinity the yawns occurred. The jewflsh, which is bottom oriented like the sea bass, remained resting on the bottom near the fix0 posit sometimes for an hour or more. The snapper, which like the pinfish cruises free away from the bottom, held its fix0 position only briefly and occasionally a pause from slow swimming about the tank. During periods of immobilization the fix0 position, whenever a yawn was about to occur, the dorsal fin flicked rapidly and then stood fully erect momentarily, thus signalling the end of a test-adj episode in the same way as in the sea bass and pinfish. In these larger fishes a notably in the jewfish, which has an unusually conspicuous mouth, the yawn its was even more prolonged and its consummatory character more evident.
It now seems proper to consider the yawn reflex a basic functional characteric of teleosts in general. The phylogenetic persistence of this reflex through amp bians and reptiles to birds and mammals, taken together with the homology of the swimbladder and lung, make the central control of yawns of special comparative interest. Consequently the brain of the pinfish was examined for a possible "yawn center".
Electrical stimulation
Within the region indicated on Fig. 1, full mouth gaping, abducted opercule and body-wall contraction were induced by tetanic stimulation with stimuli 0,5 msec duration at 60/sec frequency. The lowest effective strength in this circonstans was 0,85 V at 6,0 mm depth. The dorso-ventral depth of the cerebellum was ab 8,0 mm at this site. Current of 15 V would elicit a yawn at 20 mm depth. However, dorsal fin erection, a part of the normal yawn complex, did not occur until 4-6 V were applied at 3-6 mm depth.
A general muscular contraction appeared in the thoraco-lumbar body region during yawns. Progressive increase in wall tension, with marked displacement the scales over the swimbladder region, was evident during increasing stimulati of the yawn site. To confirm this movement as actual compression, a needle was inserted in the swimbladder of one preparation and connected to a small wall manometer. Stimulation by 10 V increments gave successive pressures of 0,8; 3,5; 4,4; 7,2 and l2 mm H20.
Swimbladder pressure variations are normal concomitants of buoyancy change and adjustments in fishes. Some studies have been reported on the central control of buoyancy which are consistent with a pressure-related cerebellar yawn since Long (1959) explored the brain of the carp (Cyprinus carplo) to determine if the pressure control site could be identified. He found a region of about 10 mm2 the caudal part of the tecta optica where he could, by electrical stimulation, elicited a 10-15 mm Hg pressure increase in the swimbladder. He demonstrated that compression was effected by body wall rather than swimbladder musculat Yawns were not a subject of investigation at that time. Bianki (1964) investI the role of the cerebellum in buoyancy by combining brain extirpation with conditioning experiments in the carp. He found that the cerebellum, but not forebrain, was necessary for the development of a stable conditioned reflex pressure changes in the swimbladder.
MeduIlary respiratory centers, basic to the breathing cycles, are well known in fishes HeaIey, 1957) and in every other vertebrate class. But extra-medullary respiratory centers, pneumotaxic and apneustic, are well known only in mammals, their normal role remains obscure (Lambertsen, 1961). The extra-medullary, apneustic-like character of the yawn site in pinfish suggests the possibility that an analogus role exists for the "apneustic center" in mammals; namely, to function as a "yawn center". As such, stimulated by a persistent variation from some control level of thoracic or pulmonary proprioceptive discharge, the center would act to divert the ventilation mechanism into a yawn sequence. This would serve restore proprioceptive tension, reset the control level and concomitantly stabilize the pulmonary residual air volume. The latter is important especially in those terrestrial animals with an alveolar lung in an open system, namely birds and mammaIs. Such an adaptation of the teleostean yawn reflex for a modified homeostatic role in terrestrial animals would be consistent with the way in which the phylogenetic development of breathing itself (McCutcheon, 1964) proceeded among vertebrates. Its confirmation will depend on elucidation of the yawn reflex especiaIly in reptiles and mammals.