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mise à jour du
5 juin 2003
1987; 23; 3; 367-375
Yawning, scratching, and protruded lips : differential conditionability of natural acts in Pigtail Monkeys (Macaca nemestrina)
Moutou Louboungou, James R Anderson


Most studies of learning abilities in nonhurnan primates involve operant procedures in which the subject executes motor acts on the environement in order to obtain rewards. Typically, the required response is biologically neutral. For example, selectively displacing only one of three geometric objects, or touching one of an array of previously illuminated panels do not form part of the animal's everyday behavioral repertoire. Attempts at operant conditioning of behavioral patterns found in the natural repertoire are much more rare, although a number of such studies using birds, fish and rodents have been reported. Experiments aimed at conditioning natural patterns are important for testing the generality of laws of learning formulated on the basis of traditional conditioning paradigms and may be of interest for the understanding of neuroanatomical substrates of species typical behavior.

The present paper describes three experiments in which we attempted to control the perfomance of three naturally occurring behavioral patterns in macaque rnonkeys, using food as a reinforcer. The patterns studied were scratching. the "protruded lips" facial expression, and yawning. With regard to scratching. we attempted to replicate and extend the findings from the only previous study on operant conditioning of scratching in a monkey. A facial expression was studied to examine whether this type of communicative act could be readily brought under voluntary control. The classic view of nonhuman primate facial expressions is that they are directly linked to the individual's emotional stat. The question posed in the present study was whether facial expressions were "hard-wired" responses quite resistant to external schedules of reinforcement, or whether they ressemble vocal responses. which can be operantly conditioned using food reinforcement. Yawning was included as a hypothesized intermediate pattern in the event that we succeeded in conditioning scratching but not the facial expression.

Experiment 1 : scratching

Macaques scratch themselves with their hands (the fingertips nails are rapidly and repeatedly drawn across the fur at a particular body location) or, less frequently, with their feet (like a dog). While it naturraly occurs as a response to itching, scratching also has characteristics of "a displacement activity" appearing in situations characterized by frustration or tension. Adult, group-living rhesus monkeys scratch more often in social contextss than when alone, and scratch often in close temporal association with a change of belia\ior in social contexts. Recently Iversen et al. ( 1984. Experiment 3) reported obtaining a high rate and impressive variety of scratching response in an adult male vervet monkey (Cercopithecus aethiops) when the presentation of food was made contingent upon scratching. In the present experiment, we used a different species of Old World monkey in a further assessement of' the conditionability of scratching.

The subject was a young adult male pigtail macaque (Macaca nemestrina) ("Paul") living in a large, indoor-outdoor cage with an adult female and an infant conspecific. The latter two were socially subordinate to Paul and did not interfere with the experiment. Food (dried pellets) and water were available ad libitum. Paul had been a subject in one previous experiment. inolving finding hidden food. but he was otherwise experimentally naive. 

Experimental sessions lasted 1 hr and were conducted daily. Two baseline phases, each consisting of three sessions, preceded the first conditioning phase. During the first baseline phase the experimenter simply sat in front of the subject'scage and recorded the spontaneous frequency of scratching. The same experimenter carried out all of the tests reported here. During the second baseline phase the experimenter presented 20 thin slices of fresh banana to the subject at regular intervals during each session, independent of the subject's behavior. Conditioning Phase 1 (four sessions) consisted of saying the subject's name and presenting a banana slice contingent upon a bout of scratching by the subject. Continuous reinforcement was used and the reward was given by hand. A criterion of at least four scratching movements per bout was set for an acceptable scratching response, and all responses were allowed to continue until they stopped spontaneously. A written record was made of every response.

Following, the establishment of the desired response in Phase 1, two sessions were conducted in wich reinforcement was made contingent upon the subject changing the form of the response from the preceding one. For example, if Paul scratched his back with his right hand an immediate repetition of this act went unrewarded, whereas any other form of scratching was f'ollowed by the presentation of another banana slice.

Phase 3 involved rewarding only one particular type of scratching. namely with the foot. Following some unsuccessful conditioning procedures not reported here, a final, extinction phase was conducted. This consisted of three sessions during Ahich no rewards were given to the subject.

Results : The major results are illustrated in Figure 1. Scratching was quickly and reliably brought under the control of the continuous reinforcement regime. During baseline sessions, Paul scratched himself between 19 and 27 tinies per hour, and there was virtually no effect of giving him food independent of his behavior. In contrast, in the first session of conditionning Phase 1, the rate of scratching rose to over 100 responses per hour. Response rates remained high throughout this conditioning phase, peaking at 135 in session 3.

Phase 2, in which the subject was required to change the form of scratching from one response to the next, began with an increase in the total number of scratching bouts performed but a drop in the number of rewards obtained. However, even in the first session of this new phase Paul obtained about four times more rewards (81) as there were spontaneous bouts of scratching during baseline sessions. The second session of Phase 2 produced a substantial increase in the number of rewards obtained, to 113. During conditioning Phase 1, Paul had developed a preference for scratching his right side or his back with the right hand, and in the fast two sessions of this "freestyle" phase 87% and 83% of all responses were repetitions of the response type just performed. The percentage of repetitions in the two sessions of Phase 2 was lower: 56% and 53% respectively.

Paul's reward-obtention rate remained high during the two sessions of Phase 3, in which scratching with the feet was selectively reinforced. During the last two session of the "" Phase 1, 35% and 26% of all scratching, responses were performed with a foot. The corresponding values for the two sessions of Phase 3 were 62% and 66% showing a clear increase in the occurrence of the rewarded form namely scratching with the feet.

Figure 2 shows the course of' scratching during the extinction sessions. Spontaneous recovery was evident at the start of each session, but performance became progressively weaker, until in the final two sessions there were no responses at all after 20 min.

Experiment 2 : protruded lips

There have been several attempts to operantly condition vocalization in nonhuman primates. Initial success was limited, but it is now well established that monkeys can control their vocalization rate in order to obtain food rewards. We are not aware of any previous attempts to operantly condition another major type of communicative act, namely facial expressions. One expression in the repertoire of the pigtail macaque is the protruded lips face, described by van Hoff (1967) and Redican (1975) and studied in some detail by Christopher and Gelini (1977). This expression is displayed mainly by adult males, often towards females in sexual contexts. However. it is also observed in a variety of nonsexual contexts. and may be directed towards nonconspecifics, including humans: in such cases the displaying individual appears aroused (e.g.. during geeting). We chose to study this particular expression because it is a clearly definable act which usually lasts several seconds.


The subjects were two adult male Macaca nemestrina (Bernt and Charlie) living in individual cages rileasuring 60 80 120 cm. Both were experimentailly naive, and they were tested separately. They were in visual contact with other macaques in the colony room but not with each other. Food (dried pellets) and water were available at libitum.

As in Experiment 1, two baseline phases each consisting of 3, 1 hr- long sessions were conducted. During the first baseline phase all spontaneous occurrences of the protruded lips face were recorded by the experimenter, who remained passive. The expression was recorded whether it was directed towards other monkeys or towards the experimenter. In the second baseline phase, 20 thin slices of banana were given to the subject during each session, independent of the subject's behavior.

The conditioning phase followed the final baseline. Bernt (three sessions) and Charlie (six sessions) were rewarded with a slice of' banana every time they displayed a protruded lips face, regardless of the target to which the expression was directed. Charlie then received five induction sessions in which the experimenter deliberately elicited the response by talking softly, imitating the expression, or tickling Charlie's chin. This procedure was also tried with Bernt but was soon stopped because this subject became very excited and aggressive towards neighboring monkeys.

Two final continuous reinforcement sessions were conducted with Charlie, in which all spontaneous instances of the response were rewarded with banana slices.

Results : The procedures involving food reward failed to produce any increase in the spontaneous production of the protruded lips face. Typically, fewer than ten responses were emitted during any session in which the expression was not deliberately elicited by the experimenter, with or withtout food reward. A total of 294 protruded lips faces were elicited from Charlie when the experimenter sought to provoke them and all of these were rewarded with food, but a return to conditions in which only spontaneous occurrences were followed by reward reduced to the rate of emission to baseline levels.

Experiment 3: yawning

Yawning has a particularly interesting place in the behavioral repertoire of primates. On the one hand. it is thought to be an innate response which increases the oxygen supply to the brain in a drowsy individual, though the evidence on this point is equivocal (Deputte 1978). However, its frequent appearance in social situations, and the distinction between "directed" and "undirected" forms indicates a role in communication describes yawning, as "halfway between a reflex and an expressive movement..." (p. 203), and goes on to point out that yawns can be produce volontarily by humans. The aim of experiment 3 was to determine whetether macaques could volontarily produce vawning for food rewards.

The subjects were Bernt and Charlie fom expermient 2. The six baseline sessions and the first three session from conditioning phase of experiments 2 provided baseline rates of yawning. Conditioning procedures then differed for the two subjects. In Session 1 of the conditionning pahse, Bernt trained to yawn through successi\e approximations. Every full yawning response was rewarded with a slice of banana and at first any mouth opening movement was also reinforced. Progressive approximations to the full yawning response were then required, and by the end of the first session simply opening the mouth wide went unrewarded. Charlic was rewarded from the start only for complete, naturally occurring yawns. Each subject thus received five sessions in which food reward could be obtained by yawning. These were followed by two extinction sessions in which no rewards were given, then by another continuous reinforcement session, and then finally by three extinction. sessions.

Results: As can be seen in figure 4, in both subjects yawning was rapidly brought under control using food reward. Baseline rates were between 7 and 18 per hour, rising to between 60 and 70 (Charlie) and 80 to 150 (Bernt) during the conditioning phases. Withdrawal of contingent food presentation rapidly brought yawning rates down to baseline levels. The resumption of of high rates of yawning during the reconditioning phase interposed between the two extinction phases frrther indicates that the reinforcement procedures were effective in controlling the yawning response.


The results of the present experiments indicate differential conditionability of the three natural responses studied, with scratching and yawning being quickly brought under control using food as a reinforcer, but the facial expression "protruded lips" being resistant to conditioning using equivalent operant procedures. Some implications of these findings are discussed below.

The subject rewarded with food for scratching quickly learned to emit this response in order to obtain the reward. He also frequently varied the form of scratching, and then subsequently increased the rate of a normally relatively infrequent form of scratching, namely with the feet, when these were required by the reinforcement regime. These results broadly agree with those of Iversen et al. (1984), who established that scratching could be operantly conditioned in vervet monkeys. The present results also lend support to the view that scratching is not a rigid, stimulus-bound reflex act in macaques. The fact that scratching can easily be controlled, and the finding that macaques frequently scratch around the time of a change in activity in social contexts suggest that scratching might be incorporated into the repertoire as a communicative gesture.

The attempt to operantly condition the protruded lips facial expression failed. Three possible reasons for this failure are worth mentioning briefly. First, it is conceivable that in macaques the controlling neurological mechanisms for facial expression are predominantly subcortical to the extent that voluntary control is minimal or absent. However, such an explanation seems unlikely, given the notable successes in operant conditioning of vocalizations despite the evidence for overwhelming subcortical control of vocalization in nonhuman primates. Furthermore, there exist descriptions of behavior in macaques which suggest the purposeful use of' facial expressions to obtain a goal. Bertrand (1976) reports that a hand-reared pigtail macaque used the protruded lips face to request to be let out to urinate, and Chevalier Skolnikoff (1982) describes adjustments of facial communicatory acts in stumptail macaques according to the orientation and responses of the recipient. For these reasons we favor the second possible reason for our failure to obtain a conditioned facial expression, namely that the expression-food contingency used in the present study was not conducive to learning. Clearly, not all responses are equally susceptible to food reinforcement and it is conceivable that some form of social reinforcement would be more effective than food in attempts of condition facial expressions, as has been recognized in studies with human infants. The third possible reason for our failure is related: the state of arousal accompanying the facial expression, especially experimenter-induced episodes, might have been intense enough to interfere with the establishment of an association between the act and the reward by the subject. In conclusion, the difficulty in conditioning the protruded lips face may well be attributable to some deficiency in the procedure used for this act. In any case, the experiment highlights the type of problems to be overcome in attempts to use conditioning paradigins to study the question of voluntary control of communication in nonhuman primates.

The most striking finding in the present study was the increase in yawning by the two macaques rewarded with food for each yawn. Both subjects appeared to behave in a fashi'on similar to that described by Barbizet - (1958) for humans making themselves yawn, i.e., inhaling deeply with the mouth open. Both subjects were also seen to abandon sortie attempted yawns, suggesting a deliberate effort to trigger the response.

It is possible that the high number of responses by the subject Bernt includes a proportion of "pseudo-yawns,"' similar to responses described in dogs by Konorski (1967). Pseudoyawns in dogs consisted of simple opening of the mouth. After the initial shaping trials with Bernt, however, acceptable responses were only those which contained all of the observable motoric components of a yawn, including closing the eyes and tilting the head back at the climax of the act. Further, in contrast to the successive approximation procedure used with Bernit rewards were given to the second subject only for full yawns from the start of the conditioning phase. An experienced, independent observer judged these yawns to be natural in appearance.

Along with observations of phenomena such as scratching in association with changes of social activity, directed yawning and the suppression of yawning in an adult male baboon with broken canines, the present results suggest that monkeys might well be capable of controlling the production of certain basically preprogrammed responses for social goals. A combination of naturalistic and experimental studies will be the most effective way to investigate these capacities.

« It is ironic that testosterone "the male sex hormone," is more closely associated with the yawning rate than with the mounting or intromitting rates » Charles Phoenix
Sexual steroids exert several effects on both central dopaminergic and oxytocinergic systems by acting either at the genomic or membrane level  
credit photo : "Asif A. Ghazanfar and Aristides Arrenberg"
Max Planck Institute for Biological Cybernetics
Tuebingen; Germany.
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