From Towards a Science of Consciousness 3 Section 5: Emotion CogNet Proceedings
The stylistic approach used in this article is somewhat unique-namely a traditional scientific report sandwiched between a short "prologue" and "epilogue." We do this to share the full text of the manuscript of our initial discovery-a contribution that was rejected by the journal Nature in September of 1997, leaving us concerned, once more, over the scientific openness of our present era. One reviewer did enthusiastically supported our effort (accepting our contribution with no major changes as a "scientifically sound" set of studies), while another rejected it outright on the basis of minor methodological concerns. At the conclusion of a harsh review, he asserted that "This is an interesting idea accumpanied by some rather bad experiments. So even though the author's conclusions may be right, it doesn't get a lot of help from the data. I am not sure that even better controlled experiments would be more convincing to all readers Even after we pointed out that most of our "flaws" were largely misinterpretations, the editor refused to reconsider his decision. Now, after a year of additional work and the world-wide broadcasting of our findings in the popular press following the Tucson III meeting (e.g., see New Scientist, May 2, 1998 (p. 14) and People magazine, June 15, 1998 (p. 105), as well as cameo appearances in "Believe it or Not" and "News of the Weird," we continue to believe that our interpretation of this robust tickling-induced vocal phenomenon in young rats is on the right track. Accordingly, we now share our initial results for the first time and we wish to do it in essentially the form that the work was originally submitted for peer review.
Abstract: In humans, laughter and giggling are objective indicators of joyful positive affect, and they occur most abundantly during playful social interactions. An understanding of such positive emotions has been hampered by the lack of simple measures of joyful social engagement in "lower" animals. Since the simplest way to induce laughter in children is tickling, we sought evidence for a comparable phenomenon in young rats by studying their ultrasonic "chirping" during vigorous bodily stimulation. Such vocalizations are common during juvenile play (Knutson, Burgdorf, and Panksepp 1998), and they can also be evoked by rapid manual stimulation (i.e., tickling). Stimulation of anterior body areas, which are especially important for arousing playfulness (Siviy and Panksepp 1987) yielded more chirping than stimulation of posterior zones, and full body stimulation with the animals in a supine position yielded the most. Analyses of these vocalizations suggest relationships to primate laughter: Tickling is a positive incentive state, as indexed by classical conditioning induced sensitization and instrumental approach tests; it is also correlated to natural playfulness and is inhibited by fearful arousal. These data suggest that a primal form of "laughter" evolved early in mammalian brain evolution, and provide a new way to study the neural sources of positive social-emotional processes (i.e., joyful affect) in other mammals.
Although laughter is a prominent behavior of the human species, reflecting our ability to experience joy and humor, only fragments of data suggest that other species have similar brain functions. Certain vocal patterns of chimpanzees (Jurgens 1986, Berntson, Boysen, Bauer, and Torrello 1989) and some lower primates (Preuschoft 1992), appear to reflect the existence of homologous processes, but credible evidence for other species is marginal (Douglas 1971, Masson and McCarthy 1996). However, considering the clinical evidence that the neural mechanisms for human laughter laughter exist in ancient regions of the brain, including thalamus, hypothalamus and midbrain (Arroyo et al. 1993, Black 1982, Poeck 1969), the existence of such processes in common laboratory species seems feasible, at least in principle. We now report evidence congruent with the presence of analogous, perhaps homologous, responses in domesticated rats.
Adult rats commonly exhibit two distinct types of ultrasonic vocalizations (USVs): Long distress-USVs in the low frequency range (peaking at around 22 KHz) reflect negative emotional arousal related to fear, social defeat and the postcopulatory refractory period (Haney and Miczek 1993, Sales and Pye 1974). On the other hand, short chirping-type USVs in the high frequency range (peaking at approximately 50 KHz) appear to index more positive forms of arousal that occur at high rates during desired social interactions (Knutson, Burgdorf, and Panksepp 1998, Sales and Pye 1974).
Human and chimpanzee laughter tends to emerge most readily in playful contexts (Rothbard 1973, Sroufe and Waters 1976, Van Hooff 1972), and the rough-and-tumble play of young rodents is accompanied by an abundance of short, high frequency USVs (Knutson, Burgdorf, and Panksepp 1998). Although such high frequency USVs have typically been studied in the context of adult sexual and aggressive encounters (Adler and Anisko 1979, Barfield and Geyer 1975, Tornatzky and Miczek 1995), they have also been noted during routine handling (Sales and Pye 1974). In the following experiments, we determined whether the type of chirping seen during play has has any resemblances to human laughter which may suggest a degree pf evolutionary kinship between the two phenomena.
The easiest way to induce primal laughter and joy in young children is through tickling. This response conditions rapidly (Newman, O'Grady, Ryan, and Hemmes 1993). After a few tickles, one can provoke social engagement and peals of laughter by provocative cues such as wiggling a finger (Rothbart 1973). We have now found that chirping at around 50 KHz is increased markedly in young rats by manual tickling and converging evidence suggests the response has more than a passing resemblance to human laughter.
First we determined whether tickling different parts of the body lead to different levels of chirping, and whether the response varies as a function of previous social experience and gender. Thirty-one Long-Evans hooded rat pups (13 males, 18 females) were weaned and individually housed at 24 days of age. Half the animals were assigned to pairs and allowed two 0.5 hr play sessions daily (alternately, in each other's home cages), while the remaining animals (n = 15) were handled an equal number of times but always left solitary in their own cages. At 41 and 55 days of age all animals were left undisturbed for 48 hrs and then observed during a 2 minute standard dyadic play encounter, during which the frequencies of two objective play activities of each animal, namely pins and dorsal contacts, as well as the number of 50 KHz chirps were monitored (Panksepp, Siviy, and Normansell 1984). Counting of chirps in all experiments was always done by a listener who was blind to experimental conditions. All testing, except as indicated, was carried out under dim (25 lux) illumination.
The next day, all animals were given standardized tickling tests. Animals were transported quietly in their home cages and placed for observation in a quiet observation enclosure. High frequency USVs were monitored with a Mini-3 Bat Detector (Ultra Sound Advice, London), tuned to detect the high USVs. High USVs were recorded during six successive 20 second test periods: 1) an initial no-stimulation baseline, 2) vigorous tickling-type manual stimulation of either the anterior or posterior, dorsal body surfaces, 3) a second baseline, 4) vigorous manual stimulation of the dorsal body surface that had not yet been stimulated (i.e., the sequence of anterior and posterior target areas being counterbalanced), 5) a final baseline, followed by 6) vigorous whole-body playful tickling (focusing on the ribs and ventral surface), with animals being repeatedly pinned 4-6 times, throughout the 15 sec. interval. For all animals, the tickling was done with the right hand and consisted of rapid finger movements across their respective body parts. Even though the stimulation was brisk and assertive, care was taken not to frighten the animal. Chirping typically started immediately at the onset of tickling.
As summarized in figure 20.1, tickling differentially invigorated chirping during all conditions, and the effects were similar at both ages (F(1,56) = .52). Full stimulation was more effective than anterior stimulation, which was more effective than posterior stimulation, which was more effective than no stimulation [overall F(2,56) = 86.8, p < .0001 for the three types of tickling, with all successive p's < .001]. This effect was larger in males than females [F(1,56) = 19.1, ps < .0001], but only marginally more effective in the socially isolated animals than in the play experienced ones [F(1,28) = 4.39, p < .05, on day 44, but not significant on day 58; data not shown]. The levels of dorsal contacts during the above play sessions on day 44 were correlated with levels of tickling-induced USVs on day 45 during posterior stimulation (r = .47, p < .01), anterior stimulation (r = .50, p < .01), and during the full simulation (r = .50, p < .01), suggesting that playfulness predicts responsivity to tickling prior to puberty. The respective correlations to number of pins were .45 (p< . 1), .38 and .20. There were no significant correlations to the recorded behaviors of the play partners. All correlations at the older test age were negligible, potentially because of the slight decline and increasing variability/seriousness in playfulness that occur after puberty (Panksepp 1981). The test-retest correlation between succeeding tickling tests separated by the two-week interval was r = .41 (p < .05) for anterior r = .45 (p < .02), posterior, and r = .57 (p < .01) for full body stimulation. Correlations in other tests using successive daily test days are typically above .75 for this measure.
An additional age comparison contrasted responses of six 17-day-old males and six 7-9-month-old males during five successive daily tests employing full-body tickling. The young animals exhibited much more chirping than the old ones during the tickle periods [48.3 (±6.9) vs 15.1 (±3.7) chirps / 15 sec, with F(1,10) = 17.87, p < .002] as well as during the intervening no-tickle periods [22.6 (±2.6) vs 0.7 (±0.4) with F(1,10) = 70.93, p < .001].
To evaluate the conditionability of the chirping response, another group of 11 male rats was weaned at 21 days of age and housed individually or 10 days prior to the start of testing. After two brief sessions to acclimate them to human handling and following five minutes of habituation to the test arena (a 48 x 38 x 30 cm high open-topped chamber, with corn-cob bedding on the floor), half the animals underwent systematic classical-conditioning, consisting of four trials as follows: 1) a 15 sec. base-line recording period, 2) a 15 sec. conditional stimulus (CS) period, 3) a 15 sec. unconditioned stimulus (UCS) period consisting of full-body tickling with repeated pinning (i.e., identical to the final condition of the previous experiment), 4) followed by a 15 sec. post-tickling period. For the six experimental animals, the conditioning procedure was conducted for 5 successive trials during three test sessions separated by at least 8 hrs. The CS was the experimenter's hand, which had a distinctive odor because of brief immersion in dry coffee grounds. The hand was used dynamically to follow each test animal around the observation chamber, with gentle touching of the face and the sides of the animal. A bout of vigorous tickling commenced 15 secs. thereafter. For the remaining control animals, the experimenter wore a leather glove dipped into the coffee grounds, but during the ensuing 15 secs, the glove was left immobile in the corner of the test chamber. Significant conditioning was evident during the very first training session (figure 20.2). The level of vocalization increased systematically during both the CS and UCS periods, but only for the experimental animals, as indicated by a significant group by trial interactions during both CS and UCS periods [F's(4,9) > 7.0, p's < .001]. This pattern was sustained during the subsequent two sessions (figure 20.3): Although there was no differential chirping during the 15 secs. prior to the CS, elevations were evident during the CS period [t(9) = 3.4, p < .01], even more marked elevations during the tickling period [t(9) = 9.2, p < .0001], and a modest differential excitement remained during the 15 sec. poststimulation period [t(9) = 2.49, p < .05]. To further evaluate the nature of the conditioning, an additional sensitization control group (n = 6) was added which received the CS unpaired with the UCS (namely with a 15 sec. interval between CS and UCS), and as is evident in figures 20.2 and 20.3, this group of animals did not show a clear acquisition curve, even though it did exhibit a reliable elevation of chirping over the no-CS group, indicating that part of the elevation of chirping to the CS is due to sensitization rather than associative conditioning. To determine whether animals would seek tickling, twenty-one 17-day-old group-housed animals were individually placed in one corner of the 48 x 38 x 30 cm high open-topped test chamber, with the experimenter's hand placed palm up in the diagonally opposite corner. When an animal approached to within 2 inches, it was given 15 secs. of tickling. Five sequential trials were conducted with 10-minute inter-trial intervals (during which animals left individually in holding cages). Animals showed significantly faster running times during this training session [F(4,20) = 4.68, p < .002], with the mean latencies being 19.2 (±3.5) secs. for the first trial and 6.9 (±1.1) secs. for the fifth trial.
To determine how negative emotional arousal would affect tickling-induced chirping, ten 37-day-old tickle-habituated animals were tested successively using four, 15 sec. test periods (baseline, full body tickle, baseline, tickle), contrasting three pairs of successive counterbalanced conditions: 1) hunger (18 hrs food deprivation) vs satiety, 2) dim (25 lux) vs bright (1000 lux) ambient illumination, and 3) exposure to predatory odors (30 mg of cat fur mixed into the bedding of the test cage) compared to unadulterated bedding. As summarized in figure 20.4, tickling elevated chirping under all conditions compared to the nontickle periods. Mild hunger marginally increased chirping [F(1,18) = 3.80, p < .07]. Bright light signficantly reduced chirping [F(1,18) = 60.82, p < .0001], with the effect being slightly larger for tickle than no-tickle periods as indexed by an interaction of the two test variables [F(1,18) = 4.80, p < .05]. Exposure to cat-smell had an even larger suppressive effect on chirping [F(1,18) = 71.56, p < .0001], but under this condition a significant interaction indicated that behavioral suppression was greater during the no-tickle period [F(1,18) = 10.28, p < .005]. We would note that chirping during such no-tickle period is largely a contextually conditioned response. Without prior tickling, chirping typically remain close to zero levels (see figure 20.2).
In additional control studies (data not shown), we determined that gentle touch did not provoke the vigrous chirping evident in figures 20.1-20.4, nor were static forms of somatosensory stimulation effective. Negative touch, such as holding animals by the scruff of the neck or by their tails strongly inhibited chirping. We have also monitored 22 KHz USVs, and they are rare during tickling. Finally, we determined whether this type of manual play would substitute for the satisfactions derived from dyadic play, as measured by the satiety that normally occurs during a half-hour play period (Panksepp, Siviy, and Normansell 1984). Manual tickling-play for 15 mins significantly reduced the ensuing amounts of social play exhibited by pairs of young rats. On the other hand, sustained artificial somatosensory stimulation (animals' bodies restrained snuggly in a hollowed foam pillow connected to a vibrator), had no such effect.
These studies support the possibility that the chirping induced in young rats by manual tickling may be homologous, or at least functionally akin, to human laughter. This conclusion is warranted because of the many similarities between the two phenomena. First, in humans, certain parts of the body are more ticklish than others (Ruggieri and Milizia 1983), and in rats chirping was intensified more by anterior rather than posterior body stimulation, which corresponds to the differential play reductions following anesthetization of dorsal body areas (Siviy and Panksepp 1987). In addition, just as the human tickling response conditions rapidly, so does tickle-induced chirping in rats. Laughter typically occurs during natural play episodes in human children (Rothbart 1973, Humphreys and Smith 1984), and in the present work, as in previous work (Knutson, Burgdorf, and Panksepp 1998), the level of tickling-induced chirping was strongly related to playful tendencies. Tickling was also a positive incentive as measured by a variety of approach and conditioning tests. Although we have yet to evaluate the hedonic qualities of the tickle-induced chirps in animals listening to such vocalizations, we note that comparable high frequency sex-related USVs in adult hamsters have been found to be attractive to conspecifics and to facilitate their sexual responsivity (Floody and Pfaff 1977).
That none of our animals seemed to interpret the tickling stimulation as aggression is indicated by the fact that, during the more than 1000 distinct tickling episodes that we have so far conducted, no young animal has become outwardly defensive. No rat has threatened or sought to aggressively bite the bare hand of the experimenter. However, there have been abundant, nonharmful, play bites. The animals that chirp the most, play the most, and they also exhibit the highest levels of play biting. To all appearances, young animals are aroused by and enjoy this type of bodily stimulation. They readily approach the hand that does the tickling, and they exhibit lots of squirming during the tickling. Many begin to react to the hand as if it were a play partner, exhibiting playful darts and pouncing interactions which appear to fulfill their biological need to play. However, some animals over two months of age have seriously challenged our attempts to tickle them.
It is also unlikely that the tickling provokes much anxiety, even though it can surely provoke some avoidance. In some children tickling can become so intense as to induce transitory avoidance, and excessive tickling has been used effectively as punishment in behavioral modification programs (Greene and Hoats 1971). Some subjectively evident approach-avoidance conflict was evident in a minority of the present animals, especially the ones that chirped least during the tickling. On the rare occassion that an animal has exhibited some apparent anxiety, they have invariably stopped chirping. Likewise, anxiogenic stimuli such as bright light and cat odor unambiguously diminish the response. Clearly, young rats do not regard the smell of a predator as anything to chirp about. The fact that this same aversive stimulus can activate 22 KHz distress calls in adults (Blanchard et al. 1990), further highlights the potential functional and neuroanatomical distinction between high and low USVs in rodents (Brudzynski and Barnabi 1996, Fu and Brudzynski 1994). The present work lends support to the idea that high and low USVs may index distinct affective states in rats.
In sum, the chirping emitted by tickled rats is a robust phenomenon. More than 95 percent of the young animal we have studied so far have unambiguously exhibited the response, but there are a few animals which chirp rarely during the stimulation. Thus, as in humans (Provine 1996), tickling responsivity appears to be traitlike, suggesting the genetic underpinnings of this reponse may be analyzed in animals. The overall responsivity of animals tends to remain stable throughout early development and is strongly related to playfulness. The slightly elevated levels of chirping in males may correspond to the oft reported elevations of rough-and-tumble playfulness in males, but it may also correspond to the elevated levels of fearfulness commonly seen in females. The onset of puberty does not appear to diminish the reponse, as indicated by the similar responsivities of 44- and 58-day-old animals, although much older animals did exhibit diminished ticklishness.
Since vigorous chirpers were more playful, perhaps one function of chirping is to signal readiness for friendly social interactions. Presumably these vocalizations come to be used in various ways as animals mature, including sexual and aggressive contexts. In the same way, childhood laughter may gradually come to serve several distinct functions in adults, ranging from good-humored social eagerness and communion to displays of dominance, triumph and even scorn. Whether chirping in rats transmits specific information between animals or simply promotes mood states that facilitate certain interactions remains unknown (Nyby and Whitney 1978). We favor the second option, and believe that the study of rodent chirping could be used to index the ongoing socio-emotional states of test animals in a variety of experimental situations.
Although Darwin noted in his The Expression of the Emotions in Man and Animals: "Laughter seems primarily to be the expression of mere joy or happiness" (p. 196), we would note that the motor expressions of laughter and the affective experience of mirth may be elaborated in distinct areas of the brain (Arroyo et al. 1993). Many neurological disorders are accompanied by reflexive laughter that is typically distressing to the patient (Black 1982, Poeck 1969). Accordingly, we would suggest that the rapid learning that occurs in this system (i.e., the conditioned chirping response), may be a better indicator for the neural sources of mirth than the unconditional chirping response. We suspect that brain circuits of human laughter and the neural underpinning of rodent chirping do interconnect with brain areas that mediate positive social feelings, but the locations of those areas remain unknown. In sum, although we would be surprised if rats have a sense of humor, they certainly do appear to have a sense of fun.
Rodent chirping may have evolutionary connections to comparable human emotional response systems. Alternatively, it may simply be a social-engagment signal that is unique to rodents. Skepticism about the existence of rodent laughter is to be expected as long as we know so little about the organization of social-emotional systems in the brains of animals, but at present we are optimistic that the intensive neurological analysis of the playful chirping of young rats may help clarify the fundamental brain sources of human laughter and joy. We suspect that both of these responses go back in brain evolution to a time when the readiness for friendly social engagment was communicated by simple acoustic signals. In any event, this work highlights the possibility of systematically analyzing friendly cross-species social interactions in the animal research laboratory. If a homology exists between joyous human laughter and rodent high frequency chirping, additional work on the topic may yield information of some clinical value. For instance, depressed individuals laugh and play less than normal; the elucidation of neurochemistries that promote chirping and playfulness in rodents may help guide development of new types of antidepressants. Also, the effect of positive emotions on many other bodily processes, such as autonomic reactivity and the vigor of immune responses, can now be studied systematically. If the chirping response has some evolutionary continuity with our human urge to laugh, it could further our understanding human emotions through the study of other animals (Panksepp 1998).
If there are evolutionary relations between human laughter and this form of rodent "laughter," we may finally have a credible strategy for systematically clarifing the nature of positive emotional consciousness within the human brain. We are now seeking to specify the brain areas and neurochemistries that mediate this positive affective response, and our preliminary work indicates that circuits situated in the reticular nuclei of the thalamus and mesencephalon are important. Also, glutamate is essential for triggering the response, since the NMDA receptor antagonist MK-801 can eliminate tickle-induced chirping.
We currently remain open to the possibility that many other mammals beside humans experience joyful affect during their playful social engagements. The vocal component of this state may have diminished through negative selection in the young of many other species, especially if it served to alert predators in the evolutionary history. Since ultrasonic calls do not travel far, such evolutionary weeding may not have transpired in burrowing species such as rats. The scenario we prefer is that the fundamental process of joy emerged early in brain evolution, even though the external signs of this central state may have diversified considerable among species. Of course, if the response only reflects convergent evolutionary processes in different species, insight into human joy are less likely to emerge from such work. However, if there is an evolutionary relationship between the joyous chirping of rats and the the joyous laughter of young children, a study of the rodent brain does provide a compelling way for us to try to understand the nature of a joyful form of affective consciousness within the human brain.
Our provisional conclusion is: Rats do laugh, and they certainly enjoy the frolicing that induces them to do so. We suspect that the nature of their positive internal affective experiences are not all that different from our own, even though the cognitive accompaniments (e.g., a sense of humor) are bound to differ markedly. We remain saddened that many of our colleagues in the prevailing scientific establishment are not more open to entertaining such possibilities. We believe that raw emotional experiences and a primitive sense of self, probably created by deep subcortical structures that all mammals share, may constitute the neural ground upon which the more figurative aspects of human consciousness were built.
Adler, N., and J. Anisko. 1979. The behavior of communicating: An analysis of the 22 KHz call of rats Rattus norvegicus. In American Zoologist 19:498-508.
Arroyo, S., et al. 1993. Mirth, Laughter and gelastic seizures. In Brain 166:757-880.
Barfield, R. J., and L. A. Geyer. 1975. The ultrasonic post-ejaculatory vocalization and the post-ejaculatory refractory period of the male rat. In Journal of Comparative and Physiological Psychology 88:723-834.
Berntson, G. G., S. T. Boysen, H.R. Bauer, and M. S. Torrello. 1989. Conspecific screams and laughter: cardiac and behavioral reactions of infant chimpanzees. In Developmental Psychobiology 22:771-887.
Black, D. W. 1982. Pathological Laughter a review of the literature. In Journal of Nervous and Mental Disease 170:67-81.
Blanchard, R. J., et al. 1990. The characterization and modelling of antipredator defensive behavior. In Neuroscience and Biobehavioral Reviews 14:463-472.
Brudzynski, S. M., and F. Barnabi, F. 1996. Contribution of the ascending cholinergic pathways in the production of ultrasonic vocalization in the rat. In Behavioral Brain Research 80:145-152.
Douglas, M. 1971. Do dogs laugh? A cross-cultural approach to body symbolism. In Journal of Psychosomatic Research 15:387-390.
Floody, O. R., and D. W. Pfaff. 1977. Communication among hamsters by high-frequency acoustic signals: III. Responses evoked by natural and syntetic ultrasounds. In Journal of Comparative and Physiological Psychology 91:820-829.
Fu, X. W., and S. M. Brudzynski. 1994. High-frequency ultrasonic vocalization induced by intracerebral glutamate. In Pharmacology, Biochemistry and Behavior. 49:835-841.
Greene, R. J., and D. L. Hoats, D. 1971. Aversive tickling: a simple conditioning technique. In Behavior Therapy 2:389-393.
Haney, M., and K. A. Miczek. 1993. Ultrasounds during agonistic interactions between female rats Rattus norvegicus. In Journal of Comparative Psychology 107:373-379.
Humphreys, A. P., and P. K. Smith. 1984. In Play in Animals and Humans. Ed., P. K.Smith. pp. 241-270 Blackwell, London.
Jürgens, U. 1986. The squirrel monkey as an experimental model in the study of cerebral organization of emotional vocal utterances. In European Archives of Psychiatry and Neurological Science 236:40-43.
Knutson, B., J. Burgdorf, and J. Panksepp. 1998. The prospect of play elicits high-frequency ultrasonic vocalizations in young rats. In Journal of Comparative Psychology 112:65-83.
Masson, J. M., and S. M. McCarthy. 1996. When Elephants Weep: The Emotional Lives of Animals. Delacorte Press, New York.
Newman, B., M. A. O'Grady, C. S. Ryan, and N. S. Hemmes. 1993. Pavlovian conditioning of the tickle response of human subjects: temporal and delay conditioning. In Perceptual and Motor Skills 77:779-885.
Nyby, J., and G. Whitney. 1978. Ultrasonic communication of adult mynomorph rodents. In Neuroscience and Biobehavioral Reviews 2:1-14.
Panksepp, J. 1981. The ontogeny of play in rats. In Developmental Psychobiology 14:327-332.
Panksepp, J. 1998. Affective Neuroscience: The Foundations of Human and Animal Emotions. New York: Oxford University Press.
Panksepp, J., S. Siviy, and L. Normansell. 1984. The psychobiology of play: theoretical and methodological perspectives. In Neuroscience and Biobehavioral Reviews 8:465-492
Poeck, K. 1969. In Handbook of Clinical Neurology, vol 3. Ed. P. J. Vinken, and G. W. Bruyn. Amsterdam: North Holland Publishing Co., 343-367.
Preuschoft, S. 1992. "Laughter" and "smile" in barbary macaques macaca sylvanus. In Ethology 91:220-236.
Provine, R. R. 1996. Laughter. In American Scientist. 84:38-45.
Rothbart, M. K. 1973. Laughter in young children. In Psych. Bull. 80:247-256.
Ruggieri, V., and M. Milizia. 1983. Tickle perception as micro-experience of pleasure: its phenomenology on different areas of the body and relation cerebral dominance. In Perceptual and Motor Skills 56:903-914.
Sales, G., and D. Pye. 1974. Ultrasonic Communication by Animals. New York: Wiley.
Siviy, S. M., and J. Panksepp. 1987. Sensory modulation of juvenile play in rats. In Developmental Psychobiology 20:39-55.
Sroufe, L. A. and E. Waters. 1976. The ontogenesis of smiling and laughter: A perspective on the organization of development in infancy. In Psych. Rev. 83:173-189.
Tornatzky, W., and K.A. Miczek. 1995. Alcohol, anxiolytics, and social stress in rats. In Psychopharmacology 121:135-144.
van Hooff, J. A. R. A. M. 1972. In Non-verbal Communication. Ed. R. A. Hinde. Cambridge: Cambridge University Press, 129-179.