Blindness and play fighting in juvenile rats

Physiology & Behavior, Vol. 36, pp. 199-201. Copyright©Pergamon Press Ltd., 1986. Printed in the U.S.A.

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Blindness and Play Fighting in Juvenile Rats REX A. BIERLEY,

SANDRA L. HUGHES

AND WILLIAM

W. BEATTY

D e p a r t m e n t o f Psychology, North Dakota State University, Fargo, N D 58105 R e c e i v e d 3 J a n u a r y 1985 BIERLEY, R. A., S. L. HUGHES AND W. W. BEATTY. Blindness and play fighting in juvenile rats. PHYSIOL BEHAV 36(2) 199-201, 1986.--Play behavior of blinded and sighted juvenile rats was measured using the brief pairedencounter procedure. Dyads of sighted-sighted, blind-blind, or sighted-blind rats were observed in a large or small chamber on alternate days for ages 28 through 43 days. Blinded rats played as frequently as sighted rats regardless of pair composi2 tion or chamber size. Vision is not essential for initiating or maintaining play fighting. Vision

Play fighting

Social behavior

Juvenile rats

METHOD

P L A Y fighting is an important aspect of the social behavior of juvenile mammals of many species [1, 4, 8]. Although the functions of social play for the development of adult behavior remain a subject of much debate [1, 4, 8, 12], few contemporary workers believe that play has no long-term consequences. The neurobiological basis of play is also poorly understood (see [6,14] for recent reviews). Although hormone [2,6], pharmacological [9, 10, 15] and lesion [2,10] manipulations of neural tissue have been undertaken, we know almost nothing about how the brain directs play behavior. This is not surprising since present knowledge o f the sensory inputs that elicit and initiate play fighting is quite incomplete as well. Panksepp et al. [10] reported that subcutaneous injection o f local anesthetics into the dorsal surface of the neck and upper back reduced play fighting. This suggests that tactile inputs from this region stimulate play, but the details of their influence are not yet known. Presumably inputs from the distal sensory systems (visual, auditory, olfactory) are also important since animals must come into physical contact with one another before a play bout can begin. Somewhat surprisingly neither peripheral anosmia [14] nor olfactory bulbectomy [3] disrupt play when some animals in a play group are untreated, although play is reduced when both animals in a pair are made anosmic [14]. Thor and Holloway [14] report that juvenile rats display rapid hopping and darting movements similar to that of mature estrous females in the presence of a mature male and these movements seem to attract and engage other juveniles in play. These data indicate that visual cues might also be important in the elicitation and guidance of play behaviors. It should be noted that a distinction can be made between conditions which modulate play (e.g., light vs. darkness) and those which manipulate vision directly. We chose to study the direct contribution of vision on play elicitation by observing play behavior in blinded and sighted rats under the conditions of red illumination which are optimal for eliciting play.

Animals and Surgery Subjects were 42 male albino rats obtained from the Holtzman Co., Madison, WI at 21 days of age. It is presumed that the animals were raised under normal colony conditions at Holtzman and were therefore not play naive. Approximately 12 days after eye opening, at 23 days of age, half the rats sustained bilateral enucleation performed under Chloropent anesthesia (Fort Dodge Labs; 3 ml/kg). After the eyes were removed, the wounds were packed with Surgicell (Johnson and Johnson) to Control bleeding. Two rats in the blinded group died from respiratory failure during surgery. Since previous studies in this laboratory (e.g., [2]) indicated that there were no effects of sham operations or anesthesia on play, controls (N=21) were untreated. Throughout the experiment the rats were caged singly with free access to food and water in an air-conditioned animal room (22---3°C) that was illuminated from 0800-2100. Testing occurred during the daylight portion of the L:D cycle.

Apparatus Testing occurred in two observation chambers; both were made of plywood painted flat black with a clear plastic front. The small chamber measured 51 x 32 × 47 cm high. The large chamber measured 74×74×46 cm. Both chambers were illuminated by 2 60 W red bulbs mounted 74 cm above the floor. There is considerable evidence that rodents, including albino rats, can see in red light (see [7] for references). We chose red light because there is less disturbance of ongoing activity than with white light [5].

Procedure Two days after surgery groups of 8 rats were placed into the large chamber for 30 minutes. Each group contained both blind and sighted animals. Behavior was not scored as the purpose of this procedure was to accustom the blind rats to moving about the environment and socially interacting in the

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absence of sight. This procedure was repeated on the next 2 days. Starting on the next day (Day 28) and continuing for 16 days the rats were tested in pairs for 10 min each day. On alternate days testing occurred in the large and small chambers. Test pairs consisted of 2 blind rats (B-B, N=6), 2 sighted rats (S-S, N=7) or 1 sighted and 1 blind rat (B-S, N =7). Once formed the pairs remained intact for the duration of the experiment. During the experiment one blind rat from a B-S pair and one sighted rat from an S-S pair developed respiratory disease. Data from these pairs were excluded leaving 6 pairs in each condition. Two observers recorded the number of pins (one rat has its dorsal surface to the floor with the other rat standing over it) and rears (paws raised at least 1 cm off the floor). Each observer scored I rat; the particular rat of the pair scored by each observer was counterbalanced across sessions. This procedure seemed warranted because interrater reliabilities were high (r=0.97 for pins; r=0.98 for rears) when two observers scored the same rats during a single session.

TABLE 1 MEAN* AND STANDARDERROR OF THE ME/~ OF PEREORMANCE FOR PAIRS OF BLIND AND SIGHTED RATS Treatment Arena Size

B-B

B-S

S-S

Pins Small

29.94 2.60

27.22 2.06

37.13 2.69

Large

29.11 1.91

23.84 1.89

36.45 2.80

Rears Small

34.55 2.54

40.05 2.52

39.54 2.00

Large

29.36

29.48

28.34

1.65

1.56

1.67

RESULTS As seen in Table 1, neither blinding nor the size of the observation cage exerted major influences on pins or rears. Data for total pins and total rears per pair were subjected to a mixed model A N O V A (3 vision conditions x 2 observation cages x 8 sessions). The main effect of vision condition (S-S, B-B or B-S) was not significant for either pins or rears (both F < 1). There was no observation cage (small vs. large) effect for pins, F(1,45)=2.30, p>0.05, but the observation cage effect was significant for rears, F(1,45)=15.05, p<0.001. Examination of the data revealed that animals in all vision conditions reared more in the small cage during the first three sessions of testing but not thereafter. Since the cage x sessions interaction was not significant ( F < I ) and the cage effect disappeared after three sessions little significance can be attached to this finding. The main effect of sessions as significant for both pins, F(7,315) =4.76, p <0.001, and rears, F(7,315)=7.25, p<0.001. The data for pins showed the typical age related inverted U pattern reported by Panksepp, Jalowiec, DeEskinazi and Bishop [9]. There was no consistent pattern in the rears data; rears were relatively high on sessions 1 and 4 and relatively low on sessions 5 and 6 accounting for the overall significant F. Interactions for vision condition x sessions and vision condition × cage were not significant for either pins (both F ~< 1.34) or rears (both F < 1). A similar analysis (2 vision conditions × 2 observation cages × 8 sessions) was conducted for the subjects in the mixed pair (B-S) group. This analysis yielded the same pattern of results reported above. Blind rats pinned and reared as frequently as their sighted partners. DISCUSSION The occurrence of a play bout obviously requires that information about the location (and possibly other characteristics) of potential play partners be received and processed by the animal that ultimately initiates the encounter. While somatosensory inputs from the neck appear to play an important role in arousing play fighting once the animals make contact [9], it seems clear that information from one or more of the distal sensory systems must be involved as well. The present findings demonstrate that the integrity of the visual system is not essential to normal play fighting. Several features of the present experiment make this a

*Values are the average for 8 tests in each arena.

relatively strong conclusion. First, tests were conducted using socially deprived animals. Social deprivation strongly stimulates play fighting among juvenile rats [ 10,15] creating conditions that are maximally sensitive to detecting a deficit in play. Under nearly identical testing conditions we and others have observed deficits on various indices of play fighting including pinning following administration of many different drugs [10,15]. Second, blind rats played as frequently as sighted controls even when both partners were blind. Under these conditions any decrease in play initiation by a blind rat could not be masked by a compensatory increase in play by its sighted partner. In fact no such changes occurred among the mixed pairs. Finally, blindness had no effect on play even when tests were conducted in the large arena which was sufficiently spacious so that adventitious contacts between play partners were unlikely. Clearly vision is not necessary for normal play in juvenile rats. Earlier work indicates that olfaction is probably not critical either. When play is studied in mixed pairs (one intact and one anosmic rat) or in a group cage containing 3-4 anosmic rats and a like number of intact controls, neither olfactory bulbectomy nor infusion of zinc sulfate affects play [3,14]. Some influence of olfaction cannot be ruled out since when both partners are rendered anosmic by zinc sulfate treatment, play is significantly reduced [14]. Recently Siviy and Panksepp (personal communication) have observed that peripheral deafening reduces play fighting suggesting that among the distal senses audition may be the most important for controlling this behavior. Assuming Panksepp's findings are reproducible they may imply that juvenile rats emit some sort of vocalization that invites others to play. While explicit play signals have not been described in the rat, they are known to exist among rhesus monkeys [13]. To the human observer rat play bouts are usually silent events. The only sound is an occasional squeal after a particularly vigorous round of pinning or mouthing of the neck. However, many of the vocalizations made by rats during mating and other social interactions are ultrasonic and hence inaudible to humans [8,11]. Panksepp's recent observations concerning the play of deafened rats suggest that the

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search for ultrasonic vocalizations in the context of juvenile play might prove quite rewarding. As noted in the introduction, a clear distinction can be made between lighting conditions that modulate play and manipulations that mediate visual cues. In the current study, rats were tested under conditions that have proven optimal for facilitating play. Since rats are nocturnal creatures, it is not surprising that red lighting, which minimally reduces darkness, is ideal for observing play. Panksepp et al. [10] have reported that white light significantly depresses play. A reasonable prediction is that this modulatory effect would

not be exerted on blind rats. That is, blinded rats might actually play more than sighted rats under conditions of white light. Such an outcome would be consistent with the current finding that visual detection of a play partner is not necessary to initiate play. ACKNOWLEDGEMENTS Supported by NSF Grant BNS 82-01448. We wish to thank Evelyn Butcher and L. Joy Johnson for aiding in the. preparation of the manuscript.

REFERENCES

1. Aldis, O. Play Fighting. New York: Academic Press, 1975. 2. Beatty, W. W. Hormonal organization of sex differences in play fighting and spatial behavior. In: Sex Differences in the Brain: The Relation Between Structure and Function, edited by G. J. De Vries, J. P. C. De Bruin, H. B. M. Vylings and M. A. Corner. Prog Brain Res 61: 315-330, 1984. 3. Beatty, W. W. and K. B. Costello. Olfactory bulbectomy and play fighting in juvenile rats. Physiol Behav 30: 525-527, 1983. 4. Fagen, R. Animal Play Behavior. New York: Oxford, 1981. 5. Finley, R. B., Jr. Observation of nocturnal animals by red light. J Mammal 40: 591-594, 1959. 6. Meaney, M. J. and J. Stewart. A descriptive study of social development in the rat (Rattus Norvegius). Anim Behav 29: 34--45, 1981. 7. McCormack, C. E. and C. R. Sontag. Entrainment by red light of running activity and ovulation rhythms of rats. Am J Physiol 239: R450-R454, 1980. 8. Noirot, E. Selective priming of maternal responses by auditory and olfactory cues from mouse pups. Dev Psychobiol 5: 371387, 1972.

9. Panksepp, J., J. Jalowiec, F. G. DeEskinazi and P. Bishop. Opiates and play dominance in juvenile rats. Behav Neurosci 99: 441--453, 1985. 10. Panksepp, J., S. Siviy and L. Normansell. The psychobiology of play: Theoretical and methodological considerations. Neurosci Biobehav Rev 8: 465-492, 1984. 11. Sewell, G. D. Ultrasonic signals from rodents. Ultrasonic 8: 26-30, 1970. 12. Smith, P. K. Does play matter? Functional and evolutionary aspects of animal and human play. Behav Brain Sci 5: 139-184, 1982. 13. Symons, D. Play and Aggression: A Study of Rhesus Monkeys. New York: Academic Press, 1978. 14. Thor, D. H. and W. R. Holloway, Jr. Anosmia and play fighting behavior in prepubescent male and female rats. Physiol Behav 29: 281-285, 1982. 15. Thor, D. H. and W. R. Holloway, Jr. Social play in juvenile rats: A decade of methodological and experimental research. Neurosci Biobehav Rev 8: 455-464, 1984.