Developmental Changes in Open-Field Behavior in the Kitten C. J. FREDERICKSON M. H. FREDERICKSON Program in Psychology and Human Development University of Texas at Dallas Richardson, Texas Seventy-eight kittens from 3 to 7 weeks of age were studied in an open-field arena. Three major agedependent changes were noted: (1) the number of floor squares entered was markedly higher for 5- and 6-weekalds than for younger animals, and slightly lower for 7-week-olds than for 5- and 6-week-olds; (2) the tendency to backtrack from 1 square to a just-vacated square decreased with age, the largest change occurring between 4 and 5 weeks of age; (3) the within-session decrement in locomotion was largest for 3-week-old kittens but was smallest for 4-week-olds and increased monotonically with age thereafter. The results suggest a possible role of hippocampal maturation.
Considerable evidence indicates that certain aspects of locomotor behavior in a novel environment are at least partially controlled by hippocampal function (for reviews and references see: Altman, Brunner, & Bayer, 1973; Jarrard, 1973; Kimble, 1975). Although these aspects may be absent if the lesions are small or restricted to the dorsal hppocampus (Hostetter & Thomas, 1967; Jarrard, 1968; Lanier & Isaacson, 1975; Nadel, 1968), the locomotor symptoms w h c h typically distinguish the behavior of the hippocampal-damaged animal in a novel environment are as follows. (1) Compared to normals, the hippocampal-damaged animals tend to exhibit more back-and-forth “repetitive” perambulation within the test arena (Eichelrnan, 197 1 ; Kimble, 1963). (2) The total number of open-field squares or maze arms entered by hippocampal-damaged animals tends to exceed the number entered by control animals (Jarrard, 1968; Lanier & Isaacson, 1975; Means, Leander, & Isaacson, 1971; Strong & Jackson, 1970). (3) Compared to controls, hippocampal animals tend to show reduced habituation of locomotor activity either within a session (Means etal., 1971; Roberts, Dember, & Brodwick, 1962) or between successive sessions (Eichelman, 1971; Leaton, 1965) in most, if not all (Jarrard, 1968) test environments. If the hippocampus of a neonatal animal is dysfunctional due to the absence of mature dentate granule cells (Altrnan et al., 1973; Douglas, 1975), then the neonatal Reprint requests should be sent to Dr. Christopher J. Frederickson, Program in Psychology and Human Development, University of Texas at Dallas, Box 688, Richardson, Texas 75080, U.S.A. Received for publication 16 December 1977 Revised for publication 9 September 1978 Developmental Psychobiology, 12(6):623-628 (1979) 0 1 9 7 9 by John Wiley & Sons, Inc.
0012-1 630/79/0012-0623$01 .00
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animal should show in the open field the same 3 symptoms exhibited by the hippocampal-damaged adult animal, namely, repetitive patterns of locomotion, excessive amounts of locomotion, and depressed habituation of locomotion. ‘The present study was undertaken to determine whether young kittens do behave like hippocampaldamaged adults in the open field and, if so, to determine the age at which the hippocampal symptoms might abate.
Methods The subjects were 78 mongrel kittens (Felis domesticus) brought to the laboratory by owners who could provide the exact day (+12 hr) of birth. Upon arrival at the laboratory, each litter was placed in a small room and left undisturbed with its mother for 1 5 min. Some of the kittens (n = 71) run in the open field were also run in a spontaneous alternation test (Frederickson & Frederickson, 1979) immediately prior to the open field test; the remainder of the kittens were tested only in the open field and were taken directly from the litter to the open field. No kitten was separated from its litter and mother for more than 20 min. For open-field testing, each kitten was placed in the center of a well-lighted enclosed room (6 X 7 m), the carpeted floor of which was divided into 30 rectangles (45 X 64 cm) marked by tape on the floor. For 5 min the animal’s locomotion about the room was observed through a I-way mirror and traced onto a paper sheet divided into squares corresponding to the squares marked on the observation loom floor. A crossing was indicated on the tracing sheet when all 4 of the animal’s feet were placed in a square, and time marks were placed on the paths at 15-sec intervals. Three scores were computed from the tracing record for each animal: a score for total activity, which was simply the total number of square crossings in the 5-min period; a score for habituation of locomotion, which was the number of crossings in the 5th min divided by the number of crossings in the 1st min; and a measure of repetitive or back-and-forth spatial patterns of locomotion, called a backtracking index. The latter index was calculated from the 5-min records as the number of times the animal crossed back into either the last or penultimate square that it had just vacated, divided by the number of square-crossings that led the animal into some other square.
Results Clear, qualitative differences existed in locomotor behavior among the various age groups. The 3-week-old animals walked slowly and unsteadily with their heads sometimes wobbling from side to side and their noses frequently tapping the carpet. The paths traversed by these youngest animals tended to be consistently short and circuitous (Fig. 1). Four-week-old animals were typically steadier on their feet than the 3-week-old animals, but most behaved essentially like 3-week-olds and covered only short and circuitous paths. However, a few 4-week-olds did make at least 1 long direct excursion across the open-field arena. By 5 weeks of age the coordination of locomotion was strikingly improved: animals 5 weeks and older made numerous rapid and direct excursions around and across the arena.
OPEN-FIELD BEHAVIOR OF KITTENS
r/
625
LOCOMOTION
3 weeks
4 weeks
5 weeks
7 weeks
Fig. 1 . Four illustrative paths of locomotion are shown for 4 animals. The circles mark the starting points; cross marks o n the paths denote S s e c intervals. Paths shown for the 3-, 5-, and 7-week-old animals are representative of those age groups; the path shown for the 4-week-old animal is typical of only a few animals of that age that walked a fairly direct path. In this and the following figures, “3 weeks” means 21 days of age ( + I 2 hours), “4 weeks” 28 days, and so forth.
The quantitative analysis of number of square-crossings generally confirmed the qualitative differences observed among age groups. The total activity varied significantly with Age (an analysis of variance [ANOVA] across age and successive minutes; Age: F = 7.3, df = 4/73, p < .OOl), with the major difference occurring between the relatively inactive 3- and 4-week-old group and the vigorously active 5-, 6-, and 7-week-olds (Fig. 2A). Circuitous or repetitive patterns of locomotion, as measured by the back-crossing index, also varied significantly with age (1-way ANOVA; F = 5.98, df= 4/73, p < .OOl), the major change being a large decrease in back-crossing between the ages of 4 and 5 weeks (Fig. 2B). Finally, the extent of habituation or decrease in locomotion within the 5-min test period also varied with age. Though all age groups showed some decrement in activity across the 5-min period (Age X Minutes ANOVA; for minutes: F = 7.24, df= 4/292, p < .OOl), the Age X Minutes interaction was significant ( F = 2.25, df= 16/292, p < .Ol), and the activity-decrement scores for the 4- and 5-week-old animals were substantially lower than those for the other age groups (Fig. 2C).
Discussion Of the 3 locomotor symptoms expected for animals with immature hippocampiexcessive amountis of locomotion, repetitive patterns of locomotion, and reduced habituation of locomotion-only the latter 2 seem characteristic of young kittens. In the present study, as in prior studies with kittens (Buchwald, Hull, Levine, & Villablanca, 1976) and rat pups (Candland & Campbell, 1962; Livesley & Egger, 1970;
626
FREDERICKSON AND FREDERICKSON
Williams, Carr, & Peterson, 1966) the major developmental change in total amount of open-field locomotion was not a decrease but a marked increase. Presumably, the increasing strength and steadiness of gait (Rosenblatt, 1971), correlated with maturing spinal and supraspinal motor systems (Buchwald et al., 1976; Villablanca & Olmstead, 1979), is a major factor determining the total locomotion (distance traversed) by a preweanling in an open-field test. The slight drop in total locomotion seen at 7 weeks in the present work could possibly be taken as evidence of an emerging hippocampalbased tendency to suppress open-field activity (Altman er al., 1973; Douglas, 1975). However, any tendency to suppress or decrease open-field locomotion which might be developing in 3-to-7-week-old kittens is, clearly, confounded with opposing changes which tend to increase locomotion. Habituation of locomotion (Bronstein, Neiman, Wolkoff, & Levine, 1974) and of exploratory nose-poking (Williams, Hamilton, & Carlton, 1975) have both been shown to emerge at about the time of presumed maturation of hippocampal function in rat pups. If the large within-session decrement in activity seen in the 3-week-old kittens in the present study can be attributed to fatigue, rather than habituation as is suggested by the observations that their walking was quite weak and unsteady and that 3-week-old kittens show no between-session habituation of open-field locomotion (Candland & Nagy, 1969), then the present results parallel the data for rats and are consonant with the notion that emerging hippocampal function at 5-6 weeks of age could account for the emergence of within-session habituation of locomotion in the kitten. Also consonant with the notion of emerging hippocampal function at 5-6 weeks in kittens are the present findings with spatial patterns of locomotion: animals 3 and 4 weeks old showed much more of the repetitive, back-and-forth locomotion symptomatic
A
1.0
l r l r l 3 4 5 6 7
3 4 5 6 7 AGE
IN WEEKS
Fig. 2. A . The average numbers of squares entered by each age group are plotted. The values for both the 3- and 4-week-old animals were significantly lower than those for 5-, 6-, and 7-week-olds 0, < .01, Duncan’s multiple range test); the value for the 7-week group is significantly lower than that for both the 5 - and 6-week-old groups 0, < .01). N s for the age groups are: 3 weeks, 13; 4 weeks, 23; 5 weeks, 1 7 ; 6 weeks, 12; 7 weeks, 13. Vertical bars in all figures show standard errors of means. B . Mean back-crossing index (number of back-crossings/number of non-back-crossings) for each age group; values for both the 3- and 4-week-old groups are significantly higher than those for 5 - , 6-, and 7-week-olds ($ < .05, Duncan’s multiple range lest). C. Mean decrement ratio (crossings in 5th minute/crossings in 1st minute) for each age group. Valucs for 4- and 5-week-old animals are significantly lower than those for 3-week-olds (p < 3 2 , 2-tailed t test) and less than those for both 6- and 7-week-olds 0, < .05, I-tailed t test)
OPEN-FIELD BEHAVIOR OF KITTENS
627
of hippocampal dysfunction (Eichelman, 1971; Kimble, 1963) than did animals 5 weeks old and older. Rosenblatt (1971) has suggested that the developmental shift from back-and-forth or circuitous paths to more direct paths of walking in kittens might reflect, in part, a shift from olfactory to visual guidance of locomotion. Although improvements in the visual acuity (Thorn, Gallender, & Erickson, 1976) and visually guided behaviors (Villablanca & Olmstead, 1979) occur through the 1st 2 months of life in kittens, the decrease in back-crossing behavior observed in the present study may not have been due entirely to the maturation of the visual system. First, visually guided behaviors such as walking after the mother cat (Rosenblatt, 1971), responding to a visual cliff (Gibson & Walk, 1960), and following a spot of light (Villablanca & Olmstead, 1979) all appear by 3 4 weeks in kittens, whereas the back-crossing behavior observed here did not decrease until 5 weeks of age. Second, although visual guidance may be necessary to avoid repetitive patterns of locomotion, the repetitive locomotor behavior of the hippocampal-damaged adult rat (Eichelman, 1971; b b l e , 1963) suggests that vision (in the absence of the hippocampus) is not sufficient to prevent repetitive patterns of locomotion in the open field. Three behavioral changes which could be manifestations of the emergence of hippocampal function at 5-6 weeks of age in kittens have been identified in this and a preceding report (Frederickson & Frederickson, 1979): the onset of spontaneous alternation, a decrease of repetitive patterns of locomotion, and an increase in within-session habituation of open-field locomotion. A 4th behavioral change suggesting emerging hippocampal function at about that same age is the marked improvement in passive avoidance behavior seen between 25 and 50 days of age in kittens (Davis & Jensen, 1976). An interesting question for future work will be whether identifiable anatomical, biochemical, or physiological changes in kitten hippocampus coincide with the sudden behavioral changes observed at 5-6 weeks of age.
Notes This work was supported in part by a grant from the H. S. Moss Foundation, and NIMH Grant l-RO3-MG29835.
References Altman, J., Brunner, R. L., and Bayer, S. A. (1973). The hippocampus and behavioral maturation. Behav. Biol., 8: 557-596. Bronstein, P. M., Neiman, H., Wolkoff, F. D., and Levine, M. J. (1974). The development of habituation in the rat. Anim. Learn. Behav., 2 : 92-96. Buchwald, N. A., Hull, C. D., Levine, M. S., and Villablanca, J. R. (1976). Developmental assessment of intact and brain-lesioned kittens. In M. A. B. Brazier and F. Coceani (eds.), Brain Dysfunction in Infantile Febrile Convulsions. New York: Raven Press. Pp. 166-177. Candland, D. K., and Campbell, B. A. (1962). Development of fear in the rat as measured by behavior in the open-field. J. Comp. Physiol. Psych., 55: 593-596. Candland, D. K., and Nagy, Z. M. (1969). The open field: Some comparative data. Ann. N.Y. Acad. Sci., 159: 831-851. Davis, J. L., and Jensen, R. A. (1976). The development of passive and active avoidance in learning in the cat. Dev. Psychobiol., 9: 175-179.
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Douglas, R. J. (1975). The development of hippocampal function: Implications for theory and therapy. In R. L. Isaacson and K. H. Pribram (eds.), The Hippocampus. Volume 2. Neurophysiology and Behavior. New York: Plenum Press. Pp. 327-361. Eichelman, B. S. (1971). Effect of subcortical lesions on shock-induced aggression in the rat. J. Comp. Physiol. Psych., 74: 331-339. Frederickson, C . J., and Frederickson, M. H. (1979). Emergence of spontaneous alternation in the kitten. Dev. Psychobiol., 12: 615-621. Gibson, E. J., and Walk, R. D. (1960). The visual cliff. Sci. Am., 202: 64-71. Hostetter, G . , and Thomas, G. J. (1967). Evaluation of enhanced thigmotaxis as a ccondition of impaired maze learning by rats with hippocampal lesions. J. Comp. Physiol. Psych., 63: 108-110. Jarrard, L. E. (1968). Behavior of hippocampal lesioned rats in home cage and novel situations. Physiol. Behav., 3: 65-70. Jarrard, L. E. (1973). The hippocampus and motivation. Psych. Bull., 79: 1-12. Kimble, D. P. (1963). The effects of bilateral hippocampal lesions in rats. J. Cornp. Physiol. Psych., 56: 273-283. Kimble, D. P. (1975). Choice behavior in rats with hippocampal lesions. In R. L. Isaacson and K. H. Pribram (eds.), The Hippocampus. Volume 2: Neurophysiology and Behavior. New York: Plenum Press. Pp. 327-361. Lanier, L. P., and Isaacson, R. L. (1975). Activity changes related to the location of lesions in the hippocampus. Behav. Biol., 13: 59-69. Leaton, R. N. (1965). Exploratory behavior in rats with hippocampal lesions. J . Cornp. Physiol. Psych., 59: 325-330. Livesey, P. J., and Egger, G . J. (1970). Age as a factor in open-field responsiveness in the white rat. J. Comp. Physiol. Psych., 73: 93-99. Means, L. W., Leander, J. D., and Isaacson, R. L. (1971). The effects of hippocarnpectomy on alternation behavior and response to novelty. Physiol. Behav., 6: 17-22. Nadel, L. (1968). Dorsal and ventral hippocampal lesions and behavior. Physiol. Behav., 3: 891-900. Roberts, W. W., Dember, W. N., and Brodwick, M. (1962). Alternation and exploration in rats with hippocampal lesions. J. Comp. Physiol. Psych., 55: 695-700. Rosenblatt, J. S . (1971). Suckling and home orientation in the kitten: A comparative developmental study. In E. Tobach, L. R. Aronson and E. Shaw (eds.), The Biop,FychoZogy of Developmenf. New York: Academic Press. Pp. 345-41 1. Strong, P. N., and Jackson, W. J. (1970). Effects of hippocampal lesions in rats on three measures of activity. J. Comp. Physiol. Psych., 70: 60-65. Thorn, F., Gallender, M., and Erickson, P. (1976). The development of the kitten's visual optics. Vis. Res., 16: 1145-1149. Villablanca, J. R., and Olrnstead, C. E. (1979). Neurological development of kittens. Dev. Psychobiol., 12: 101-127. Williams, C. D., Carr, R . M., and Peterson, H. W. (1966). Maze exploration in young rats of four ages. J. Genet. Psych., 109: 241-247. Williams, J. M., Hamilton, L. W., and Carlton, P. L. (1975). Ontogenetic dissociation of two classes of habituation. J. Comp. Physiol. Psych., 89: 733-737.
Considerable evidence indicates that certain aspects of locomotor behavior in a novel environment are at least partially controlled by hippocampal function (for reviews and references see: Altman, Brunner, & Bayer, 1973; Jarrard, 1973; Kimble, 1975). Although these aspects may be absent if the lesions are small or restricted to the dorsal hppocampus (Hostetter & Thomas, 1967; Jarrard, 1968; Lanier & Isaacson, 1975; Nadel, 1968), the locomotor symptoms w h c h typically distinguish the behavior of the hippocampal-damaged animal in a novel environment are as follows. (1) Compared to normals, the hippocampal-damaged animals tend to exhibit more back-and-forth “repetitive” perambulation within the test arena (Eichelrnan, 197 1 ; Kimble, 1963). (2) The total number of open-field squares or maze arms entered by hippocampal-damaged animals tends to exceed the number entered by control animals (Jarrard, 1968; Lanier & Isaacson, 1975; Means, Leander, & Isaacson, 1971; Strong & Jackson, 1970). (3) Compared to controls, hippocampal animals tend to show reduced habituation of locomotor activity either within a session (Means etal., 1971; Roberts, Dember, & Brodwick, 1962) or between successive sessions (Eichelman, 1971; Leaton, 1965) in most, if not all (Jarrard, 1968) test environments. If the hippocampus of a neonatal animal is dysfunctional due to the absence of mature dentate granule cells (Altrnan et al., 1973; Douglas, 1975), then the neonatal Reprint requests should be sent to Dr. Christopher J. Frederickson, Program in Psychology and Human Development, University of Texas at Dallas, Box 688, Richardson, Texas 75080, U.S.A. Received for publication 16 December 1977 Revised for publication 9 September 1978 Developmental Psychobiology, 12(6):623-628 (1979) 0 1 9 7 9 by John Wiley & Sons, Inc.
0012-1 630/79/0012-0623$01 .00
624
FREDERICKSON AND FREDEFUCKSON
animal should show in the open field the same 3 symptoms exhibited by the hippocampal-damaged adult animal, namely, repetitive patterns of locomotion, excessive amounts of locomotion, and depressed habituation of locomotion. ‘The present study was undertaken to determine whether young kittens do behave like hippocampaldamaged adults in the open field and, if so, to determine the age at which the hippocampal symptoms might abate.
Methods The subjects were 78 mongrel kittens (Felis domesticus) brought to the laboratory by owners who could provide the exact day (+12 hr) of birth. Upon arrival at the laboratory, each litter was placed in a small room and left undisturbed with its mother for 1 5 min. Some of the kittens (n = 71) run in the open field were also run in a spontaneous alternation test (Frederickson & Frederickson, 1979) immediately prior to the open field test; the remainder of the kittens were tested only in the open field and were taken directly from the litter to the open field. No kitten was separated from its litter and mother for more than 20 min. For open-field testing, each kitten was placed in the center of a well-lighted enclosed room (6 X 7 m), the carpeted floor of which was divided into 30 rectangles (45 X 64 cm) marked by tape on the floor. For 5 min the animal’s locomotion about the room was observed through a I-way mirror and traced onto a paper sheet divided into squares corresponding to the squares marked on the observation loom floor. A crossing was indicated on the tracing sheet when all 4 of the animal’s feet were placed in a square, and time marks were placed on the paths at 15-sec intervals. Three scores were computed from the tracing record for each animal: a score for total activity, which was simply the total number of square crossings in the 5-min period; a score for habituation of locomotion, which was the number of crossings in the 5th min divided by the number of crossings in the 1st min; and a measure of repetitive or back-and-forth spatial patterns of locomotion, called a backtracking index. The latter index was calculated from the 5-min records as the number of times the animal crossed back into either the last or penultimate square that it had just vacated, divided by the number of square-crossings that led the animal into some other square.
Results Clear, qualitative differences existed in locomotor behavior among the various age groups. The 3-week-old animals walked slowly and unsteadily with their heads sometimes wobbling from side to side and their noses frequently tapping the carpet. The paths traversed by these youngest animals tended to be consistently short and circuitous (Fig. 1). Four-week-old animals were typically steadier on their feet than the 3-week-old animals, but most behaved essentially like 3-week-olds and covered only short and circuitous paths. However, a few 4-week-olds did make at least 1 long direct excursion across the open-field arena. By 5 weeks of age the coordination of locomotion was strikingly improved: animals 5 weeks and older made numerous rapid and direct excursions around and across the arena.
OPEN-FIELD BEHAVIOR OF KITTENS
r/
625
LOCOMOTION
3 weeks
4 weeks
5 weeks
7 weeks
Fig. 1 . Four illustrative paths of locomotion are shown for 4 animals. The circles mark the starting points; cross marks o n the paths denote S s e c intervals. Paths shown for the 3-, 5-, and 7-week-old animals are representative of those age groups; the path shown for the 4-week-old animal is typical of only a few animals of that age that walked a fairly direct path. In this and the following figures, “3 weeks” means 21 days of age ( + I 2 hours), “4 weeks” 28 days, and so forth.
The quantitative analysis of number of square-crossings generally confirmed the qualitative differences observed among age groups. The total activity varied significantly with Age (an analysis of variance [ANOVA] across age and successive minutes; Age: F = 7.3, df = 4/73, p < .OOl), with the major difference occurring between the relatively inactive 3- and 4-week-old group and the vigorously active 5-, 6-, and 7-week-olds (Fig. 2A). Circuitous or repetitive patterns of locomotion, as measured by the back-crossing index, also varied significantly with age (1-way ANOVA; F = 5.98, df= 4/73, p < .OOl), the major change being a large decrease in back-crossing between the ages of 4 and 5 weeks (Fig. 2B). Finally, the extent of habituation or decrease in locomotion within the 5-min test period also varied with age. Though all age groups showed some decrement in activity across the 5-min period (Age X Minutes ANOVA; for minutes: F = 7.24, df= 4/292, p < .OOl), the Age X Minutes interaction was significant ( F = 2.25, df= 16/292, p < .Ol), and the activity-decrement scores for the 4- and 5-week-old animals were substantially lower than those for the other age groups (Fig. 2C).
Discussion Of the 3 locomotor symptoms expected for animals with immature hippocampiexcessive amountis of locomotion, repetitive patterns of locomotion, and reduced habituation of locomotion-only the latter 2 seem characteristic of young kittens. In the present study, as in prior studies with kittens (Buchwald, Hull, Levine, & Villablanca, 1976) and rat pups (Candland & Campbell, 1962; Livesley & Egger, 1970;
626
FREDERICKSON AND FREDERICKSON
Williams, Carr, & Peterson, 1966) the major developmental change in total amount of open-field locomotion was not a decrease but a marked increase. Presumably, the increasing strength and steadiness of gait (Rosenblatt, 1971), correlated with maturing spinal and supraspinal motor systems (Buchwald et al., 1976; Villablanca & Olmstead, 1979), is a major factor determining the total locomotion (distance traversed) by a preweanling in an open-field test. The slight drop in total locomotion seen at 7 weeks in the present work could possibly be taken as evidence of an emerging hippocampalbased tendency to suppress open-field activity (Altman er al., 1973; Douglas, 1975). However, any tendency to suppress or decrease open-field locomotion which might be developing in 3-to-7-week-old kittens is, clearly, confounded with opposing changes which tend to increase locomotion. Habituation of locomotion (Bronstein, Neiman, Wolkoff, & Levine, 1974) and of exploratory nose-poking (Williams, Hamilton, & Carlton, 1975) have both been shown to emerge at about the time of presumed maturation of hippocampal function in rat pups. If the large within-session decrement in activity seen in the 3-week-old kittens in the present study can be attributed to fatigue, rather than habituation as is suggested by the observations that their walking was quite weak and unsteady and that 3-week-old kittens show no between-session habituation of open-field locomotion (Candland & Nagy, 1969), then the present results parallel the data for rats and are consonant with the notion that emerging hippocampal function at 5-6 weeks of age could account for the emergence of within-session habituation of locomotion in the kitten. Also consonant with the notion of emerging hippocampal function at 5-6 weeks in kittens are the present findings with spatial patterns of locomotion: animals 3 and 4 weeks old showed much more of the repetitive, back-and-forth locomotion symptomatic
A
1.0
l r l r l 3 4 5 6 7
3 4 5 6 7 AGE
IN WEEKS
Fig. 2. A . The average numbers of squares entered by each age group are plotted. The values for both the 3- and 4-week-old animals were significantly lower than those for 5-, 6-, and 7-week-olds 0, < .01, Duncan’s multiple range test); the value for the 7-week group is significantly lower than that for both the 5 - and 6-week-old groups 0, < .01). N s for the age groups are: 3 weeks, 13; 4 weeks, 23; 5 weeks, 1 7 ; 6 weeks, 12; 7 weeks, 13. Vertical bars in all figures show standard errors of means. B . Mean back-crossing index (number of back-crossings/number of non-back-crossings) for each age group; values for both the 3- and 4-week-old groups are significantly higher than those for 5 - , 6-, and 7-week-olds ($ < .05, Duncan’s multiple range lest). C. Mean decrement ratio (crossings in 5th minute/crossings in 1st minute) for each age group. Valucs for 4- and 5-week-old animals are significantly lower than those for 3-week-olds (p < 3 2 , 2-tailed t test) and less than those for both 6- and 7-week-olds 0, < .05, I-tailed t test)
OPEN-FIELD BEHAVIOR OF KITTENS
627
of hippocampal dysfunction (Eichelman, 1971; Kimble, 1963) than did animals 5 weeks old and older. Rosenblatt (1971) has suggested that the developmental shift from back-and-forth or circuitous paths to more direct paths of walking in kittens might reflect, in part, a shift from olfactory to visual guidance of locomotion. Although improvements in the visual acuity (Thorn, Gallender, & Erickson, 1976) and visually guided behaviors (Villablanca & Olmstead, 1979) occur through the 1st 2 months of life in kittens, the decrease in back-crossing behavior observed in the present study may not have been due entirely to the maturation of the visual system. First, visually guided behaviors such as walking after the mother cat (Rosenblatt, 1971), responding to a visual cliff (Gibson & Walk, 1960), and following a spot of light (Villablanca & Olmstead, 1979) all appear by 3 4 weeks in kittens, whereas the back-crossing behavior observed here did not decrease until 5 weeks of age. Second, although visual guidance may be necessary to avoid repetitive patterns of locomotion, the repetitive locomotor behavior of the hippocampal-damaged adult rat (Eichelman, 1971; b b l e , 1963) suggests that vision (in the absence of the hippocampus) is not sufficient to prevent repetitive patterns of locomotion in the open field. Three behavioral changes which could be manifestations of the emergence of hippocampal function at 5-6 weeks of age in kittens have been identified in this and a preceding report (Frederickson & Frederickson, 1979): the onset of spontaneous alternation, a decrease of repetitive patterns of locomotion, and an increase in within-session habituation of open-field locomotion. A 4th behavioral change suggesting emerging hippocampal function at about that same age is the marked improvement in passive avoidance behavior seen between 25 and 50 days of age in kittens (Davis & Jensen, 1976). An interesting question for future work will be whether identifiable anatomical, biochemical, or physiological changes in kitten hippocampus coincide with the sudden behavioral changes observed at 5-6 weeks of age.
Notes This work was supported in part by a grant from the H. S. Moss Foundation, and NIMH Grant l-RO3-MG29835.
References Altman, J., Brunner, R. L., and Bayer, S. A. (1973). The hippocampus and behavioral maturation. Behav. Biol., 8: 557-596. Bronstein, P. M., Neiman, H., Wolkoff, F. D., and Levine, M. J. (1974). The development of habituation in the rat. Anim. Learn. Behav., 2 : 92-96. Buchwald, N. A., Hull, C. D., Levine, M. S., and Villablanca, J. R. (1976). Developmental assessment of intact and brain-lesioned kittens. In M. A. B. Brazier and F. Coceani (eds.), Brain Dysfunction in Infantile Febrile Convulsions. New York: Raven Press. Pp. 166-177. Candland, D. K., and Campbell, B. A. (1962). Development of fear in the rat as measured by behavior in the open-field. J. Comp. Physiol. Psych., 55: 593-596. Candland, D. K., and Nagy, Z. M. (1969). The open field: Some comparative data. Ann. N.Y. Acad. Sci., 159: 831-851. Davis, J. L., and Jensen, R. A. (1976). The development of passive and active avoidance in learning in the cat. Dev. Psychobiol., 9: 175-179.
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Douglas, R. J. (1975). The development of hippocampal function: Implications for theory and therapy. In R. L. Isaacson and K. H. Pribram (eds.), The Hippocampus. Volume 2. Neurophysiology and Behavior. New York: Plenum Press. Pp. 327-361. Eichelman, B. S. (1971). Effect of subcortical lesions on shock-induced aggression in the rat. J. Comp. Physiol. Psych., 74: 331-339. Frederickson, C . J., and Frederickson, M. H. (1979). Emergence of spontaneous alternation in the kitten. Dev. Psychobiol., 12: 615-621. Gibson, E. J., and Walk, R. D. (1960). The visual cliff. Sci. Am., 202: 64-71. Hostetter, G . , and Thomas, G. J. (1967). Evaluation of enhanced thigmotaxis as a ccondition of impaired maze learning by rats with hippocampal lesions. J. Comp. Physiol. Psych., 63: 108-110. Jarrard, L. E. (1968). Behavior of hippocampal lesioned rats in home cage and novel situations. Physiol. Behav., 3: 65-70. Jarrard, L. E. (1973). The hippocampus and motivation. Psych. Bull., 79: 1-12. Kimble, D. P. (1963). The effects of bilateral hippocampal lesions in rats. J. Cornp. Physiol. Psych., 56: 273-283. Kimble, D. P. (1975). Choice behavior in rats with hippocampal lesions. In R. L. Isaacson and K. H. Pribram (eds.), The Hippocampus. Volume 2: Neurophysiology and Behavior. New York: Plenum Press. Pp. 327-361. Lanier, L. P., and Isaacson, R. L. (1975). Activity changes related to the location of lesions in the hippocampus. Behav. Biol., 13: 59-69. Leaton, R. N. (1965). Exploratory behavior in rats with hippocampal lesions. J . Cornp. Physiol. Psych., 59: 325-330. Livesey, P. J., and Egger, G . J. (1970). Age as a factor in open-field responsiveness in the white rat. J. Comp. Physiol. Psych., 73: 93-99. Means, L. W., Leander, J. D., and Isaacson, R. L. (1971). The effects of hippocarnpectomy on alternation behavior and response to novelty. Physiol. Behav., 6: 17-22. Nadel, L. (1968). Dorsal and ventral hippocampal lesions and behavior. Physiol. Behav., 3: 891-900. Roberts, W. W., Dember, W. N., and Brodwick, M. (1962). Alternation and exploration in rats with hippocampal lesions. J. Comp. Physiol. Psych., 55: 695-700. Rosenblatt, J. S . (1971). Suckling and home orientation in the kitten: A comparative developmental study. In E. Tobach, L. R. Aronson and E. Shaw (eds.), The Biop,FychoZogy of Developmenf. New York: Academic Press. Pp. 345-41 1. Strong, P. N., and Jackson, W. J. (1970). Effects of hippocampal lesions in rats on three measures of activity. J. Comp. Physiol. Psych., 70: 60-65. Thorn, F., Gallender, M., and Erickson, P. (1976). The development of the kitten's visual optics. Vis. Res., 16: 1145-1149. Villablanca, J. R., and Olrnstead, C. E. (1979). Neurological development of kittens. Dev. Psychobiol., 12: 101-127. Williams, C. D., Carr, R . M., and Peterson, H. W. (1966). Maze exploration in young rats of four ages. J. Genet. Psych., 109: 241-247. Williams, J. M., Hamilton, L. W., and Carlton, P. L. (1975). Ontogenetic dissociation of two classes of habituation. J. Comp. Physiol. Psych., 89: 733-737.
