‘‘Impoverished” Rats Weigh More than “Enriched” Rats Because They Eat More BEVERLY FIALA FREDERICK M. SNOW WILLIAM T. GREENOUCH Department o f Psychology and Neural and Behavioral BioEogy Program University of Illinois at Urbana-Champaign Net consumption measures indicated that rats reared individually in standard laboratory cages consume more food and water and gain weight more rapidly than do their littermates reared in groups in large toy-filled cages.
A consistently reported difference between rats reared in complex environments (“enriched”) and their counterparts reared in isolation (“impoverished”) is the greater body weight of the isolation-reared rats (e.g., Geller, Yuwiler, & Zolman, 1965; Greenough, Yuwiler, & Dollinger, 1973; Rosenzweig, Bennett, & Diamond, 1972a). Informal observations in this laboratory indicate that skeletal size does not differ between such groups but that the isolated animals typically have much more extensive deposits of adipose tissue. This difference is of some interest because it suggests a potential metabolic difference between these differentially reared animals which could be involved in or affect the various differences which have been reported in brain weight, chemistry, and morphology (e.g., Rosenzweig, Bennett, & Diamond, 1972a; 1972b; Greenough, 1975). Isolation rearing may produce both immediate (Patton & Gardner, 1969) and lasting (Miller, Caul, & Mirsky, 1971) metabolic changes in primates and in some rodent species and strains (Baer, 1971; Valzelli, 1973). Alternatively, the body weight differences could reflect differences in the opportunity for exercise and/or differences in food intake. Although differential exercise can account for sizeable differences in body weight if intake is held constant, food intake may increase if activity is restricted to very low levels (Mayer, 1968). The only published intake data for enriched and impoverished rats appear incidentally in a study by Tagney (1973) who reported that isolated rats consumed more pieces of food than their enriched littermates. However, the data came from only 12 pairs of rats over two 23-hr periods, involving a novel environment for the enriched animals and during which electrophysiological recordings Reprint requests and correspondence should be sent to William T. Greenough, Department of Psychology, University of Illinois, Champaign, Illinois 6 1820, U.S.A. Received for publication 30 July 1976 Revised for publication 29 November 1976 Developmental Psychobiology, 10(6): 537-541 (1977) @ 1977 by John Wiley & Sons, Inc.
537
538
FIALA, SNOW, AND GREENOUGH
were taken. Moreover, no correction appears to have been made for food droppings or spillage. The present paper reports food intake data recorded for 2 days of every week and body weights taken once weekly in male and female rats reared from weaning to puberty in typical complex and impoverished environments
Subjects Forty-six male littermate pairs and 12 female littermate pairs of Longkxans hooded rats Rattus norvegicus (a total of 116 rats; descendants of stock from Simonsen-Laboratories, Gilroy, California) were matched for body weight. coat color, and coat pattern and pair members were randomly assigned at weaning (23-26 days of age) to environmental conditions. Females were from the same litters as a subset of the males, but were not matched with males for body weight because females tended to weigh less than males at weaning.
Environments Housing conditions were essentially identical to those previously described (Greenough & Volkmar, 1973; Rosenzweig, et a/., 1972b; Tagney, 1973). In the enriched condition (EC), groups of 12 rats were housed together in a large (80 cm x 82 cni x 90 cm) wire mesh cage. A different set of wood, metal, and plastic toys drawn from a pool of over 100 objects was placed in the cage each day. In addition, the group was allowed approximately 30 min daily free exploration of a 1.2-rn square field that was provided with a similar daily set of toys. Home cage toys were changed during this exploration period. In the isolated condition (IC), rats were individually housed in standard stainless steel laboratory cages (22 x 25 x 30 em) with wire mesh fronts and bottoms. The IC rats could hear and smell, but could not see, adjacent animals although they had a view of other cages about 1.5 m away. Female IC rats and their 12 male littermates were handled only for weekly weighing. The other 34 male 1C rats were handled briefly once each day. Purina laboratory rat chow and tap water were available to both groups ad lib, except that no food or water was available to EC's during the daily 30-min exploration period. Lighting was on a 12-hr light: 12-hr dark cycle (lights on at 0700 hours) and room temperature was maintained at 24" 2°C. These housing conditions were maintained for 30 days.
*
Intake and Body Weight Measures Each r a t was removed from its environment and weighed once weekly, beginning at 28 days of age. Intake was recorded on the same days of the week for all animals, regardless of the 4-day maximum age difference. Animals were supplied with prerneasured amounts of food and water sufficient for the 48-hr weekly recording period. For IC rats, food was placed in a hopper on the cage front; for EC rats, food was placed in a pile in the center of the cage floor. For both
“IMPOVERISHED” RGTS EAT MORE
539
groups, water was available from standard bottle spouts (Girton) protruding through the wire mesh of the cage. At the end of the recording period, food dust and crumb spillage were separated from feces beneath the cage and weighed with the remaining food to determine consumption. Water remaining in bottles was measured but no attempt was made to correct for spillage.
Results Because individual food and water intake could not be measured for EC rats, individual IC values were compared with the corresponding EC mean using the sign test (Siegel, 1956). Male IC rats consumed significantly more food than their EC littermates during all but the 3rd weekly test, whereas females consumed more in all weekly tests (see Table I). Similarly, male IC rats consumed significantly greater amounts of water during a l l weekly tests. Weekly differences between EC and IC females fell short of significance for water consumption. Initial body weight did not differ due to the matching procedure. An overall (Housing Condition x Weeks) ANOVA for the males indicated significant effects of Housing Condition (F = 66.5; d f = 1/90; p < .OOl), Weeks (F = 3465.5; d f = 3/270; p < .OOl), and an interaction (F = 60.2; df = 3/270; p < .OOl). For females the same significant results occurred: Housing (F = 15.9; df = 1/22; p < .001), Weeks (F = 1072.8; df = 3/66; p < .001), and interaction ( F = 23.5; d f = 3/66; p < .001). In both genders, all differences a t individual weeks were significant < .005) by t-tests, except Week 1 for females.
Discussion These data indicate that the widely reported weight difference between EC and IC rats is at least in part a function of higher food intake by the IC’s. Why isolates eat more is not intuitively obvious. The isolates may simply eat to relieve
TABLE 1.Mean Food and Water Consumption per 48-hr Period, Week Group
1
2
3
4
26 26
33 26 43a 4Ia
42
43
Food (g)
EC- males females IC - males females Water (ml) EC- males females IC - males females a .
31a 33a 37 36 42a
38
49 50 5 6a 56
Differs from corresponding EC mean; p
29
30
44 3Ia
51a
62 67a
66 48 78a
65
12
41
< .05.
37a
540
FIALA, SNOW, AND GREENOUGH 250
i
200
150
>
D
0
m
100
50
I WEANING
28
35
42
49
Age (days) Fig. 1. Mean body weight at 1-week intervals during differential housing.
the boredom of their situation. Also, the toys in the EC cage may provide an alternative outlet for some gnawing “need” which exists in these rats. (The toys in the EC cages were heavily chewed; survival time for wood and plastic toys was extremely short.) However, no obvious differences existed in the amount of spillage collected for the 2 groups as might be expected if gnawing were the source of the consumption difference. An alternative explanation is based upon Mayer’s (1968) contention that an organism must reach some minimal level of exercise before it begins to regulate intake in accord with need. Mayer noted (p. 73) that food intake is greater in rats at extremely low levels of activity than at moderate levels. Clearly, differential opportunity for, and participation in, exercise appears to exist in the 2 environments. Typically in our laboratory, the weights of differentially housed rats have approached each other when the animals were placed in the same environment (B. Fass, K. Wrege, and W. T. Greenough, unpublished data). Overall, these results suggest little reason at this point to propose metabolic. differences similar to those in monkeys between isolation- and complexity-group-rearedrats.
Notes This research was supported by Grants No. HD06862 from NIH and GY8744 from NSF. While this research was conducted, Dr. Greenough held a fellowship aw:irded by the
“IMPOVERISHED” RATS EAT MORE
541
James McKeen Cattell Foundation. We thank William E. Kappauf for advice regarding statistical analyses.
References Baer, H. (1971). Long-term isolation stress and its effects on drug response in rodents. Lab. Anim. Sci., 21: 341-349. Geller, E., Yuwiler, A., and Zolman, J. F. (1965). Effects of environmental complexity on constituents of brain and liver. J. Neurochem., 12: 949-955. Greenough, W. T. (1975). Environmental modification of the developing brain. Amer. Scientist, 63: 3746. Greenough, W. T., and Volkmar, F. R. (1973). Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp. Neurol., 40: 491-504. Greenough, W. T., Yuwiler, A., and Dollinger, M. (1973). Effects of posttrial eserine administration on learning in “enriched” and “impoverished” reared rats. Behav. Biol., 8: 261-272. Mayer, J. (1968). Overweight: Causes, Cost, and Control. Englewood Cliffs, New Jersey: PrenticeHall. Miller, R. E., Caul, W. F., and Mirsky, I . A. (1971). Patterns of eating and drinking in socially-isolated rhesus monkeys. Physiol. Behav., 7: 127-134. Patton, R. G., and Gardner, L. I. (1969). Short stature associated with maternal deprivation syndrome: Disordered family environment as cuase of so-called idiopathic hypopituitarism. In L. I. Gardner (Ed.), Endocrine and Genetic Diseases of Childhood. Philadelphia: Saunders. Pp. 17-89. Rosenzweig, M. R., Bennett, E. L., and Diamond, M. C. (1972a). Chemical and anatomical plasticity of brain: Replications and extensions, 1970. In J. Gaito (Ed.), Macromolecules and Behavior (2nd Edition),New York: AppletonCenturyCrofts. Pp. 205-278. Rosenzweig, M. R., Bennett, E. L., and Diamond, M. C. (1972b). Brain changes in response to experience. Scient. Am., 226(2): 22-29. Siegel, S . (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Tagney, J. (1973). Sleep patterns related t o rearing in rats in enriched and impoverished environments. Brain Res., 53: 353-361. Valzelli, L. (1973). The “isolation syndrome” in mice. Psychopharmacotogy, 31: 305-320.
A consistently reported difference between rats reared in complex environments (“enriched”) and their counterparts reared in isolation (“impoverished”) is the greater body weight of the isolation-reared rats (e.g., Geller, Yuwiler, & Zolman, 1965; Greenough, Yuwiler, & Dollinger, 1973; Rosenzweig, Bennett, & Diamond, 1972a). Informal observations in this laboratory indicate that skeletal size does not differ between such groups but that the isolated animals typically have much more extensive deposits of adipose tissue. This difference is of some interest because it suggests a potential metabolic difference between these differentially reared animals which could be involved in or affect the various differences which have been reported in brain weight, chemistry, and morphology (e.g., Rosenzweig, Bennett, & Diamond, 1972a; 1972b; Greenough, 1975). Isolation rearing may produce both immediate (Patton & Gardner, 1969) and lasting (Miller, Caul, & Mirsky, 1971) metabolic changes in primates and in some rodent species and strains (Baer, 1971; Valzelli, 1973). Alternatively, the body weight differences could reflect differences in the opportunity for exercise and/or differences in food intake. Although differential exercise can account for sizeable differences in body weight if intake is held constant, food intake may increase if activity is restricted to very low levels (Mayer, 1968). The only published intake data for enriched and impoverished rats appear incidentally in a study by Tagney (1973) who reported that isolated rats consumed more pieces of food than their enriched littermates. However, the data came from only 12 pairs of rats over two 23-hr periods, involving a novel environment for the enriched animals and during which electrophysiological recordings Reprint requests and correspondence should be sent to William T. Greenough, Department of Psychology, University of Illinois, Champaign, Illinois 6 1820, U.S.A. Received for publication 30 July 1976 Revised for publication 29 November 1976 Developmental Psychobiology, 10(6): 537-541 (1977) @ 1977 by John Wiley & Sons, Inc.
537
538
FIALA, SNOW, AND GREENOUGH
were taken. Moreover, no correction appears to have been made for food droppings or spillage. The present paper reports food intake data recorded for 2 days of every week and body weights taken once weekly in male and female rats reared from weaning to puberty in typical complex and impoverished environments
Subjects Forty-six male littermate pairs and 12 female littermate pairs of Longkxans hooded rats Rattus norvegicus (a total of 116 rats; descendants of stock from Simonsen-Laboratories, Gilroy, California) were matched for body weight. coat color, and coat pattern and pair members were randomly assigned at weaning (23-26 days of age) to environmental conditions. Females were from the same litters as a subset of the males, but were not matched with males for body weight because females tended to weigh less than males at weaning.
Environments Housing conditions were essentially identical to those previously described (Greenough & Volkmar, 1973; Rosenzweig, et a/., 1972b; Tagney, 1973). In the enriched condition (EC), groups of 12 rats were housed together in a large (80 cm x 82 cni x 90 cm) wire mesh cage. A different set of wood, metal, and plastic toys drawn from a pool of over 100 objects was placed in the cage each day. In addition, the group was allowed approximately 30 min daily free exploration of a 1.2-rn square field that was provided with a similar daily set of toys. Home cage toys were changed during this exploration period. In the isolated condition (IC), rats were individually housed in standard stainless steel laboratory cages (22 x 25 x 30 em) with wire mesh fronts and bottoms. The IC rats could hear and smell, but could not see, adjacent animals although they had a view of other cages about 1.5 m away. Female IC rats and their 12 male littermates were handled only for weekly weighing. The other 34 male 1C rats were handled briefly once each day. Purina laboratory rat chow and tap water were available to both groups ad lib, except that no food or water was available to EC's during the daily 30-min exploration period. Lighting was on a 12-hr light: 12-hr dark cycle (lights on at 0700 hours) and room temperature was maintained at 24" 2°C. These housing conditions were maintained for 30 days.
*
Intake and Body Weight Measures Each r a t was removed from its environment and weighed once weekly, beginning at 28 days of age. Intake was recorded on the same days of the week for all animals, regardless of the 4-day maximum age difference. Animals were supplied with prerneasured amounts of food and water sufficient for the 48-hr weekly recording period. For IC rats, food was placed in a hopper on the cage front; for EC rats, food was placed in a pile in the center of the cage floor. For both
“IMPOVERISHED” RGTS EAT MORE
539
groups, water was available from standard bottle spouts (Girton) protruding through the wire mesh of the cage. At the end of the recording period, food dust and crumb spillage were separated from feces beneath the cage and weighed with the remaining food to determine consumption. Water remaining in bottles was measured but no attempt was made to correct for spillage.
Results Because individual food and water intake could not be measured for EC rats, individual IC values were compared with the corresponding EC mean using the sign test (Siegel, 1956). Male IC rats consumed significantly more food than their EC littermates during all but the 3rd weekly test, whereas females consumed more in all weekly tests (see Table I). Similarly, male IC rats consumed significantly greater amounts of water during a l l weekly tests. Weekly differences between EC and IC females fell short of significance for water consumption. Initial body weight did not differ due to the matching procedure. An overall (Housing Condition x Weeks) ANOVA for the males indicated significant effects of Housing Condition (F = 66.5; d f = 1/90; p < .OOl), Weeks (F = 3465.5; d f = 3/270; p < .OOl), and an interaction (F = 60.2; df = 3/270; p < .OOl). For females the same significant results occurred: Housing (F = 15.9; df = 1/22; p < .001), Weeks (F = 1072.8; df = 3/66; p < .001), and interaction ( F = 23.5; d f = 3/66; p < .001). In both genders, all differences a t individual weeks were significant < .005) by t-tests, except Week 1 for females.
Discussion These data indicate that the widely reported weight difference between EC and IC rats is at least in part a function of higher food intake by the IC’s. Why isolates eat more is not intuitively obvious. The isolates may simply eat to relieve
TABLE 1.Mean Food and Water Consumption per 48-hr Period, Week Group
1
2
3
4
26 26
33 26 43a 4Ia
42
43
Food (g)
EC- males females IC - males females Water (ml) EC- males females IC - males females a .
31a 33a 37 36 42a
38
49 50 5 6a 56
Differs from corresponding EC mean; p
29
30
44 3Ia
51a
62 67a
66 48 78a
65
12
41
< .05.
37a
540
FIALA, SNOW, AND GREENOUGH 250
i
200
150
>
D
0
m
100
50
I WEANING
28
35
42
49
Age (days) Fig. 1. Mean body weight at 1-week intervals during differential housing.
the boredom of their situation. Also, the toys in the EC cage may provide an alternative outlet for some gnawing “need” which exists in these rats. (The toys in the EC cages were heavily chewed; survival time for wood and plastic toys was extremely short.) However, no obvious differences existed in the amount of spillage collected for the 2 groups as might be expected if gnawing were the source of the consumption difference. An alternative explanation is based upon Mayer’s (1968) contention that an organism must reach some minimal level of exercise before it begins to regulate intake in accord with need. Mayer noted (p. 73) that food intake is greater in rats at extremely low levels of activity than at moderate levels. Clearly, differential opportunity for, and participation in, exercise appears to exist in the 2 environments. Typically in our laboratory, the weights of differentially housed rats have approached each other when the animals were placed in the same environment (B. Fass, K. Wrege, and W. T. Greenough, unpublished data). Overall, these results suggest little reason at this point to propose metabolic. differences similar to those in monkeys between isolation- and complexity-group-rearedrats.
Notes This research was supported by Grants No. HD06862 from NIH and GY8744 from NSF. While this research was conducted, Dr. Greenough held a fellowship aw:irded by the
“IMPOVERISHED” RATS EAT MORE
541
James McKeen Cattell Foundation. We thank William E. Kappauf for advice regarding statistical analyses.
References Baer, H. (1971). Long-term isolation stress and its effects on drug response in rodents. Lab. Anim. Sci., 21: 341-349. Geller, E., Yuwiler, A., and Zolman, J. F. (1965). Effects of environmental complexity on constituents of brain and liver. J. Neurochem., 12: 949-955. Greenough, W. T. (1975). Environmental modification of the developing brain. Amer. Scientist, 63: 3746. Greenough, W. T., and Volkmar, F. R. (1973). Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp. Neurol., 40: 491-504. Greenough, W. T., Yuwiler, A., and Dollinger, M. (1973). Effects of posttrial eserine administration on learning in “enriched” and “impoverished” reared rats. Behav. Biol., 8: 261-272. Mayer, J. (1968). Overweight: Causes, Cost, and Control. Englewood Cliffs, New Jersey: PrenticeHall. Miller, R. E., Caul, W. F., and Mirsky, I . A. (1971). Patterns of eating and drinking in socially-isolated rhesus monkeys. Physiol. Behav., 7: 127-134. Patton, R. G., and Gardner, L. I. (1969). Short stature associated with maternal deprivation syndrome: Disordered family environment as cuase of so-called idiopathic hypopituitarism. In L. I. Gardner (Ed.), Endocrine and Genetic Diseases of Childhood. Philadelphia: Saunders. Pp. 17-89. Rosenzweig, M. R., Bennett, E. L., and Diamond, M. C. (1972a). Chemical and anatomical plasticity of brain: Replications and extensions, 1970. In J. Gaito (Ed.), Macromolecules and Behavior (2nd Edition),New York: AppletonCenturyCrofts. Pp. 205-278. Rosenzweig, M. R., Bennett, E. L., and Diamond, M. C. (1972b). Brain changes in response to experience. Scient. Am., 226(2): 22-29. Siegel, S . (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Tagney, J. (1973). Sleep patterns related t o rearing in rats in enriched and impoverished environments. Brain Res., 53: 353-361. Valzelli, L. (1973). The “isolation syndrome” in mice. Psychopharmacotogy, 31: 305-320.
