Behavioural Brahl Research, 52 (1992) 45-48 9 1992 Elsevier Science Publishers B.V. All rights reserved. 0166-4328/92/$05.00
45
BBR 01375
Lateralization and reaching skill related: results and implications from a large sample of Long-Evans rats Ian Q. Whishaw Department of Psychology, Universityof Lethbridge, Lethbridge, Alta. (Canada) (Received 8 June 1992) (Revised version received 30 July 1992) (Accepted 11 August 1992)
Key words: Limb asymmetry; Limb preference; Limb use; Skilled rat reaching
Limb preference and reaching success were examined in 580 Long-Evans rats. Most rats displayed a strong asymmetry. Although slightly more rats used the left limb than used the right limb, the difference was not significant. Thus, Long-Evans rats do not show dominance with respect to limb use. There was a significant correlation between the degree of lateralization and success of limb use. This relation suggests either that endogenous factors contributing to limb lateralization also contribute to motor skill or else the use of a lateralized reaching strategy facilitates the development of skill in reaching. The results are discussed in terms of their methodological implications for studies of selective breeding and strain differences and also in terms of their significance for understanding the evolutionary basis of lateralization and dominance.
INTRODUCTION
Most humans display limb dominance in that they use their right hand preferentially for many skilled movements 1. A search for the explanation of dominance has led to the examination not only of cultural and genetic factors but has also led to investigations of handedness in other animals 1'8. There are now a number of reports that preferential use of the left limb can be found in a number of primate and prosimian species 12, although the significance of these findings for human dominance is still controversial s. Rodents are able to use a limb to reach for food and they share many similarities with primates in the anatomy of their motor systems and the movements that they use when reaching 19. Furthermore, they Will also preferentially use one limb when they are trained to reach for food l~ To date, there is no evidence that dominance is displayed or can be produced in rodents. Through genetic selection, mice strains that are strongly lateralized or ambidextrous have been developed but the same studies have been unable to influence the direction of lateralization 3"6. Thus, these studies suggest Correspondence: I.Q. Whishaw, Department of Psychology, University of Lethbridge, Lethbridge, Alta., Canada, T I K 3M4. Fax:(1)(403)329-2255: E-mail Whishaw @ HG. ULETH. CA.
that strength, but not direction, oflateralization may be genetically determined. Only a few studies have examined limb preferences in rats. Peterson 1~has reported that almost equal numbers of animals are right and left limbed with fewer animals displaying ambidexterity. Tsai and Maurer tl3 have reported a tendency toward a right preference. Whishaw et al. ~7 have reported an almost equal division between right limbed, left limbed, and ambidextrous animals. Thus, the results from rats seem consistent with the results from mice. There is no striking bias in direction but there are variations in the degree of lateralization in different strains or populations. The present study reports on the results obtained from a large number of Long-Evans rats from which data was collected over a 6-year period (1986-1992) 16'2~
MATERIALS A N D M E T H O D S
SttbjecIs Four hundred and thirty-four female and 136 male adult Long-Evans hooded rats, aged between 90 and 120 days when they were tested, were used. They were housed in hanging wire mesh cages in an animal colony lighted on a 12:1:2 h light-dark cycle. Testing was done during the light portion of the cycle.
46
Apparatus The rats were pretrained in one of 9boxes (10 • 18 • 10 cm high). The front and floor were constructed of 2 mm bars that were separated from each other by 9 mm, edge to edge. The tops, backs and sides were Plexiglas. A 4-cm-wide and 5-mm-deep tray, containing granules of food (20-40 mg chick feed), was mounted in front of each box and extended for the length of the box. To obtain food, the rat had only to reach through the bars, grasp and retract it (for a photo of a similar apparatus see ref. 17). The floors of the boxes were made of metal grids, so that ifa rat dropped the food it fell through the grids and was lost.
Trainhlg The rats were food-deprived and then given a measured amount of food each day until they were reduced to about 9 0 ~ of their initial body weight. After training began, feeding was restricted so that the food obtained during training/testing plus supplemental feeding maintained them at this weight. For training, the rats were placed individually in one of the compartments of the reaching boxes and left there for 1 h. The food tray was periodically replenished. Training lasted for an hour e,,.ch day for 10 days with tests distributed over a 14-day period. If a rat failed to start reaching, it was given additional training. This included being left overnight in the reaching boxes and receiving operant conditioning of having cookie mash spread onto the paw when it was advanced toward the food.
Testhzg Each rat was given a 10-min test at the end of the training period. Performance was scored by depressing buttons, connected to relays and then to a microcomputer, indicating hits and misses for each limb. If the rats made a reaching movement in which a paw was inserted through the bars of the cage, the movement was scored as a 'reach'. If the rat obtained a piece of food and then consumed it, the reach was scored as a 'hit'.
calculated as follows: hit 9/0 = successful reaches/total reaches x 100. The results were analyzed using analysis of variance (ANOVA), Pearson's correlation coefficient, and Za-tests 2~.
RESULTS
Reaching success All of the rats learned to advance their limb through the bars of the reaching cage. The rats made an average of 75.69_+ 2.02 (S.E.M.) reaches with an average hit percent of 59.68 + 0.66. Most rats received reaching success scores that ranged between 40 and 7 0 ~ . A few rats received scores of over 9 0 ~ and a few rats received very low scores ( 0 . 0 5 . Nor was there a significant difference in the total number of rats that preferred their left ( > 50 ~o left preference) vs. right ( > 50 ~o right preference) limb, Zzl = 2.23, P > 0.05. 40"
m
30"
Q
Data analysis The measure of degree of asymmetry in the rats was percent of laterafity, calculated for each rat according to the following formula: side bias = ((right side-left side)/(right side + left side))x 100. Right and left side refer to the number of right and left limb reaches. These scores were then expressed as: (1) function of right side bias, e.g., 100~ = exclusive right limb use, 0~o = exclusive left limb use, or (2)degree of asymmetry, e.g. I 0 0 ~ = exclusive use of one limb and 0% = equal use of left and right limb. Reaching success scores were
-~
20"
O O
~'~
10"
0 - -U1.R.~,~.~.~.~.Vl.n.~.~Fl.n.r~-~m-VI,N 0
S0
100
Right Paw Use (%) Fig. 1. Distribution o f limb preference in 580 L o n g - E v a n s male a n d female rats expressed as a pcrccnt o f right p a w use, e.g., 0 % = exclusive left limb u s e a n d 1 0 0 ~ = exclusive right limb use. Each bar represents a 5 ~ bin.
47 Degree of L a t e r a l i z a t i o n 80"
60"
Q 40"
r,j 20"
R e a c h i n g Success 60"
7-
32 r
40'
t~ 20'
I00 45 40 35 30 25 20 15 10 S Lateralization
Score (%)
Fig. 2. Laterality scores (lop) a n d reaching s u c c e s s (bottom) in 580 L o n g - E v a n s rats. (Laterality score o f 1 0 0 ~ = exclusive u s e o f either the left or right limb, latcrality score o f 50 ~o = equal u s e o f both the left a n d right limb.)
A comparison of reaching success in right vs. left limbed rats indicated no significant difference in hit percent scores, FI,578 = 0.3 I, P > 0.05. There were also no differences in reaching success in groups of rats that displayed comparable degrees of left vs. right limb preference, F9.578 = 1.10, P = 0.36. When a correlation between lateralization scores and reaching success was performed, a significant correlation was obtained, r = 578 = 0.35, P < 0.001. That is, the most lateralized rats had the best success scores. The distribution of rats as a function of lateralization is shown in Fig. 2 (top) and average reaching success is shown in Fig. 2 (bottom).
DISCUSSION
Measurement of limb use and success in limb use in a large, sample of Long-Evans rats showed that most of the rats displayed a strong limb preference. That is many rats almost exclusively preferred to use the left limb, many rats almost exclusively preferred to use the right limb, and smaller numbers displayed various degrees of ambidexterity. Most rats started reaching within a day or two of being placed in the boxes and i
by the end of the training period would have made thousands of reaches. Thus, the results represent asymptotic performance using this training procedure. These results are generally consistent with a number of previous studies in showing that rats do not display dominance with respect to limb use; that is, as a population, and unlike humans, they do not show a preference for one limb. In genetic studies using mice, it has been shown that bias in limb use can be selected for. Stains oflateralized and ambidextrous mice have been developed 3'6. It seems likely that variation in degree of lateralization may be found also in strains or populations of rats. For example Whishaw et al.~7 report almost equal numbers of left, right and ambidextrous rats in a population of Sprague-Dawley (OLAC, Bicester, UK) rats. Miklyaeva et al. 9 report that in an unspecified population of albino rats an almost equal number were left and right limbed rats and about 20 ~o of the animals were ambidextrous. Tsai and Maurer ~3 report a tendency to right limb use in a sample of albino rats. These distributions can be contrasted with the somewhat larger number of rats showing strong lateralization in the present study. Although the methods, data analyses, and numbers of subjects in these studies are different, the results suggest that there is variation in limb preferences in different rat populations. An important finding in the present study is that there is a relationship between degree of lateralization and success in limb use. Rats that make greater use of one limb require fewer reaches to obtain food than more ambidextrous rats. This result is intriguing because it suggests that there is some adaptive advantage to lateralization. This advantage could be conferred by central mechanisms, limb structure, or experiential factors. The relationship between success and lateralization could suggest that neural mechanisms that mediate lateralization also mediate effective limb control. It is interesting that genetically selected, strongly lateralized, mice have heavier brains than normal mice, while weakly lateralized mice have lighter brains than normal mice ~4. It has also been found that mice selectively bred for whisker pad asymmetry show an opposite shift in the distribution of limb preference2. Finally there are reports that rats with small unilateral motor cortex lesions made neonatally display increased ambidexterity 5'11 while larger lesions produce a shift in limb preference ~6. All of these observations support the idea that limb preference can be an expression of a central nervous system asymmetry. On the other hand, it is possible that the fortuitous adoption of a strategy of limiting reaching to one limb
48 facilitates skill learning, which in turn leads to better performance 4. Our own observations show that limb preferences are displayed as soon as rats begin to reach and they remained very stable over months of testing. Nevertheless, if use of a limb is restricted, rats will readily shift limb use and make very good use of the non-preferred limb t7. Limb structure may also influence preference and success, but to date there have been no studies on the relationship between limb structure and limb use. Whatever the cause, the finding of a relation between laterality and success reported here has two implications. First, measures oflaterality could in part be measures of skill. Consequently, studies on laterality should include a measure of skill to ensure that selection of strength of preference is in fact not selection for motor skill. Second, the relationship suggests that there is an advantage to lateralization. The acquisition of a skilled movement may be more effectively attained by limiting practice and use to one limb. Skill in turn could be subject to selective evolutionary pressure, and could thus provide a first step toward the evolution of dominance.
ACKNOWLEDGEMENTS
This research was supported by grants from the Natural Sciences and Engineering Research Council of Canada. The author thanks Jo-Anne Tomie for testing many of the animals and for organizing the data and thanks Bryan Koib for the use of his data.
REFERENCES 1 Annett, M., Left, Right, Hand and Brahl, Erlbaum, New York, Erlbaum, 1985. 2 Barnroud, P. and van der Loos, H., Direction of handedness linked to hereditary asymmetry of a sensory system, Proc. Natl. Acad. Sci. USA, in press. 3 Betancur, C., Nevcu, P.J. and LeMoal, M., Strain and sex differences in the degree of paw preference in mice, Behav. Brahl Res., 45 (1991) 97-101.
4 Bureg, J. and Br~cha, V., The control of movements by the motor cortex. In B. Kolb and R.C. Tees (Eds.) Tile Cerebral Cortex of the Rat, MIT Press, Cambridge, MA, 1990, pp. 213-238. 5 Castro, A.J., Limb preference after lesions of the cerebral hemisphere in adult and neonatal rats, PhysioL Behvav., 18 (1977) 605-608. 6 Collins, R.L., On the inheritance of direction and degree of asymmetry. In S.D. Glick (Ed.), Cerebral Lateralization hz Non-Human Species, Academic Press, New York, 1985, pp. 41-71. 7 Br~cha, V., Zhuravin, I.A. and Buret, J., The reaching reaction in the rat: a part of the digging pattern? Behav. Brabl Res., 36 (1990) 53-64. 8 MacNeilage, P.F., Studdcrt-Kennedy, M.G. and Lindblom, B., Primate handedness reconsidered, Behav. Brain Sci., 10 (1987) 247-303. 9 Miklyaeva, E.I., Ioffe, M.E. and Kulikov, M.A., Innate versus learned factors determining limb preference in the rat, Behav. Brabl Res., 46 (1991) 103-117. 10 Peterson, G.M., Mechanisms of handedness in the rat, Comp. Psych. Monograph., 9 (1934) 1-67. 11 Plumct, J., Cadusseau, J. and Roger, M., Skilled forelimb use in the rat: amelioration of functional deficits resulting from neonatal damage to the frontal cortex by neonatal transplantation of fetal cortical tissue, Rest. NeuroL Neurosci., 3 (1991) 135-147. 12 Sanford, C., Guin, K. and Ward, J.P., Posture and laterality in the bushbaby ( Galago senegalensis), Brain Behav. EvoL, 25 (1984) 217-224. 13 Tsai, L.S. and Maurcr, S., 'Right-handedness' in white rats, Science, 72 (1930) 436-438. 14 Ward, R. and Collins, R.L., Brain size and shape in strongly and weakly lateralized mice, Brain Res., 328 (1985) 243-249. 15 Warren, J.lk|., Handedness and laterality in humans and other animals, PhysioL PsychoL, 95 (1980) 351-359. 16 Whishaw, I.Q. and Kolb, B., Sparing of skilled forelimb reaching and corticospinal projections after neonatal motor cortex removal or hemidecortication in the rat: support for the Kennard doctrine, Brah~ Res., 451 (1988) 97-114. 17 Whishaw, I.Q., O'Connor, R.B. and Dunnet, S.B., The contributions of motor cortex, nigrostriatal dopamine and caudateputamen to skilled forelimb use in the rat, Brain, 109 (1986) 805-843. 18 Whishaw, I.Q. and Pellis, S.M., The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component, Behav. Brahl. Res., 41 (1990) 77-91. 19 Whishaw, I.Q., Pellis, S.M. and Gorny, B.P., Skilled reaching in rats and humans: evidence for parallel development or homology, Behav. Brabz Res., 47 (1992) 59-70. 20 Whishaw, I.Q. and Tomie, J., Olfaction directs skilled forelimb reaching in the rat, Behav. Brain Res., 32 (1989) 11-21. 21 Winer, B.J., Statistical Principlesbl Expedmental Design, lqcGrawHill, New York, 1962.
45
BBR 01375
Lateralization and reaching skill related: results and implications from a large sample of Long-Evans rats Ian Q. Whishaw Department of Psychology, Universityof Lethbridge, Lethbridge, Alta. (Canada) (Received 8 June 1992) (Revised version received 30 July 1992) (Accepted 11 August 1992)
Key words: Limb asymmetry; Limb preference; Limb use; Skilled rat reaching
Limb preference and reaching success were examined in 580 Long-Evans rats. Most rats displayed a strong asymmetry. Although slightly more rats used the left limb than used the right limb, the difference was not significant. Thus, Long-Evans rats do not show dominance with respect to limb use. There was a significant correlation between the degree of lateralization and success of limb use. This relation suggests either that endogenous factors contributing to limb lateralization also contribute to motor skill or else the use of a lateralized reaching strategy facilitates the development of skill in reaching. The results are discussed in terms of their methodological implications for studies of selective breeding and strain differences and also in terms of their significance for understanding the evolutionary basis of lateralization and dominance.
INTRODUCTION
Most humans display limb dominance in that they use their right hand preferentially for many skilled movements 1. A search for the explanation of dominance has led to the examination not only of cultural and genetic factors but has also led to investigations of handedness in other animals 1'8. There are now a number of reports that preferential use of the left limb can be found in a number of primate and prosimian species 12, although the significance of these findings for human dominance is still controversial s. Rodents are able to use a limb to reach for food and they share many similarities with primates in the anatomy of their motor systems and the movements that they use when reaching 19. Furthermore, they Will also preferentially use one limb when they are trained to reach for food l~ To date, there is no evidence that dominance is displayed or can be produced in rodents. Through genetic selection, mice strains that are strongly lateralized or ambidextrous have been developed but the same studies have been unable to influence the direction of lateralization 3"6. Thus, these studies suggest Correspondence: I.Q. Whishaw, Department of Psychology, University of Lethbridge, Lethbridge, Alta., Canada, T I K 3M4. Fax:(1)(403)329-2255: E-mail Whishaw @ HG. ULETH. CA.
that strength, but not direction, oflateralization may be genetically determined. Only a few studies have examined limb preferences in rats. Peterson 1~has reported that almost equal numbers of animals are right and left limbed with fewer animals displaying ambidexterity. Tsai and Maurer tl3 have reported a tendency toward a right preference. Whishaw et al. ~7 have reported an almost equal division between right limbed, left limbed, and ambidextrous animals. Thus, the results from rats seem consistent with the results from mice. There is no striking bias in direction but there are variations in the degree of lateralization in different strains or populations. The present study reports on the results obtained from a large number of Long-Evans rats from which data was collected over a 6-year period (1986-1992) 16'2~
MATERIALS A N D M E T H O D S
SttbjecIs Four hundred and thirty-four female and 136 male adult Long-Evans hooded rats, aged between 90 and 120 days when they were tested, were used. They were housed in hanging wire mesh cages in an animal colony lighted on a 12:1:2 h light-dark cycle. Testing was done during the light portion of the cycle.
46
Apparatus The rats were pretrained in one of 9boxes (10 • 18 • 10 cm high). The front and floor were constructed of 2 mm bars that were separated from each other by 9 mm, edge to edge. The tops, backs and sides were Plexiglas. A 4-cm-wide and 5-mm-deep tray, containing granules of food (20-40 mg chick feed), was mounted in front of each box and extended for the length of the box. To obtain food, the rat had only to reach through the bars, grasp and retract it (for a photo of a similar apparatus see ref. 17). The floors of the boxes were made of metal grids, so that ifa rat dropped the food it fell through the grids and was lost.
Trainhlg The rats were food-deprived and then given a measured amount of food each day until they were reduced to about 9 0 ~ of their initial body weight. After training began, feeding was restricted so that the food obtained during training/testing plus supplemental feeding maintained them at this weight. For training, the rats were placed individually in one of the compartments of the reaching boxes and left there for 1 h. The food tray was periodically replenished. Training lasted for an hour e,,.ch day for 10 days with tests distributed over a 14-day period. If a rat failed to start reaching, it was given additional training. This included being left overnight in the reaching boxes and receiving operant conditioning of having cookie mash spread onto the paw when it was advanced toward the food.
Testhzg Each rat was given a 10-min test at the end of the training period. Performance was scored by depressing buttons, connected to relays and then to a microcomputer, indicating hits and misses for each limb. If the rats made a reaching movement in which a paw was inserted through the bars of the cage, the movement was scored as a 'reach'. If the rat obtained a piece of food and then consumed it, the reach was scored as a 'hit'.
calculated as follows: hit 9/0 = successful reaches/total reaches x 100. The results were analyzed using analysis of variance (ANOVA), Pearson's correlation coefficient, and Za-tests 2~.
RESULTS
Reaching success All of the rats learned to advance their limb through the bars of the reaching cage. The rats made an average of 75.69_+ 2.02 (S.E.M.) reaches with an average hit percent of 59.68 + 0.66. Most rats received reaching success scores that ranged between 40 and 7 0 ~ . A few rats received scores of over 9 0 ~ and a few rats received very low scores ( 0 . 0 5 . Nor was there a significant difference in the total number of rats that preferred their left ( > 50 ~o left preference) vs. right ( > 50 ~o right preference) limb, Zzl = 2.23, P > 0.05. 40"
m
30"
Q
Data analysis The measure of degree of asymmetry in the rats was percent of laterafity, calculated for each rat according to the following formula: side bias = ((right side-left side)/(right side + left side))x 100. Right and left side refer to the number of right and left limb reaches. These scores were then expressed as: (1) function of right side bias, e.g., 100~ = exclusive right limb use, 0~o = exclusive left limb use, or (2)degree of asymmetry, e.g. I 0 0 ~ = exclusive use of one limb and 0% = equal use of left and right limb. Reaching success scores were
-~
20"
O O
~'~
10"
0 - -U1.R.~,~.~.~.~.Vl.n.~.~Fl.n.r~-~m-VI,N 0
S0
100
Right Paw Use (%) Fig. 1. Distribution o f limb preference in 580 L o n g - E v a n s male a n d female rats expressed as a pcrccnt o f right p a w use, e.g., 0 % = exclusive left limb u s e a n d 1 0 0 ~ = exclusive right limb use. Each bar represents a 5 ~ bin.
47 Degree of L a t e r a l i z a t i o n 80"
60"
Q 40"
r,j 20"
R e a c h i n g Success 60"
7-
32 r
40'
t~ 20'
I00 45 40 35 30 25 20 15 10 S Lateralization
Score (%)
Fig. 2. Laterality scores (lop) a n d reaching s u c c e s s (bottom) in 580 L o n g - E v a n s rats. (Laterality score o f 1 0 0 ~ = exclusive u s e o f either the left or right limb, latcrality score o f 50 ~o = equal u s e o f both the left a n d right limb.)
A comparison of reaching success in right vs. left limbed rats indicated no significant difference in hit percent scores, FI,578 = 0.3 I, P > 0.05. There were also no differences in reaching success in groups of rats that displayed comparable degrees of left vs. right limb preference, F9.578 = 1.10, P = 0.36. When a correlation between lateralization scores and reaching success was performed, a significant correlation was obtained, r = 578 = 0.35, P < 0.001. That is, the most lateralized rats had the best success scores. The distribution of rats as a function of lateralization is shown in Fig. 2 (top) and average reaching success is shown in Fig. 2 (bottom).
DISCUSSION
Measurement of limb use and success in limb use in a large, sample of Long-Evans rats showed that most of the rats displayed a strong limb preference. That is many rats almost exclusively preferred to use the left limb, many rats almost exclusively preferred to use the right limb, and smaller numbers displayed various degrees of ambidexterity. Most rats started reaching within a day or two of being placed in the boxes and i
by the end of the training period would have made thousands of reaches. Thus, the results represent asymptotic performance using this training procedure. These results are generally consistent with a number of previous studies in showing that rats do not display dominance with respect to limb use; that is, as a population, and unlike humans, they do not show a preference for one limb. In genetic studies using mice, it has been shown that bias in limb use can be selected for. Stains oflateralized and ambidextrous mice have been developed 3'6. It seems likely that variation in degree of lateralization may be found also in strains or populations of rats. For example Whishaw et al.~7 report almost equal numbers of left, right and ambidextrous rats in a population of Sprague-Dawley (OLAC, Bicester, UK) rats. Miklyaeva et al. 9 report that in an unspecified population of albino rats an almost equal number were left and right limbed rats and about 20 ~o of the animals were ambidextrous. Tsai and Maurer ~3 report a tendency to right limb use in a sample of albino rats. These distributions can be contrasted with the somewhat larger number of rats showing strong lateralization in the present study. Although the methods, data analyses, and numbers of subjects in these studies are different, the results suggest that there is variation in limb preferences in different rat populations. An important finding in the present study is that there is a relationship between degree of lateralization and success in limb use. Rats that make greater use of one limb require fewer reaches to obtain food than more ambidextrous rats. This result is intriguing because it suggests that there is some adaptive advantage to lateralization. This advantage could be conferred by central mechanisms, limb structure, or experiential factors. The relationship between success and lateralization could suggest that neural mechanisms that mediate lateralization also mediate effective limb control. It is interesting that genetically selected, strongly lateralized, mice have heavier brains than normal mice, while weakly lateralized mice have lighter brains than normal mice ~4. It has also been found that mice selectively bred for whisker pad asymmetry show an opposite shift in the distribution of limb preference2. Finally there are reports that rats with small unilateral motor cortex lesions made neonatally display increased ambidexterity 5'11 while larger lesions produce a shift in limb preference ~6. All of these observations support the idea that limb preference can be an expression of a central nervous system asymmetry. On the other hand, it is possible that the fortuitous adoption of a strategy of limiting reaching to one limb
48 facilitates skill learning, which in turn leads to better performance 4. Our own observations show that limb preferences are displayed as soon as rats begin to reach and they remained very stable over months of testing. Nevertheless, if use of a limb is restricted, rats will readily shift limb use and make very good use of the non-preferred limb t7. Limb structure may also influence preference and success, but to date there have been no studies on the relationship between limb structure and limb use. Whatever the cause, the finding of a relation between laterality and success reported here has two implications. First, measures oflaterality could in part be measures of skill. Consequently, studies on laterality should include a measure of skill to ensure that selection of strength of preference is in fact not selection for motor skill. Second, the relationship suggests that there is an advantage to lateralization. The acquisition of a skilled movement may be more effectively attained by limiting practice and use to one limb. Skill in turn could be subject to selective evolutionary pressure, and could thus provide a first step toward the evolution of dominance.
ACKNOWLEDGEMENTS
This research was supported by grants from the Natural Sciences and Engineering Research Council of Canada. The author thanks Jo-Anne Tomie for testing many of the animals and for organizing the data and thanks Bryan Koib for the use of his data.
REFERENCES 1 Annett, M., Left, Right, Hand and Brahl, Erlbaum, New York, Erlbaum, 1985. 2 Barnroud, P. and van der Loos, H., Direction of handedness linked to hereditary asymmetry of a sensory system, Proc. Natl. Acad. Sci. USA, in press. 3 Betancur, C., Nevcu, P.J. and LeMoal, M., Strain and sex differences in the degree of paw preference in mice, Behav. Brahl Res., 45 (1991) 97-101.
4 Bureg, J. and Br~cha, V., The control of movements by the motor cortex. In B. Kolb and R.C. Tees (Eds.) Tile Cerebral Cortex of the Rat, MIT Press, Cambridge, MA, 1990, pp. 213-238. 5 Castro, A.J., Limb preference after lesions of the cerebral hemisphere in adult and neonatal rats, PhysioL Behvav., 18 (1977) 605-608. 6 Collins, R.L., On the inheritance of direction and degree of asymmetry. In S.D. Glick (Ed.), Cerebral Lateralization hz Non-Human Species, Academic Press, New York, 1985, pp. 41-71. 7 Br~cha, V., Zhuravin, I.A. and Buret, J., The reaching reaction in the rat: a part of the digging pattern? Behav. Brabl Res., 36 (1990) 53-64. 8 MacNeilage, P.F., Studdcrt-Kennedy, M.G. and Lindblom, B., Primate handedness reconsidered, Behav. Brain Sci., 10 (1987) 247-303. 9 Miklyaeva, E.I., Ioffe, M.E. and Kulikov, M.A., Innate versus learned factors determining limb preference in the rat, Behav. Brabl Res., 46 (1991) 103-117. 10 Peterson, G.M., Mechanisms of handedness in the rat, Comp. Psych. Monograph., 9 (1934) 1-67. 11 Plumct, J., Cadusseau, J. and Roger, M., Skilled forelimb use in the rat: amelioration of functional deficits resulting from neonatal damage to the frontal cortex by neonatal transplantation of fetal cortical tissue, Rest. NeuroL Neurosci., 3 (1991) 135-147. 12 Sanford, C., Guin, K. and Ward, J.P., Posture and laterality in the bushbaby ( Galago senegalensis), Brain Behav. EvoL, 25 (1984) 217-224. 13 Tsai, L.S. and Maurcr, S., 'Right-handedness' in white rats, Science, 72 (1930) 436-438. 14 Ward, R. and Collins, R.L., Brain size and shape in strongly and weakly lateralized mice, Brain Res., 328 (1985) 243-249. 15 Warren, J.lk|., Handedness and laterality in humans and other animals, PhysioL PsychoL, 95 (1980) 351-359. 16 Whishaw, I.Q. and Kolb, B., Sparing of skilled forelimb reaching and corticospinal projections after neonatal motor cortex removal or hemidecortication in the rat: support for the Kennard doctrine, Brah~ Res., 451 (1988) 97-114. 17 Whishaw, I.Q., O'Connor, R.B. and Dunnet, S.B., The contributions of motor cortex, nigrostriatal dopamine and caudateputamen to skilled forelimb use in the rat, Brain, 109 (1986) 805-843. 18 Whishaw, I.Q. and Pellis, S.M., The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component, Behav. Brahl. Res., 41 (1990) 77-91. 19 Whishaw, I.Q., Pellis, S.M. and Gorny, B.P., Skilled reaching in rats and humans: evidence for parallel development or homology, Behav. Brabz Res., 47 (1992) 59-70. 20 Whishaw, I.Q. and Tomie, J., Olfaction directs skilled forelimb reaching in the rat, Behav. Brain Res., 32 (1989) 11-21. 21 Winer, B.J., Statistical Principlesbl Expedmental Design, lqcGrawHill, New York, 1962.
