Peripheral and cerebral asymmetries in the rat

Science

Volumn 278, Issue 5337, 1997, Pages 483-486

  LaMendola, Nicholas P ^a   Bever, Thomas G ^b  

^a University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ARTICLE; BRAIN ASYMMETRY; CONTROLLED STUDY; FEEDING BEHAVIOR; LEARNING; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

ANIMALS; BRAIN; DOMINANCE, CEREBRAL; FUNCTIONAL LATERALITY; MALE; MAZE LEARNING; RATS; RATS, SPRAGUE-DAWLEY; VIBRISSAE;

ANIMALIA;

EID: 0030723330     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.278.5337.483     Document Type: Article

References (64)

1. Reviewed in D. Kimura, Sci. Am. 228 (no. 3), 70 (1973).
2. M. Kinsbourne, in Attention and Performance, P. M. A. Rabbitt and S. Dornic, Eds. (Academic Press, New York, 1975), pp. 81-97.
3. Some contemporary examples of proposed differences in LH-RH processing include categorical versus coordinate processing [S. M. Kosslyn, Psychol. Rev. 94, 148 (1987)], analytic versus holistic processing [J. Levy, Nature 224, 614 (1969); T. G. Bever, in Mechanisms of Language Development, E. Huxley and D. Ingram, Eds. (Wiley, New York, 1970), pp. 186-230], and serial versus parallel processing [V. L. Bianki, The Right and Left Hemispheres of the Animal Brain: Cerebral Lateralization of Function (Gordon & Breach, New York, 1988)].
4. Some contemporary examples of proposed differences in LH-RH processing include categorical versus coordinate processing [S. M. Kosslyn, Psychol. Rev. 94, 148 (1987)], analytic versus holistic processing [J. Levy, Nature 224, 614 (1969); T. G. Bever, in Mechanisms of Language Development, E. Huxley and D. Ingram, Eds. (Wiley, New York, 1970), pp. 186-230], and serial versus parallel processing [V. L. Bianki, The Right and Left Hemispheres of the Animal Brain: Cerebral Lateralization of Function (Gordon & Breach, New York, 1988)].
5. Some contemporary examples of proposed differences in LH-RH processing include categorical versus coordinate processing [S. M. Kosslyn, Psychol. Rev. 94, 148 (1987)], analytic versus holistic processing [J. Levy, Nature 224, 614 (1969); T. G. Bever, in Mechanisms of Language Development, E. Huxley and D. Ingram, Eds. (Wiley, New York, 1970), pp. 186-230], and serial versus parallel processing [V. L. Bianki, The Right and Left Hemispheres of the Animal Brain: Cerebral Lateralization of Function (Gordon & Breach, New York, 1988)].
6. Some contemporary examples of proposed differences in LH-RH processing include categorical versus coordinate processing [S. M. Kosslyn, Psychol. Rev. 94, 148 (1987)], analytic versus holistic processing [J. Levy, Nature 224, 614 (1969); T. G. Bever, in Mechanisms of Language Development, E. Huxley and D. Ingram, Eds. (Wiley, New York, 1970), pp. 186-230], and serial versus parallel processing [V. L. Bianki, The Right and Left Hemispheres of the Animal Brain: Cerebral Lateralization of Function (Gordon & Breach, New York, 1988)].
7. R. A. Jacobs, M. I. Jordan, A. G. Barto, Cognit. Sci. 15, 219 (1991).
8. Reviewed in J. L. Bradshaw and L. J. Rogers, The Evolution of Lateral Asymmetries, Language, Tool Use, and Intellect (Academic Press, New York, 1993), a review of laterality in vertebrates.
9. LH specialization for communicative behaviors has been reported in zebra finches [F. Nottebohm and M. E. Nottebohm, J. Comp. Physiol. A 108, 171 (1976) ] and nonhuman primates [H. E. Heffner and R. S. Heffner, J. Neurophysiol. 56, 683 (1986)].
10. LH specialization for communicative behaviors has been reported in zebra finches [F. Nottebohm and M. E. Nottebohm, J. Comp. Physiol. A 108, 171 (1976) ] and nonhuman primates [H. E. Heffner and R. S. Heffner, J. Neurophysiol. 56, 683 (1986)].
11. Physiological asymmetries in mice and rats are reviewed in [G. F. Sherman and A. M. Galaburda, in Cerebral Lateralization in Nonhuman Species, S. D. Click, Ed. (Academic Press, Orlando, FL, 1985), pp. 89-106]. Much of the literature on individual behavioral asymmetries arises from studies of paw preference [R. L. Collins, J. Hered. 59, 9 (1968)] and spontaneous turning preference [B. Zimmerberg, S. D. Glick, T. P. Jerussi, Science 185, 623 (1974)]. Castellano et al. [M. A. Castellano, M. D. Diaz Palarea, J. Barroso, M. Rodriguez, Behav. Neurosci. 103, 46 (1989)] have reported some side preferences for specific tasks at the population level.
12. Physiological asymmetries in mice and rats are reviewed in [G. F. Sherman and A. M. Galaburda, in Cerebral Lateralization in Nonhuman Species, S. D. Click, Ed. (Academic Press, Orlando, FL, 1985), pp. 89-106]. Much of the literature on individual behavioral asymmetries arises from studies of paw preference [R. L. Collins, J. Hered. 59, 9 (1968)] and spontaneous turning preference [B. Zimmerberg, S. D. Glick, T. P. Jerussi, Science 185, 623 (1974)]. Castellano et al. [M. A. Castellano, M. D. Diaz Palarea, J. Barroso, M. Rodriguez, Behav. Neurosci. 103, 46 (1989)] have reported some side preferences for specific tasks at the population level.
13. Physiological asymmetries in mice and rats are reviewed in [G. F. Sherman and A. M. Galaburda, in Cerebral Lateralization in Nonhuman Species, S. D. Click, Ed. (Academic Press, Orlando, FL, 1985), pp. 89-106]. Much of the literature on individual behavioral asymmetries arises from studies of paw preference [R. L. Collins, J. Hered. 59, 9 (1968)] and spontaneous turning preference [B. Zimmerberg, S. D. Glick, T. P. Jerussi, Science 185, 623 (1974)]. Castellano et al. [M. A. Castellano, M. D. Diaz Palarea, J. Barroso, M. Rodriguez, Behav. Neurosci. 103, 46 (1989)] have reported some side preferences for specific tasks at the population level.
14. Physiological asymmetries in mice and rats are reviewed in [G. F. Sherman and A. M. Galaburda, in Cerebral Lateralization in Nonhuman Species, S. D. Click, Ed. (Academic Press, Orlando, FL, 1985), pp. 89-106]. Much of the literature on individual behavioral asymmetries arises from studies of paw preference [R. L. Collins, J. Hered. 59, 9 (1968)] and spontaneous turning preference [B. Zimmerberg, S. D. Glick, T. P. Jerussi, Science 185, 623 (1974)]. Castellano et al. [M. A. Castellano, M. D. Diaz Palarea, J. Barroso, M. Rodriguez, Behav. Neurosci. 103, 46 (1989)] have reported some side preferences for specific tasks at the population level.
15. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
16. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
17. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
18. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
19. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
20. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
21. Lesion studies of hemispheric superiority on spatial tasks in the rat are contradictory. Two studies report inferior spatial learning when the RH is lesioned [D. P. Crowne, M. F. Novotny, S. E. Maier, R. Vitols, Behav. Neurosci. 106, 811 (1992); V. King and J. V. Corwin, Behav. Brain Res. 50, 53 (1992)]. One study reports the opposite [K. J. Burcham, B. Haskins, J. V. Corwin, Soc. Neurosci. Abstr. 22, 682 (1996)]. Kolb et al. [B. Kolb, A. Mackintosh, I. Q. Whishaw, Behav. Neurosci. 98, 44 (1984)] used a battery of unilateral lesion studies and reported no behavioral asymmetries on spatial tasks. Using a unilateral spreading depression paradigm, V. L. Bianki [in (3), p. 330] reported no spatial asymmetry in learning a spatial task except that the left hemisphere moved faster. Finally, there are two conflicting studies of rats learning a Morris water maze with monocular vision: Female split-brain rats learned the maze better with the right eye intact [A. Adelstein and D. P. Crowne, Behav. Neurosci. 105, 459 (1991); male rats handled in infancy learned the maze better with the left eye intact [P. E. Cowell, N. S. Waters, V. H. Denenberg, Laterality, in press.
22. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
23. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
24. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
25. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
26. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
27. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
28. S. B. Vincent, Behav. Monogr. 9, 1 (1912); E. Guic-Robles, C. Valdivieso, G. Guajardo, Behav. Brain Res. 31, 285 (1989); H. R. Schiffman et al., Anim. Behav. 18, 290 (1970); K. A. Hutson and R. B. Masterton, J. Neurophysiol. 56, 1196 (1986); A. S. Ahl, Vet. Res. Commun. 10, 245 (1986); J. P. Huston et al., Exp. Neurol. 93, 380 (1986); A. A. Dunn-Meynell and B. E. Levin, Brain Res. 675, 143 (1995).
29. 2 in area suspended about 25.4 cm above its entry, and mazes were located on a table in running rooms (1.83 × 1.83 m) with eccentric lighting sources near the 2.44-m-high ceiling. A baited arm had three Noyes 45-mg pellets in a 3.175-cm-deep, 3.81-cm-wide well at its far end. Thirty-two 90-to 120-day-old male Sprague-Dawley albino rats from Harlan Sprague Dawley, were run at 85 to 90% of their ad lib weight after about a week of daily handling. All animals were individually housed and cared for according to animal care guidelines at the University of Rochester and University of Arizona. A rat's initial response to the maze situation is sometimes emotional. We pretrained animals on an initial maze in part because prior research suggests the emotionality itself may be asymmetrical [V. H. Denenberg, Behav. Brain Sci. 4, 1 (1981)]. We defined completely correct performance as entering each baited alley once and eating the food in it; entering a never-baited arm or reentering any arm was counted as an error. Performance on the initial maze was highly variable, but there were no significant correlations between number of errors on the training maze and on the second maze. The asymptotic error score for the last 10 trials on maze 1 were not significantly different in the four experimental groups. However, to further reduce the effect of interrat variability, we converted rats' performance on the second maze into standardized scores. The last 10 to 15 trials of the training maze determined the baseline mean number of errors and standard deviation for each rat. Each measure of errors on the second maze for the rat was converted to standard scores by using this mean and standard deviation. All statistical analyses of errors were done on these standard scores. Occasionally, rats just sit in a maze, which can distort overall analyses. We excluded the following trials from analysis: in the normal maze learning study, any trial longer than 10 min; in the distorted maze studies, any trial longer than 5 min. In all, fewer than 2% of trials were excluded; there was no relation between the number of excluded trials to unilateral conditions in any study.
30. 2 in area suspended about 25.4 cm above its entry, and mazes were located on a table in running rooms (1.83 × 1.83 m) with eccentric lighting sources near the 2.44-m-high ceiling. A baited arm had three Noyes 45-mg pellets in a 3.175-cm-deep, 3.81-cm-wide well at its far end. Thirty-two 90-to 120-day-old male Sprague-Dawley albino rats from Harlan Sprague Dawley, were run at 85 to 90% of their ad lib weight after about a week of daily handling. All animals were individually housed and cared for according to animal care guidelines at the University of Rochester and University of Arizona. A rat's initial response to the maze situation is sometimes emotional. We pretrained animals on an initial maze in part because prior research suggests the emotionality itself may be asymmetrical [V. H. Denenberg, Behav. Brain Sci. 4, 1 (1981)]. We defined completely correct performance as entering each baited alley once and eating the food in it; entering a never-baited arm or reentering any arm was counted as an error. Performance on the initial maze was highly variable, but there were no significant correlations between number of errors on the training maze and on the second maze. The asymptotic error score for the last 10 trials on maze 1 were not significantly different in the four experimental groups. However, to further reduce the effect of interrat variability, we converted rats' performance on the second maze into standardized scores. The last 10 to 15 trials of the training maze determined the baseline mean number of errors and standard deviation for each rat. Each measure of errors on the second maze for the rat was converted to standard scores by using this mean and standard deviation. All statistical analyses of errors were done on these standard scores. Occasionally, rats just sit in a maze, which can distort overall analyses. We excluded the following trials from analysis: in the normal maze learning study, any trial longer than 10 min; in the distorted maze studies, any trial longer than 5 min. In all, fewer than 2% of trials were excluded; there was no relation between the number of excluded trials to unilateral conditions in any study.
31. Rats in each unilateral whisker condition learned the maze to some degree over the 4 days. Linear trend analysis showed improvement across 4 days: F(1,6) = 16.71, P < 0.05 for LW-intactrats;F(1,7) = 11.75, P < 0.01 for RW-intact rats. There was considerable variability on the second and third days, but a comparison of performance on the first and fourth days showed significant improvement for both LW-intact rats [F(1,12) = 7.99, P < 0.01] and RW-intact rats [F(1, 14) = 9.15, P < 0.01].
32. Rats in each unilateral KCl condition learned the maze to some degree over the 4 days. Rats with the LH intact showed a significant descending linear trend [F(1,6) = 16.71, P < 0.001], as did RH-intact rats [F(1,9) = 14.20, P < 0.001]. In addition, the fourth-day performance was better than the first-day performance for LH-intact rats [F(1,12) = 7.02, P < 0.01] and for RH-intact rats [F(1,18) = 18.51, P < 0.001].
33. We also ran two groups of rats without any unilateral treatment while they learned the second maze. One group of six rats was subjected to the same Halothane procedure (21) as rats with anesthetized whiskers, but no lidocaine was administered; the other group of eight rats had cannulae surgically installed (22), but only saline-soaked pledgets were placed in both cannulae before each day's training. Both groups learned the second maze significantly better than rats in either anesthetized whisker condition and better than rats in the RH-intact condition. Both groups performed within 10% of rats in the LH-intact condition. These results suggest that the LH-intact rat and the untreated rat are accessing the same level of learning capacity. The very poor overall performance of rats in each anesthetized whisker condition may reflect aversion to having half the whiskers numbed; in contrast, prior research has suggested that KCl-induced cortical spreading depression is not aversive [V. I. Koroleva and J. Bures, Neurosci. Lett. 149, 153 (1993)]. Another informative control condition would be to anesthetize both whisker sets. We tried this with four animals. They could move through the maze but had great difficulty in the last stages of locating the food rewards; the result was that they did not eat the rewards and so cannot be compared with rats in the other conditions.
34. 2 = 0.06) or within each of the experimental conditions. Also, by using turn bias on the initial maze as a measure, all unilateral conditions had about the same ratio of right-turning versus left-turning rats. The potential importance of a turning-bias confound prompted us to replicate the initial unilateral whisker study with explicit attention to turn bias and performance on the initial maze. We trained 16 rats on the initial maze as before. Then we assigned 8 rats to the LW-and 8 rats to the RW-anesthetized condition, so that each condition had the same proportion of rats showing a right-turn bias on the initial maze; we also arranged the two groups so that their asymptotic performance on the initial maze was within a few percentage points. The maze learning for 4 days showed the same pattern as in our original study. Rats in each condition learned the maze, but rats with RW intact learned the second maze with fewer errors than rats with LW intact. Also, in this study, more animals with LW intact failed to find all five rewards within the allotted time on a given trial.
35. J. O'Keefe, Hippocampus 1, 230 (1991).
36. B. L. McNaughton et al., J. Cognit. Neurosci. 3, 190 (1991); R. L. Gallistel and A. E. Cramer, J. Exp. Biol. 199, 211 (1996); D. S. Olton, in (10).
37. B. L. McNaughton et al., J. Cognit. Neurosci. 3, 190 (1991); R. L. Gallistel and A. E. Cramer, J. Exp. Biol. 199, 211 (1996); D. S. Olton, in (10).
38. B. L. McNaughton et al., J. Cognit. Neurosci. 3, 190 (1991); R. L. Gallistel and A. E. Cramer, J. Exp. Biol. 199, 211 (1996); D. S. Olton, in (10).
39. We also ran rats without any whisker anesthesia on the same paradigms. After they learned the initial maze, the rats were subjected to the same Halothane procedure as the whisker-anesthetized conditions (22) but without any unilateral anesthesia. In the repointed start alley condition, five bilaterally intact rats then performed better than rats with either unilateral whisker condition; this suggests that rats in both unilateral conditions are somewhat affected by a change in the start alley. In the maze-rotation condition, five bilaterally intact rats performed better than the RW-intact rats, but they performed the same as the LW-intact rats. This suggests that the intact animal can learn to ignore the maze rotation, whereas the isolated LH-RW system cannot.
40. J. O'Keefe and L. Nadel, The Hippocampus As a Spatial Map (Clarendon Press, Oxford, 1978); M. A. Wilson and B. L. McNaughton, Science 261, 1055 (1995); N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, MA, 1993); E. L. Jarrard, Behav. Neural Biol. 60, 9 (1993).
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42. J. O'Keefe and L. Nadel, The Hippocampus As a Spatial Map (Clarendon Press, Oxford, 1978); M. A. Wilson and B. L. McNaughton, Science 261, 1055 (1995); N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, MA, 1993); E. L. Jarrard, Behav. Neural Biol. 60, 9 (1993).
43. J. O'Keefe and L. Nadel, The Hippocampus As a Spatial Map (Clarendon Press, Oxford, 1978); M. A. Wilson and B. L. McNaughton, Science 261, 1055 (1995); N. J. Cohen and H. Eichenbaum, Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, MA, 1993); E. L. Jarrard, Behav. Neural Biol. 60, 9 (1993).
44. Many lesion studies support the role of the posterior parietal cortex [B. V. DiMattia and R. P. Kesner, Behav. Neurosci. 102, 397 (1988)] and ventrolateral orbital cortex [J. V. Corwin, M. Fussinger, R. C. Meyer, V. R. King, R. L. Reep, Behav. Brain Res. 61, 79 (1994)] in the processing of allocentric space and the medial agranular cortex [B. Kolb, in The Cerebral Cortex of the Rat, B. Kolb and R. C. Tees, Eds. (MIT Press, Cambridge, MA, 1990), pp. 437-458] and prefrontal cortex [R. P. Kesner et al., Behav. Neurosci. 103, 956 (1989)] in egocentric space.
45. Many lesion studies support the role of the posterior parietal cortex [B. V. DiMattia and R. P. Kesner, Behav. Neurosci. 102, 397 (1988)] and ventrolateral orbital cortex [J. V. Corwin, M. Fussinger, R. C. Meyer, V. R. King, R. L. Reep, Behav. Brain Res. 61, 79 (1994)] in the processing of allocentric space and the medial agranular cortex [B. Kolb, in The Cerebral Cortex of the Rat, B. Kolb and R. C. Tees, Eds. (MIT Press, Cambridge, MA, 1990), pp. 437-458] and prefrontal cortex [R. P. Kesner et al., Behav. Neurosci. 103, 956 (1989)] in egocentric space.
46. Many lesion studies support the role of the posterior parietal cortex [B. V. DiMattia and R. P. Kesner, Behav. Neurosci. 102, 397 (1988)] and ventrolateral orbital cortex [J. V. Corwin, M. Fussinger, R. C. Meyer, V. R. King, R. L. Reep, Behav. Brain Res. 61, 79 (1994)] in the processing of allocentric space and the medial agranular cortex [B. Kolb, in The Cerebral Cortex of the Rat, B. Kolb and R. C. Tees, Eds. (MIT Press, Cambridge, MA, 1990), pp. 437-458] and prefrontal cortex [R. P. Kesner et al., Behav. Neurosci. 103, 956 (1989)] in egocentric space.
47. Many lesion studies support the role of the posterior parietal cortex [B. V. DiMattia and R. P. Kesner, Behav. Neurosci. 102, 397 (1988)] and ventrolateral orbital cortex [J. V. Corwin, M. Fussinger, R. C. Meyer, V. R. King, R. L. Reep, Behav. Brain Res. 61, 79 (1994)] in the processing of allocentric space and the medial agranular cortex [B. Kolb, in The Cerebral Cortex of the Rat, B. Kolb and R. C. Tees, Eds. (MIT Press, Cambridge, MA, 1990), pp. 437-458] and prefrontal cortex [R. P. Kesner et al., Behav. Neurosci. 103, 956 (1989)] in egocentric space.
48. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
49. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
50. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
51. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
52. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
53. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
54. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
55. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
56. M. Banich, Neuropsychology: The Neural Bases of Mental Function (Houghton-Mifflin, Boston, 1997), chap. 6; H. D. Brown and S. M. Kosslyn in Brain Asymmetry, R. J. Davidson and K. Hugdahl, Eds. (MIT Press, Cambridge, MA, 1995), pp. 77-97. At a general level, prior research suggests that spatial ability is dominant in the RH of humans, which appears to be the opposite of our findings in rats [B. Milner, Neuropsychologia 3, 317 (1965); M. Habib and A. Sirigu, Cortex 23, 73 (1987)]. However, almost all research on humans has been devoted to simple perceptual problems in external space instead of personal way finding. In fact, the LH has been implicated in Euclidian geometrical processing [L. Franco and R. W. Sperry, Neuropsychologia 15, 107 (1977); E. DeRenzi, Disorders of Space Exploration and Cognition (Wiley, New York, 1982); Z. Mehta and F. Newcombe, Cortex 27 153 (1991)], and both hemispheres contribute to personal way-finding skills [G. Ratcliff and F. Newcombe, J. Neurol. Neurosurg. Psychiatr. 36, 448 (1973); E. J. Maguire, T. Burke, J. Phillips, H. Staunton, Neuropsychologia 34, 993 (1996)].
57. The left-right contrasts for working memory errors were significant for whiskers F(1,13) = 7.94, P < 0.01] and for hemisphere [F(1,15) = 4.73, P < 0.05] conditions. Contrasts in both conditions for reference memory errors were not significant. Note that reference memory errors plus working memory errors does not add up to the number of overall errors. This is because the overall error measure includes cases when the rat reenters an always unbaited arm; we omitted those from this differential analysis because such errors are simultaneously reference and working memory errors.
58. The procedure was adapted from the technique described in D. H. Thor and W. B. Ghiselli, Psychol. Rep. 33, 815 (1973 ). The rat was first lightly anesthetized by inhalation of Halothane; then 0.2 ml of 2% lidocaine with epinephrine was subcutaneously injected into the mystacial vibrissal region on one side. The operational test for numbing the whiskers was that they stopped twitching. Each rat was always injected on the same side of the whiskers across all four daily experimental sessions. We unilaterally anesthetized the whiskers instead of shaving them because prior research showed that rats accommodate quickly to a permanent loss of whiskers: H. Milani, H. Steiner, J. P. Huston, Behav. Neurosci. 103, 1067 (1989). We trained rats on the second maze for only 4 days because of concern that repeated injections would cause discomfort.
59. The procedure was adapted from the technique described in D. H. Thor and W. B. Ghiselli, Psychol. Rep. 33, 815 (1973 ). The rat was first lightly anesthetized by inhalation of Halothane; then 0.2 ml of 2% lidocaine with epinephrine was subcutaneously injected into the mystacial vibrissal region on one side. The operational test for numbing the whiskers was that they stopped twitching. Each rat was always injected on the same side of the whiskers across all four daily experimental sessions. We unilaterally anesthetized the whiskers instead of shaving them because prior research showed that rats accommodate quickly to a permanent loss of whiskers: H. Milani, H. Steiner, J. P. Huston, Behav. Neurosci. 103, 1067 (1989). We trained rats on the second maze for only 4 days because of concern that repeated injections would cause discomfort.
60. Before rats were trained on the initial maze, 6-mm cannulae with a 4-mm internal diameter were affixed above a 2-mm hole in the skull 3-to 4-mm off the midline, midway between lambda and bregma - roughly above the parietotemporal cortex. Thirty minutes before each daily second maze learning session, a cotton pellet soaked in a 6% KCl solution was placed on the dura in the cannula above one hemisphere, and a pellet with saline solution was placed in the other cannula [A. A. P. Leão, J. Neurophysiol. 7, 359 (1944); B. Grafstein, ibid. 19, 154 (1955)]. Prior studies characteristically used high KCl concentrations, at least 20%. We used a 6% solution to reduce the possibility of a motor hemiplegia or sensory neglect - all animals with KCl administered still performed the edge-paw placement test bilaterally and showed no sign of unilateral dysfunction. Recording of cortical electroencephalograms with two rats suggests that with our procedure the active depolarization period lasts 5 to 10 min. Thus, by the time rats ran in the maze, active depolarization may have been finished; the treated hemisphere may have been in a state of mild edema and consequent mild ischemia.
61. Before rats were trained on the initial maze, 6-mm cannulae with a 4-mm internal diameter were affixed above a 2-mm hole in the skull 3-to 4-mm off the midline, midway between lambda and bregma - roughly above the parietotemporal cortex. Thirty minutes before each daily second maze learning session, a cotton pellet soaked in a 6% KCl solution was placed on the dura in the cannula above one hemisphere, and a pellet with saline solution was placed in the other cannula [A. A. P. Leão, J. Neurophysiol. 7, 359 (1944); B. Grafstein, ibid. 19, 154 (1955)]. Prior studies characteristically used high KCl concentrations, at least 20%. We used a 6% solution to reduce the possibility of a motor hemiplegia or sensory neglect - all animals with KCl administered still performed the edge-paw placement test bilaterally and showed no sign of unilateral dysfunction. Recording of cortical electroencephalograms with two rats suggests that with our procedure the active depolarization period lasts 5 to 10 min. Thus, by the time rats ran in the maze, active depolarization may have been finished; the treated hemisphere may have been in a state of mild edema and consequent mild ischemia.
62. Rats with LW intact made significantly more learning errors than rats with RW intact [F(1,13) = 8.05, P < 0.01]. Rats with LH intact made fewer errors than rats with RH intact [F(1,15) = 5.96, P < 0.01]. Each of three distinct normal maze baiting patterns in maze 2 elicited the same overall superiority of the LH-RW system.
63. With the same initial maze as in the previous experiment, we tested 56 male Sprague-Dawley albino rats (90 to 120 days old) on a variation of the selectively baited radial maze task.
64. Rats with LW intact made marginally more errors than rats with RW intact when the starting position was changed on each trial [F(1,26) = 2.20, P < 0.1]. However, the difference for working memory errors alone was significant [F(1,26) = 4.20, P < 0.05], Rats with RW intact made more errors than rats with LW intact when the maze was rotated to a new position before each trial [F(1,12) = 4.05, P < 0.05]. 27. We wish to thank the following: many undergraduate assistants, notably P. Krein, J. Pak, J. Lyons, and J. Weimer at the University of Rochester and L. Fambauch at the University of Arizona; C. Burgess, K. O'Connor, and J. Ison for helping to develop our use of the spreading depression technique; M. Banich, C. Barnes, F. Bedford, J. Bures, V. Denenberg, L. Gerken, J. Kelley, B. Kolb, B. McNaughton, M. Moscovitch, L. Nadel, and F. Wilson for their advice; an anonymous reviewer for calling our attention to the potential importance of turn bias; and the veterinary staffs of the University of Rochester and the University of Arizona for advice on surgical techniques. Finally, we especially thank the director and personnel of the University of Arizona Animal Care Facility for generously providing laboratory space. Supported by private gifts to the University of Rochester and the University of Arizona.