Brain Research, 166 (1979) 405-408 © Elsevier/North-Holland Biomedical Press
405
Hyperflexion and changes in interlimb coordination of locomotion induced by cooling of the cerebellar intermediate cortex in normal cats
MASAO UDO, KANJI MATSUKAWA and HARUO KAMEI
Department of Biophysical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka" Osaka 560 (Japan) (Accepted December 28th, 1978)
In observation of walking cats with chronic cerebellar cortical lesions, Chambers and Sprague reported that the hyperflexion occurred in the ipsilateral limbs after lesions in the intermediate part 1. The hyperflexed locomotor movements also occurred in the ipsilateral forelimb when Lobule V of the intermediate cortex was cooled in the decerebrate walking catsL The present work was undertaken to see whether the hyperflexion that was induced in a forelimb actually leads to a disturbance in coordinated execution of 4-legged locomotion. For this purpose, it was preferable to observe normal cats walking on a treadmill (speed, 34-102 cm/sec) during the cerebellar cooling. The occipital bone of adult cats ( n = 4 ) was drilled through under Nembutal anaesthesia, 9-40 days before the experiments, and a plastic socket was fixed to place a cooling probe under direct vision upon the surface of the intermediate Lobule V of the right side. Dura mater was opened in 2 cats, and left intact in the others. The probe was made of a copper plate (cerebellar contact area, 3 × 4 sq.mm) attached to a copper tube. Through the copper tube, cooled ethylalcohol was circulated for 2-4 min via elastic tubes from a temperature-controlled bath (flow rate, 8-10 cc/sec). Compared with cooling conditions of the decerebrate cats 5, the temperature of ethanol had to be made considerably lower (between--30 a n d - - 6 0 °C) to induce similar hyperflexed movements. However, acute destructions of intermediate Lobule V of the decerebrate walking cats gave similar hyperflexion as present experiments, indicating that such low temperature was needed to cool this Lobule (see below), probably due to the presence of the dura or a layer (1-1.5 mm thick) of adhesive connective tissue that proliferated on the cerebellar surface. Statistical test (t-test) was made for changes in a parameter of locomotor movements, i.e., its mean value for more than 10 successive steps during cooling period was compared with that for equivalent steps before and after the cooling. The changes were reproduced in all of 3-7 cooling sessions that were made on a cat. Mean (4- S.D.) values from a representative session are given below. Abbreviations, RF, LF and RH, LH: right, left forelimb and right, left hindlimb. Footfallpatterns. As reported in the decerebrate cats 5, the hyperflexed locomotor movements occurred in R F during cooling, typical mean -+- S.D. values for the
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maximally flexed elbow angle being 71.7 4- 2.7 ° before, and 49.4 4- 5.4 ° during cooling (p < 0.01 ; further details in the next section). Probably due to this hyperflexion, more time was spent to place down the limb and duration of RF swing phase was 13-43 prolonged (P < 0.01). In contrast, duration of RF stance phase was 6-21 ~ shortened (P < 0.01). In LF, duration of the stance phase was 5-10 ~ prolonged (P < 0.01), the limb being lifted off at backward point; and duration of the swing phase was 13-21 shortened (P < 0.01), both of flexion and extension movements in the swing phase occurring with higher angular velocities (not illustrated). Length of a step cycle was nearly equal among 4 limbs, although slightly changed in both directions (e.g., mean 4- S.D. at RF, 765 4- 32 msec before, and 735 4- 29 msec during cooling, the other limbs giving similar values). As a result, the alternated footfall pattern in bilateral forelimbs was clearly changed into an asymmetric pattern, e.g., period of bi-support where both forelimbs were contact was 105 4- 14 msec and 138 4- 26 msec before cooling, and 142 4- 18 msec and 69 4- 18 msec during cooling as shown in Fig. 1A, B.
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Fig. 1. Effects of cooling of the cerebellar intermediate cortex over Lobule V. A, B: footfall patterns of both forelimbs. Duration of stance (horizontal bar) and swing (open space between bars) phases was shown from the moments of RF lift-off (vertical interrupted line) over 5 step cycles, before (A) and during (B) cooling. C: view from front before (solid line), and during (interrupted line) cooling. E: joint angles of RF (ordinates) versus time (abscissa). Before (circles) and during (crosses) cooling. Measured according to the scheme in D, elbow (1), shoulder (2) and scapular (3)joint. Horizontal bars below indicate stance phase before (single thick line) and during (double thin lines) cooling. Swing phase (open space between bars) was divided into F and E1 components according to the angle plots of the elbow joint. Measurements in A - E were all made from the videocoder system (time resolution, 16 msec), and angular velocity (angle versus time) was calculated by smoothing 5 neighbouring ordinates ~.
407 There was virtually no change in the movements of both hindlimbs where the symmetrical alternation was maintained. Asymmetry was also noticed in timings of hind- and forelimb touchdowns between right and left sides, e.g., difference between R H and R F touchdowns became longer (129 ± 11 msec before, and 281 4- 51 msec during cooling) than that between L H and LF touchdowns (150 4- 11 msec before, and 131 4- 14 msec during cooling). It was characteristic that cats walked with their body trunk obviously rotated about its longitudinal axis (15-20 ° declined to the right side, Fig. 1C) and also about its vertical axis, its caudal half being 12-26 ° displaced to the right as to often lean to the right side wall of the test chamber. A major factor that concerns with these rotations may well be a delay in touchdown of RF, its touchdown at appropriate timings being considered by previous authors ~,4 to work so as to counteract rotational movements of body trunk that were imposed by LF and hindlimbs. The changes in LF might work to compensate rotation about the transverse axis and might facilitate the rotation about the other 2 axes. A quantitative evaluation of these dynamics should be an interesting subject of succeeding investigations. Joint movements, cooled area, E M G and their comparison with decerebrate cats. Changes in joint movements of RF are shown in Fig. I E. The limb was lifted off with less joint angles (at elbow, 127 4- 4.0 ° before, and 110 4- 3.1 ° during cooling, P < 0.01), and the elbow was clearly hyperflexed (values above), and extension movement to place down the limb in the E1 phase developed with reduction (13 ~ ) in angular velocity. These changes were similar to those from the decerebrate cats when the intermediate Lobule V was cooled upto depth of about 5 mm with concomitant cooling of the adjacent hemisphere 5. In this regard, acute destructions with 5 mm depth were recently made in the intermediate Lobule V of the decerebrate cats (n=3). Changes with similar magnitudes as in Fig. 1E were thereby induced, suggesting that the present cooling effects can be, at least largely, attributable to this single Lobule.
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500rnsec Fig. 2. Changes of EMG patterns of both forelimbs during cooling. EMGs were recorded through bipolar wire electrodes from elbow extensor (M. triceps brachii, EE) and elbow flexor (M. biceps brachii, EF) of right (with prefix i) and left (with prefix c) forelimbs. Notations b and d, before and during cooling. After passed through a high-pass filter (with 3 dB down at 25 Hz) and rectified, the EMGs were integrated with a time constant of 10 msec, and traces of the integrated EMGs were superimposed over 5 succeeding steps, horizontal bars below indicating stance phase of each step.
408 E M G patterns of forelimbs are shown in Fig. 2. In RF, enhanced activity of the flexor was clearly seen in the late stance and F phases leading to the hyperflexion. Just after R F touchdown, there was enhanced activity of extensors, probably the limb being loaded with more weight than usual due to the delayed touchdown. The extensor activity of R F was shorter, and that of LF was longer in the stance phase as related to the changes in their stance durations. In LF, flexor activity was enhanced mainly in the F phase, and extensor activity was enhanced in the E1 phase, both being related to the shortening of the swing phase mentioned above. These changes in movements and E M G s of both forelimbs were seen with similar tendency in the decerebrate cats on cooling of the intermediate Lobule V 5 (Udo et al., unpublished). The present report demonstrates that the hyperflexed locomotor movements that were similar as reported in chronic cats ~ and decerebrate cats 5, occurred in a forelimb during cooling of Lobule V of the intermediate cortex of the normal cats walking on a treadmill. It was thereby observed that a modest delay in touchdown of the particular limb which was induced by cooling of a relevant Lobule, can cause obvious disturbance in execution of locomotion. In addition, similar gait disturbance was occasionally observed when the cats walked on the stopped treadmill, i.e., in overground locomotion. The similarity between cerebellar cooling effects of decerebrate and normal cats suggested that cerebellar control mechanisms of these walking cats are comparable.
1 Chambers, W. W. and Sprague, J. M., Functional localization in the cerebellum. II. Somatotopic organization in cortex and nuclei, Arch. Neurol. Psychiat. (Chic.), 74 (1955) 653-680. 2 Gray, J., Animal Locomotion, William Clowes, London, 1965, pp. 95-101. 3 Lanczos, C., Applied Analysis, Prentice Hall, Englewood Cliffs, N. J., 1956, pp. 321-324. 4 Manter, J., The dynamics of quadrupedal walking, J. exp. Biol., 15 (1938) 522-540. 5 Udo, M., Matsukawa, K. and Kamei, H., Effects of partial cooling of cerebellar cortex at Lobules V and IV of the intermediate part in the decerebrate walking cats under monitoring vertical floor reaction forces, Brain Research, 160 (1979) 559-564.
405
Hyperflexion and changes in interlimb coordination of locomotion induced by cooling of the cerebellar intermediate cortex in normal cats
MASAO UDO, KANJI MATSUKAWA and HARUO KAMEI
Department of Biophysical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka" Osaka 560 (Japan) (Accepted December 28th, 1978)
In observation of walking cats with chronic cerebellar cortical lesions, Chambers and Sprague reported that the hyperflexion occurred in the ipsilateral limbs after lesions in the intermediate part 1. The hyperflexed locomotor movements also occurred in the ipsilateral forelimb when Lobule V of the intermediate cortex was cooled in the decerebrate walking catsL The present work was undertaken to see whether the hyperflexion that was induced in a forelimb actually leads to a disturbance in coordinated execution of 4-legged locomotion. For this purpose, it was preferable to observe normal cats walking on a treadmill (speed, 34-102 cm/sec) during the cerebellar cooling. The occipital bone of adult cats ( n = 4 ) was drilled through under Nembutal anaesthesia, 9-40 days before the experiments, and a plastic socket was fixed to place a cooling probe under direct vision upon the surface of the intermediate Lobule V of the right side. Dura mater was opened in 2 cats, and left intact in the others. The probe was made of a copper plate (cerebellar contact area, 3 × 4 sq.mm) attached to a copper tube. Through the copper tube, cooled ethylalcohol was circulated for 2-4 min via elastic tubes from a temperature-controlled bath (flow rate, 8-10 cc/sec). Compared with cooling conditions of the decerebrate cats 5, the temperature of ethanol had to be made considerably lower (between--30 a n d - - 6 0 °C) to induce similar hyperflexed movements. However, acute destructions of intermediate Lobule V of the decerebrate walking cats gave similar hyperflexion as present experiments, indicating that such low temperature was needed to cool this Lobule (see below), probably due to the presence of the dura or a layer (1-1.5 mm thick) of adhesive connective tissue that proliferated on the cerebellar surface. Statistical test (t-test) was made for changes in a parameter of locomotor movements, i.e., its mean value for more than 10 successive steps during cooling period was compared with that for equivalent steps before and after the cooling. The changes were reproduced in all of 3-7 cooling sessions that were made on a cat. Mean (4- S.D.) values from a representative session are given below. Abbreviations, RF, LF and RH, LH: right, left forelimb and right, left hindlimb. Footfallpatterns. As reported in the decerebrate cats 5, the hyperflexed locomotor movements occurred in R F during cooling, typical mean -+- S.D. values for the
406
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maximally flexed elbow angle being 71.7 4- 2.7 ° before, and 49.4 4- 5.4 ° during cooling (p < 0.01 ; further details in the next section). Probably due to this hyperflexion, more time was spent to place down the limb and duration of RF swing phase was 13-43 prolonged (P < 0.01). In contrast, duration of RF stance phase was 6-21 ~ shortened (P < 0.01). In LF, duration of the stance phase was 5-10 ~ prolonged (P < 0.01), the limb being lifted off at backward point; and duration of the swing phase was 13-21 shortened (P < 0.01), both of flexion and extension movements in the swing phase occurring with higher angular velocities (not illustrated). Length of a step cycle was nearly equal among 4 limbs, although slightly changed in both directions (e.g., mean 4- S.D. at RF, 765 4- 32 msec before, and 735 4- 29 msec during cooling, the other limbs giving similar values). As a result, the alternated footfall pattern in bilateral forelimbs was clearly changed into an asymmetric pattern, e.g., period of bi-support where both forelimbs were contact was 105 4- 14 msec and 138 4- 26 msec before cooling, and 142 4- 18 msec and 69 4- 18 msec during cooling as shown in Fig. 1A, B.
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Fig. 1. Effects of cooling of the cerebellar intermediate cortex over Lobule V. A, B: footfall patterns of both forelimbs. Duration of stance (horizontal bar) and swing (open space between bars) phases was shown from the moments of RF lift-off (vertical interrupted line) over 5 step cycles, before (A) and during (B) cooling. C: view from front before (solid line), and during (interrupted line) cooling. E: joint angles of RF (ordinates) versus time (abscissa). Before (circles) and during (crosses) cooling. Measured according to the scheme in D, elbow (1), shoulder (2) and scapular (3)joint. Horizontal bars below indicate stance phase before (single thick line) and during (double thin lines) cooling. Swing phase (open space between bars) was divided into F and E1 components according to the angle plots of the elbow joint. Measurements in A - E were all made from the videocoder system (time resolution, 16 msec), and angular velocity (angle versus time) was calculated by smoothing 5 neighbouring ordinates ~.
407 There was virtually no change in the movements of both hindlimbs where the symmetrical alternation was maintained. Asymmetry was also noticed in timings of hind- and forelimb touchdowns between right and left sides, e.g., difference between R H and R F touchdowns became longer (129 ± 11 msec before, and 281 4- 51 msec during cooling) than that between L H and LF touchdowns (150 4- 11 msec before, and 131 4- 14 msec during cooling). It was characteristic that cats walked with their body trunk obviously rotated about its longitudinal axis (15-20 ° declined to the right side, Fig. 1C) and also about its vertical axis, its caudal half being 12-26 ° displaced to the right as to often lean to the right side wall of the test chamber. A major factor that concerns with these rotations may well be a delay in touchdown of RF, its touchdown at appropriate timings being considered by previous authors ~,4 to work so as to counteract rotational movements of body trunk that were imposed by LF and hindlimbs. The changes in LF might work to compensate rotation about the transverse axis and might facilitate the rotation about the other 2 axes. A quantitative evaluation of these dynamics should be an interesting subject of succeeding investigations. Joint movements, cooled area, E M G and their comparison with decerebrate cats. Changes in joint movements of RF are shown in Fig. I E. The limb was lifted off with less joint angles (at elbow, 127 4- 4.0 ° before, and 110 4- 3.1 ° during cooling, P < 0.01), and the elbow was clearly hyperflexed (values above), and extension movement to place down the limb in the E1 phase developed with reduction (13 ~ ) in angular velocity. These changes were similar to those from the decerebrate cats when the intermediate Lobule V was cooled upto depth of about 5 mm with concomitant cooling of the adjacent hemisphere 5. In this regard, acute destructions with 5 mm depth were recently made in the intermediate Lobule V of the decerebrate cats (n=3). Changes with similar magnitudes as in Fig. 1E were thereby induced, suggesting that the present cooling effects can be, at least largely, attributable to this single Lobule.
iEE
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500rnsec Fig. 2. Changes of EMG patterns of both forelimbs during cooling. EMGs were recorded through bipolar wire electrodes from elbow extensor (M. triceps brachii, EE) and elbow flexor (M. biceps brachii, EF) of right (with prefix i) and left (with prefix c) forelimbs. Notations b and d, before and during cooling. After passed through a high-pass filter (with 3 dB down at 25 Hz) and rectified, the EMGs were integrated with a time constant of 10 msec, and traces of the integrated EMGs were superimposed over 5 succeeding steps, horizontal bars below indicating stance phase of each step.
408 E M G patterns of forelimbs are shown in Fig. 2. In RF, enhanced activity of the flexor was clearly seen in the late stance and F phases leading to the hyperflexion. Just after R F touchdown, there was enhanced activity of extensors, probably the limb being loaded with more weight than usual due to the delayed touchdown. The extensor activity of R F was shorter, and that of LF was longer in the stance phase as related to the changes in their stance durations. In LF, flexor activity was enhanced mainly in the F phase, and extensor activity was enhanced in the E1 phase, both being related to the shortening of the swing phase mentioned above. These changes in movements and E M G s of both forelimbs were seen with similar tendency in the decerebrate cats on cooling of the intermediate Lobule V 5 (Udo et al., unpublished). The present report demonstrates that the hyperflexed locomotor movements that were similar as reported in chronic cats ~ and decerebrate cats 5, occurred in a forelimb during cooling of Lobule V of the intermediate cortex of the normal cats walking on a treadmill. It was thereby observed that a modest delay in touchdown of the particular limb which was induced by cooling of a relevant Lobule, can cause obvious disturbance in execution of locomotion. In addition, similar gait disturbance was occasionally observed when the cats walked on the stopped treadmill, i.e., in overground locomotion. The similarity between cerebellar cooling effects of decerebrate and normal cats suggested that cerebellar control mechanisms of these walking cats are comparable.
1 Chambers, W. W. and Sprague, J. M., Functional localization in the cerebellum. II. Somatotopic organization in cortex and nuclei, Arch. Neurol. Psychiat. (Chic.), 74 (1955) 653-680. 2 Gray, J., Animal Locomotion, William Clowes, London, 1965, pp. 95-101. 3 Lanczos, C., Applied Analysis, Prentice Hall, Englewood Cliffs, N. J., 1956, pp. 321-324. 4 Manter, J., The dynamics of quadrupedal walking, J. exp. Biol., 15 (1938) 522-540. 5 Udo, M., Matsukawa, K. and Kamei, H., Effects of partial cooling of cerebellar cortex at Lobules V and IV of the intermediate part in the decerebrate walking cats under monitoring vertical floor reaction forces, Brain Research, 160 (1979) 559-564.
