Acta physiol. scand. 1979. 105. 251-253 From the 'Department of Physiolosy 111, Karolinska Institutet, and the 2Department of Physiology 11, Karolinska Institutet, Stockholm, Sweden
Control of the trunk during walking in the cat BY HANS CARLSON, ~ J O N THALBERTSMA and 'MICHAELZOMLEFER
While there is a great deal of information concerning the electromyographic (EMG) patterns and movements of the hindlimb in tetrapod locomotion (Grillner 1973, there is little knowledge about the control of the trunk. Recent experiments performed on the cat's lumbar back muscles have shown large portions, i.e. M. longissimus and iliocostalis, to be fast contracting and easily fatiguable, while the multifidi contract somewhat more slowly (Carlson 1978 a, b). The aim of this study has been to explore patterns of activity in the different lumbar back muscles during fast and slow walks and relate them to the trunk movements. Eleven experiments were performed on cats (n - 3 : 2.2, 2.3 and 3.2 kg), which were trained to walk on a moving treadmill or overground at cycle durations ranging from about 350 to 1 200 nis, corresponding to speeds ranging from 1.O to 0.2 m/s, respectively. Bipolar, intramuscular electrodes were chronically implanted (Zomlefer et af. 1977) into the multifidi (Mf), longissimus (Lo) and iliocostalis muscles at various levels along the lumbar spine (Ll-L6), as well as into both vasti lateralii (VL). The EMG wires were led percutaneously to a plug on the animal's back, which could be connected with a detachable cable to amplifiers. Electrode placement was verified post mortem. The movements of one hindlimb and the lower spine were recorded using a Selspot System (Selcom Co., Partille, Sweden). Small light emitting diodes were glued onto the shaved skin over the spinal processes at Th9, L3, and L5 as well as the iliac crest and the hip, knee, ankle metatarsophalangeal joints. Two cameras sampled each diode position at 160 Hz in both the sagittal and horizontal planes. Position and electromyographic data were fed online to a minicomputer (Hewlett-Packard 21 MX) for later processing. The EMG activity in both the medially located multifidi muscles and the lateral longissimus and iliocostalis displayed two distinct large bursts during each step cycle (see Fig. 1 A). The two bursts had similar durations and were synchronous in the different muscles, while each burst was tightly linked to the onset of the ipsi-and the contralateral VL activity (Fig. 1 B). The duration of the bursts increased nearly threefold (from about 150 to 400 ms) whereas the amplitude (mean value of each burst per unit time) decreased by a factor of four as cycle duration increased over the range studied. There will thus be two periods of activity in the lumbar back muscles during each step cycle. These bursts will coincide with the periods of overlapping EMG activity in the limb extensor muscles of the two sides, and thus they occur during the phases of double hindlimb support. 25 1
252
HANS CARLSON,
JONT
HALBERTSMA AND MICHAEL ZOMLEFER
1
ONSET(8) OF MUSCLE ACTIVITY IN RELATION TO IPS1 TOUCHDOWN.
130'
1
. . .. #-
I70' s
---L.--? aI
VL(k=0014)
aiMfL4Ist(k=-0040)
co VL i MfL4
-
i LoL4 Tr
HORIZONTAL Th9 ipsi L 3 L5 Th9 L3 L 5
-.. . \
L
L
co VL(k= - 0 4 4 0 ) ~1MfL42nd(k=-0580)
.5
1.0CYCLE DUR(8)
50 HORIZONTAL DISPLACEMENT OF. L 3 (mm)
(k=37mm/s)
+-iY-
E SAGITTAL Th 9 L5 Th9 L3 L5
SAGITTAL DISPLACEMENT OF L3 (mm)
*. .*
.
(k=-5mm.X
-v
Fig. I. A) Ankle angle (ANKLE) with rectified and filtered EMG's from ipsi- and contralateral VL, a s well as the ipsilateral Mf and Lo muscles a t the L 4 level (iVL, COVL,iMfL4 and iLoL4, respectively). Step cycle labeling, shown for the ipsilateral hindlimb, is the same as that used by Philippson (1905). B) Onset of EMG activity (relative to ipsilateral hindlimb touchdown) us. cycle duration (CYCLE DUR) for iVL, COVL, and the first and second bursts of iMfL4 (iMfL4lst and iMfL42nd). A positive value(+) indicates that the onset time is prior to ipsi-hindlimb touchdown. The time for onset of COVLwill increase with increasing cycle duration, since both hindlimbs are alternating in a given step cycle. C ) Horizontal plane displacements and angle. The three uppermost curves show the relative trajectories of the marker diodes at the Th9, L3, and L5 levels. Movement toward the ipsilateral side (see A) is defined by arrow (t).The fourth trace shows the net angular displacement determined by L5-L3-Th9 (see inset). Minimum value corresponds to lateral bending with concavity toward the ipsilateral side. D) Peak to peak displacements in horizontal plane (L3 level) vs. step cycle duration. E) Sagittal displacements and angle. The first three traces indicate the movements of the three back diodes (Th9, L3, and L5 levels) as seen from the ipsilateral side. Movement upward is denoted by arrow (?). In the three cats investigated, a systematic asymmetry occurred in these traces, which may be due to (say) differences of the stiffness of the hindlimb during the yield. Bottom trace shows the net angular displacements formed by 3 diodes as viewed in the sagittal plane (see inset), with minimum and maximum values corresponding to flexion and extension, respectively. F) Peak to peak displacements in sagittal plane (L3 level) us. step cycle duration. The straight lines for the Mf and VL onsets ("---" and "--", respectively, in B) a s well as the horizontal and sagittal displacements (in D and F) were constructed using the grouping method (Bartlett 1949) with 3 groups (slope=k).
The movements in the spine will be a consequence of the amount of internal as well as external forces acting on the trunk. To estimate the intrinsic movements of the spine in the horizontal plane, the diode positions were compared with one another, and if the angle between LSL3-Th9 is plotted (see lowermost curve in Fig. 1 C), it turns out that the lateral bending lies in the range of 10-15". However, the movements of the entire spine (Fig. 1 C), i.e. the simultaneous movements of the three back markers, are more marked. The lateral movements decrease from about 40 mm to about 10 mm as cycle duration
TRUNK CONTROL IN THE WALKING CAT
253
decreases (Fig. 1 D). The body moves over to the side of the supporting hindlimb and reaches the extreme lateral position at the end of the support phase. The trunk is thus swaying from side to side with an amplitude that is maximal at low speeds. Apparently, these movements are important to the equilibrium control of the animal and where most probably induced by limb action. In the sagittal plane, the intrinsic movements of the spine, i.e. flexions and extensions, are small, while the entire spine moves up and down about 20 mm during each step cycle (Fig. 1 E). These displacements are of about the same amplitude throughout a wide range of cycle durations (Fig. 1 F). The EMG and movement data presented above suggest that the primary role of the back muscles during walking is to control the stiffness of the back, rather than to induce movements. This work was supported by the Swedish Medical Research Council (Project nr. 3026), and the Swedish Defense Research Organization (Project nr. H657), and funds from Karolinska Institutet. M . Z. holds a postdoctoral exchange fellowship from the Swedish Medical Research Council. J. H. is supported, in part, by the Delft University of Technology, the Netherlands. The authors would like to thank Dr. Sten Grillner for his help in the preparation of this manuscript.
References BARTLETT, M. S., Fitting a straight line when both variables are subject to error. Biornerrics 1949. 5. 297-212. CARLSON, H., Morphology and contraction properties of cat lumbar back muscles. Acta physiol. scand. 1978 a. 103. 18&197. CARLSON, H., Histochemical fiber composition of lumbar back muscles in the cat. Acta physiol. scand. 1978 b. 103. 198-209. GRILLNER, S . , Locomotion in vertebrates-central mechanisms and reflex interaction. Physiol. Rev. 1975.55. 247-304. PHILIPPSON, M., L'autonomie et la centralisation dans le systeme nerveux des animaux. Trau. Lab. Physiol. Insr. Soluay, Bruxelles 1905. 7. 1-208. ZOMLEFER, M. R., F. E. ZAIAC,and W. S. LEVINE,Kinematics and muscular activity of cats during maximal height jumps. Brain Res. 1977. 126: 3. 563-566.
Control of the trunk during walking in the cat BY HANS CARLSON, ~ J O N THALBERTSMA and 'MICHAELZOMLEFER
While there is a great deal of information concerning the electromyographic (EMG) patterns and movements of the hindlimb in tetrapod locomotion (Grillner 1973, there is little knowledge about the control of the trunk. Recent experiments performed on the cat's lumbar back muscles have shown large portions, i.e. M. longissimus and iliocostalis, to be fast contracting and easily fatiguable, while the multifidi contract somewhat more slowly (Carlson 1978 a, b). The aim of this study has been to explore patterns of activity in the different lumbar back muscles during fast and slow walks and relate them to the trunk movements. Eleven experiments were performed on cats (n - 3 : 2.2, 2.3 and 3.2 kg), which were trained to walk on a moving treadmill or overground at cycle durations ranging from about 350 to 1 200 nis, corresponding to speeds ranging from 1.O to 0.2 m/s, respectively. Bipolar, intramuscular electrodes were chronically implanted (Zomlefer et af. 1977) into the multifidi (Mf), longissimus (Lo) and iliocostalis muscles at various levels along the lumbar spine (Ll-L6), as well as into both vasti lateralii (VL). The EMG wires were led percutaneously to a plug on the animal's back, which could be connected with a detachable cable to amplifiers. Electrode placement was verified post mortem. The movements of one hindlimb and the lower spine were recorded using a Selspot System (Selcom Co., Partille, Sweden). Small light emitting diodes were glued onto the shaved skin over the spinal processes at Th9, L3, and L5 as well as the iliac crest and the hip, knee, ankle metatarsophalangeal joints. Two cameras sampled each diode position at 160 Hz in both the sagittal and horizontal planes. Position and electromyographic data were fed online to a minicomputer (Hewlett-Packard 21 MX) for later processing. The EMG activity in both the medially located multifidi muscles and the lateral longissimus and iliocostalis displayed two distinct large bursts during each step cycle (see Fig. 1 A). The two bursts had similar durations and were synchronous in the different muscles, while each burst was tightly linked to the onset of the ipsi-and the contralateral VL activity (Fig. 1 B). The duration of the bursts increased nearly threefold (from about 150 to 400 ms) whereas the amplitude (mean value of each burst per unit time) decreased by a factor of four as cycle duration increased over the range studied. There will thus be two periods of activity in the lumbar back muscles during each step cycle. These bursts will coincide with the periods of overlapping EMG activity in the limb extensor muscles of the two sides, and thus they occur during the phases of double hindlimb support. 25 1
252
HANS CARLSON,
JONT
HALBERTSMA AND MICHAEL ZOMLEFER
1
ONSET(8) OF MUSCLE ACTIVITY IN RELATION TO IPS1 TOUCHDOWN.
130'
1
. . .. #-
I70' s
---L.--? aI
VL(k=0014)
aiMfL4Ist(k=-0040)
co VL i MfL4
-
i LoL4 Tr
HORIZONTAL Th9 ipsi L 3 L5 Th9 L3 L 5
-.. . \
L
L
co VL(k= - 0 4 4 0 ) ~1MfL42nd(k=-0580)
.5
1.0CYCLE DUR(8)
50 HORIZONTAL DISPLACEMENT OF. L 3 (mm)
(k=37mm/s)
+-iY-
E SAGITTAL Th 9 L5 Th9 L3 L5
SAGITTAL DISPLACEMENT OF L3 (mm)
*. .*
.
(k=-5mm.X
-v
Fig. I. A) Ankle angle (ANKLE) with rectified and filtered EMG's from ipsi- and contralateral VL, a s well as the ipsilateral Mf and Lo muscles a t the L 4 level (iVL, COVL,iMfL4 and iLoL4, respectively). Step cycle labeling, shown for the ipsilateral hindlimb, is the same as that used by Philippson (1905). B) Onset of EMG activity (relative to ipsilateral hindlimb touchdown) us. cycle duration (CYCLE DUR) for iVL, COVL, and the first and second bursts of iMfL4 (iMfL4lst and iMfL42nd). A positive value(+) indicates that the onset time is prior to ipsi-hindlimb touchdown. The time for onset of COVLwill increase with increasing cycle duration, since both hindlimbs are alternating in a given step cycle. C ) Horizontal plane displacements and angle. The three uppermost curves show the relative trajectories of the marker diodes at the Th9, L3, and L5 levels. Movement toward the ipsilateral side (see A) is defined by arrow (t).The fourth trace shows the net angular displacement determined by L5-L3-Th9 (see inset). Minimum value corresponds to lateral bending with concavity toward the ipsilateral side. D) Peak to peak displacements in horizontal plane (L3 level) vs. step cycle duration. E) Sagittal displacements and angle. The first three traces indicate the movements of the three back diodes (Th9, L3, and L5 levels) as seen from the ipsilateral side. Movement upward is denoted by arrow (?). In the three cats investigated, a systematic asymmetry occurred in these traces, which may be due to (say) differences of the stiffness of the hindlimb during the yield. Bottom trace shows the net angular displacements formed by 3 diodes as viewed in the sagittal plane (see inset), with minimum and maximum values corresponding to flexion and extension, respectively. F) Peak to peak displacements in sagittal plane (L3 level) us. step cycle duration. The straight lines for the Mf and VL onsets ("---" and "--", respectively, in B) a s well as the horizontal and sagittal displacements (in D and F) were constructed using the grouping method (Bartlett 1949) with 3 groups (slope=k).
The movements in the spine will be a consequence of the amount of internal as well as external forces acting on the trunk. To estimate the intrinsic movements of the spine in the horizontal plane, the diode positions were compared with one another, and if the angle between LSL3-Th9 is plotted (see lowermost curve in Fig. 1 C), it turns out that the lateral bending lies in the range of 10-15". However, the movements of the entire spine (Fig. 1 C), i.e. the simultaneous movements of the three back markers, are more marked. The lateral movements decrease from about 40 mm to about 10 mm as cycle duration
TRUNK CONTROL IN THE WALKING CAT
253
decreases (Fig. 1 D). The body moves over to the side of the supporting hindlimb and reaches the extreme lateral position at the end of the support phase. The trunk is thus swaying from side to side with an amplitude that is maximal at low speeds. Apparently, these movements are important to the equilibrium control of the animal and where most probably induced by limb action. In the sagittal plane, the intrinsic movements of the spine, i.e. flexions and extensions, are small, while the entire spine moves up and down about 20 mm during each step cycle (Fig. 1 E). These displacements are of about the same amplitude throughout a wide range of cycle durations (Fig. 1 F). The EMG and movement data presented above suggest that the primary role of the back muscles during walking is to control the stiffness of the back, rather than to induce movements. This work was supported by the Swedish Medical Research Council (Project nr. 3026), and the Swedish Defense Research Organization (Project nr. H657), and funds from Karolinska Institutet. M . Z. holds a postdoctoral exchange fellowship from the Swedish Medical Research Council. J. H. is supported, in part, by the Delft University of Technology, the Netherlands. The authors would like to thank Dr. Sten Grillner for his help in the preparation of this manuscript.
References BARTLETT, M. S., Fitting a straight line when both variables are subject to error. Biornerrics 1949. 5. 297-212. CARLSON, H., Morphology and contraction properties of cat lumbar back muscles. Acta physiol. scand. 1978 a. 103. 18&197. CARLSON, H., Histochemical fiber composition of lumbar back muscles in the cat. Acta physiol. scand. 1978 b. 103. 198-209. GRILLNER, S . , Locomotion in vertebrates-central mechanisms and reflex interaction. Physiol. Rev. 1975.55. 247-304. PHILIPPSON, M., L'autonomie et la centralisation dans le systeme nerveux des animaux. Trau. Lab. Physiol. Insr. Soluay, Bruxelles 1905. 7. 1-208. ZOMLEFER, M. R., F. E. ZAIAC,and W. S. LEVINE,Kinematics and muscular activity of cats during maximal height jumps. Brain Res. 1977. 126: 3. 563-566.
