- Email: [email protected]
Is there a peripheral control of the central pattern generators for swimming in dogfish?
Brain Research, 127 (1977) 291-295
291
© Elsevier/North-Holland Biomedical Press
Is there a peripheral control of the central pattern generators for swimming in dogfish?
STEN GRILLNER and PETER WALLI~N The Department of Physiology, GIH, Stockholm and Kristineberg's Zoological Station, Fiskebiickskil (Sweden)
(Accepted February 10th, 1977)
A variety of experiments in vertebrates 1,5,7-1° and in invertebrates16, ~7 have shown that the locomotor movements are controlled by central pattern generators. Without signals providing information about peripheral events, spinal interneuronal networks can produce the appropriate motor output pattern both in cat 8 and in dogfish 7. These pattern generators can thus operate without peripheral feedback. Such experiments give, however, no information regarding how feedback signals are used when present. Our experiments were designed to test if they can act on the generator network. Spiny dogfish show after a spinal transection (3rd-6th segment) spontaneous and well-coordinated swimming movements3,4, ~2,~a. Rhythmic efferent burst activity can be recorded in different ventral roots along the body, even after the animal has been completely immobilized by an intravenous injection of curare 7. Under these conditions the central network produces without any feedback a 'normal' rhythmic motor output with a maintained intersegmental coordination. The experimenter can then superimpose a rhythmic movement on the body resembling swimming, which may be of quite a different frequency from that of the rhythmic motor output, i.e. a mismatch between the central command and the actual movement can be induced. Spiny dogfish (n ~-- 15) were spinalized (3rd-6th segment) and curarized (for methods, see ref. 7) and two or three pairs of ventral roots 10-25 segments apart were dissected with a dorsal approach. The general condition of the preparation was checked by recording the heart rate (ECG) 7. To maintain hydrostatic conditions as close to normal as possible, the body of the fish was immersed in water except for the most dorsal part in which a longitudinal incision was made to dissect the ventral roots. The body was fixed with 3 or 4 clamps around the 'vertebral' column (see Fig. 1 left). The spinal cord with longitudinal nerve bundles was also transected just rostral to the tail fin. This completely 'denervated' tail fin could be used as a handle through which movements could be induced in the caudal 'innervated' part of the body (see Fig. 1). By bending the tail fin and thereby the body back and forth at different frequencies, the effect on the efferent discharge in different ventral roots could be studied (bipolar conventional recording with Ag-AgC1 electrodes). Fig. 1 shows alternating activity in
292
rVR4J
Fig. 1. Ventral root recordings (left, 1. VR no 41 ; right, r. VR no 41) from a curarized spinal dogfish with and without a superimposed movement of the caudal third of the body (compare drawing). Movements to the left (1) (position of the tail fin) is upwards in this trace. Note that frequency increases gradually from zero to a high rate and then back to zero again. Time calibration as indicated. In the drawing on the left, the upper and lower spinalizations are indicated by bars. Two clamps (usually 3 or 4 were used) are indicated as well as the ventral roots. a pair of ventral roots under resting conditions. W h e n the tail fin is moved passively (see movement trace) the duration of the bursts shortens corresponding to the cycle duration o f the imposed movement. The efferent activity clearly follows the imposed movement within a large frequency range. Fig. 2 shows that the activity does not only follow a movement at higher rate than the basic rhythm, but also slower movements. Afferent signals can thus delay and prolong the bursts to match the imposed movement. The graph in Fig. 3 shows a close correlation with cycle durations both higher and lower than the resting level. This dependence on peripheral signals was demonstrated in all preparations in which spontaneous rhythmic activity occurred (n ---- 9). The preparations followed rates up to 1 Hz or somewhat more, but then the rhythmic activity usually ceased. Sometimes a transitional state would occur with activity only on one side (Fig. 1). F r o m the 'filtered' ventral root recordings in Fig. 2, it is clear that with an increased burst rate, the amplitude of the m o t o r output increases. Also during 'intact' swimming there is a recruitment of new m o t o r units with increasing speed (i.e. higher
293
7 Z~S
|
4 8
t 31-
......
"!
fur
.....
~ ~
r 4 8 - flit. i 48-fill
~
'
L
"
"sLow(a"
,
,
,,
i tl
/ ............
'
'
-
Fig. 2. Recordings from three ventral roots (r. V R no 31, r. V R no 48, 1.48). Preparation as in Fig. 1. The rectified and filtered version of the recordings, at respective ventral roots, are shown below. Movements at higher and lower rates than 'resting' are shown. Note that left is downwards in the movement traces. Time calibration as indicated. Movement calibration equals a lateral displacement of 10 cm at the tip of the tail fin.
294 9-
/
/
A8-
/ /
/
/
/.
/.
///
"-~ 6.
/ •
/. / 0
E 4
.t •
0 r-,
/
//
\y=x
/
2
7
4/
//
z ' 3
.
E
~z / // /
resting o activity - 0
,
efferent rhythm,interval (s) Fig. 3. The duration of each cycle of movement is plotted versus the duration of the corresponding efferent cycle (i.e. from onset of one burst of activity to onset of the subsequent burst). The spontano~us resting level is indicated along the abscissa as zero movement.
burst rate) and probably also a frequency modulation of the motor units (cf. ref. 6). This shows that the movement signal does not only shorten or prolong the resting level motor output (in that case the amplitude should have been unchanged). It rather suggests that the motor output amplitude is appropriate for that particular burst rate (speed), at least it changes qualitatively in the same direction. The superimposed movement modifies the activity over the entire spinal cord. The coordination between the different segments can remain unchanged i.e. a 'wave' is propagated down the body with a constant phase coupling 4. The segment in which the activity starts, the leading segment, is normally located in the rostral third of the fish. Under the present conditions it may also be located in the middle or the caudal part4, 7. This results in a reversed direction of the propagating 'wave' (backwards swimming). In that case the superposition of a movement in the caudal part of the body will often cause the leading segment to be located more rostrally. The imposed movement was limited to the caudal third of the body (i.e. caudal to the clamp). Driving of the efferent activity occurred with movement amplitudes in a range from those encountered during ordinary swimming to movements of only a few millimeters, in a dogfish of 0.75 m. The input is thus very powerful. It should be noted that when the tail is moved e.g. to the left the burst occurs on the left side. This is similar to intact swimming when an active contraction on the left side rather than the experimenter causes the movement to the left. Our study gives as such no information regarding what type of receptor is responsible. One likely candidate is, however, a subcutaneous stretch receptor described by Roberts 14 that would provide an
295
appropriate feedback signal. It is noteworthy that no intramuscular stretch receptor has been described in the dogfish. During natural conditions the speed of swimming (frequency) can be set by a descending control upon the pattern generators 6,7,11. These can be driven within the norma I frequency range - - with maintained intersegmental coordination - - without any phasic afferent signals. During the swimming movements, however, afferent feedback signals will continuously supply the spinal cord with information about the ongoing movement. These signals are clearly potent enough to modify the motor output significantly. It is possible that these signals are not used as long as the movement proceeds according to the central plan, but whenever the movements are slowed down or speeded up due to external events, the reflex input can instantaneously act to modify the central motor command itself (cf. ref. 5). A similar type of control has been implied also in the cat hind limb from receptors influenced by the hip positionS, 15.
1 Brown, T. G., The intrinsic factors in the act of progression in the mammal, Proc. roy. Soc. B, 84 (1911) 308-319. 2 Edgerton, V. R., Grillner, S., SjrstrSm, A. and Zangger, P., Central generation of locomotion in vertebrates. In R. Herman, S. Grillner, P. Stein and D. Stuart (Eds.), Neural Control of Locomotion, Plenum Press, New York, 1976, pp. 439-464. 3 Gray, J. and Sand, A., The locomotory rhythm of the dogfish (Scyllium canicula), J. exp. BioL, 13 (1936) 200-209. 4 Grillner, S., On the generation of locomotion in the spinal dogfish, Exp. Brain Res., 20 (1974) 459470. 5 Grillner, S., Locomotion in vertebrates - - central mechanisms and reflex interaction, PhysioL Rev., 55 (1975) 247-304. 6 Grillner, S. and Kashin, S., On the generation and performance of swimming in fish. In R. Herman, S. Grillner, P. Stein and D. Stuart (Eds.), Neural Control of Locomotion, Plenum Press, New York, 1976, pp. 181-201. 7 Grillner, S., Perret, C. and Zangger, P., Central generation of locomotion in the spinal dogfish, Brain Research, 109 (1976) 255-269. 8 Grillner, S. and Zangger, P., How detailed is the central pattern generator for locomotion? Brain Research, 88 (1975) 367-371. 9 Hoist, E. von, Erregungsbildung und Erregungsleitung im Fischrtickenmark, Pfliigers Arch. ges. PhysioL, 235 (1935) 345-359. 10 Holst, E. von, Die relative Koordination, Ergebn. Physiol., 42 (1939) 228-306. 11 Kashin, S., Feldman, A. G. and Orlovsky, G. N., Locomotion of fish evoked by electrical stimulation of the brain, Brain Research, 82 (1974) 41-47. 12 Lemare, D. W., Reflex and rhythmical movements in the dogfish, J. exp. BioL, 13 (1936) 429-442. 13 Lissmann, H. W., The neurological basis of the locomotory rhythm in the spinal dogfish (Scyllium canicula, dcanthias vulgaris), I. Reflex behaviour, J. exp. BioL, 23 (1946) 143-161. 14 Roberts, B. L., The response of a proprioceptor to the undulatory movements of dogfish, J. exp. BioL, 51 (1969) 775-785. 15 Rossignol, S., Grillner, S. and Forssberg, H., Factors of importance for the initiation of flexion during walking, Neurosci. Abstr., 1 (1975) 181. 16 Selverston, A. 1., Neuronal mechanisms for rhythmic motor pattern generation in a simple system. In R. Herman, S. Grillner, P. Stein and D. Stuart (Eds.), Neural Control of Locomotion, Plenum Press, New York, 1976, pp. 377-399. 17 Wilson, D. M., The origin of the flight-motor command in grasshoppers. In R. F. Reiss (Ed.), Neuronal Theory and Modeling, Stanford University Press, Stanford, Calif., 1964, pp. 331-345.
291
© Elsevier/North-Holland Biomedical Press
Is there a peripheral control of the central pattern generators for swimming in dogfish?
STEN GRILLNER and PETER WALLI~N The Department of Physiology, GIH, Stockholm and Kristineberg's Zoological Station, Fiskebiickskil (Sweden)
(Accepted February 10th, 1977)
A variety of experiments in vertebrates 1,5,7-1° and in invertebrates16, ~7 have shown that the locomotor movements are controlled by central pattern generators. Without signals providing information about peripheral events, spinal interneuronal networks can produce the appropriate motor output pattern both in cat 8 and in dogfish 7. These pattern generators can thus operate without peripheral feedback. Such experiments give, however, no information regarding how feedback signals are used when present. Our experiments were designed to test if they can act on the generator network. Spiny dogfish show after a spinal transection (3rd-6th segment) spontaneous and well-coordinated swimming movements3,4, ~2,~a. Rhythmic efferent burst activity can be recorded in different ventral roots along the body, even after the animal has been completely immobilized by an intravenous injection of curare 7. Under these conditions the central network produces without any feedback a 'normal' rhythmic motor output with a maintained intersegmental coordination. The experimenter can then superimpose a rhythmic movement on the body resembling swimming, which may be of quite a different frequency from that of the rhythmic motor output, i.e. a mismatch between the central command and the actual movement can be induced. Spiny dogfish (n ~-- 15) were spinalized (3rd-6th segment) and curarized (for methods, see ref. 7) and two or three pairs of ventral roots 10-25 segments apart were dissected with a dorsal approach. The general condition of the preparation was checked by recording the heart rate (ECG) 7. To maintain hydrostatic conditions as close to normal as possible, the body of the fish was immersed in water except for the most dorsal part in which a longitudinal incision was made to dissect the ventral roots. The body was fixed with 3 or 4 clamps around the 'vertebral' column (see Fig. 1 left). The spinal cord with longitudinal nerve bundles was also transected just rostral to the tail fin. This completely 'denervated' tail fin could be used as a handle through which movements could be induced in the caudal 'innervated' part of the body (see Fig. 1). By bending the tail fin and thereby the body back and forth at different frequencies, the effect on the efferent discharge in different ventral roots could be studied (bipolar conventional recording with Ag-AgC1 electrodes). Fig. 1 shows alternating activity in
292
rVR4J
Fig. 1. Ventral root recordings (left, 1. VR no 41 ; right, r. VR no 41) from a curarized spinal dogfish with and without a superimposed movement of the caudal third of the body (compare drawing). Movements to the left (1) (position of the tail fin) is upwards in this trace. Note that frequency increases gradually from zero to a high rate and then back to zero again. Time calibration as indicated. In the drawing on the left, the upper and lower spinalizations are indicated by bars. Two clamps (usually 3 or 4 were used) are indicated as well as the ventral roots. a pair of ventral roots under resting conditions. W h e n the tail fin is moved passively (see movement trace) the duration of the bursts shortens corresponding to the cycle duration o f the imposed movement. The efferent activity clearly follows the imposed movement within a large frequency range. Fig. 2 shows that the activity does not only follow a movement at higher rate than the basic rhythm, but also slower movements. Afferent signals can thus delay and prolong the bursts to match the imposed movement. The graph in Fig. 3 shows a close correlation with cycle durations both higher and lower than the resting level. This dependence on peripheral signals was demonstrated in all preparations in which spontaneous rhythmic activity occurred (n ---- 9). The preparations followed rates up to 1 Hz or somewhat more, but then the rhythmic activity usually ceased. Sometimes a transitional state would occur with activity only on one side (Fig. 1). F r o m the 'filtered' ventral root recordings in Fig. 2, it is clear that with an increased burst rate, the amplitude of the m o t o r output increases. Also during 'intact' swimming there is a recruitment of new m o t o r units with increasing speed (i.e. higher
293
7 Z~S
|
4 8
t 31-
......
"!
fur
.....
~ ~
r 4 8 - flit. i 48-fill
~
'
L
"
"sLow(a"
,
,
,,
i tl
/ ............
'
'
-
Fig. 2. Recordings from three ventral roots (r. V R no 31, r. V R no 48, 1.48). Preparation as in Fig. 1. The rectified and filtered version of the recordings, at respective ventral roots, are shown below. Movements at higher and lower rates than 'resting' are shown. Note that left is downwards in the movement traces. Time calibration as indicated. Movement calibration equals a lateral displacement of 10 cm at the tip of the tail fin.
294 9-
/
/
A8-
/ /
/
/
/.
/.
///
"-~ 6.
/ •
/. / 0
E 4
.t •
0 r-,
/
//
\y=x
/
2
7
4/
//
z ' 3
.
E
~z / // /
resting o activity - 0
,
efferent rhythm,interval (s) Fig. 3. The duration of each cycle of movement is plotted versus the duration of the corresponding efferent cycle (i.e. from onset of one burst of activity to onset of the subsequent burst). The spontano~us resting level is indicated along the abscissa as zero movement.
burst rate) and probably also a frequency modulation of the motor units (cf. ref. 6). This shows that the movement signal does not only shorten or prolong the resting level motor output (in that case the amplitude should have been unchanged). It rather suggests that the motor output amplitude is appropriate for that particular burst rate (speed), at least it changes qualitatively in the same direction. The superimposed movement modifies the activity over the entire spinal cord. The coordination between the different segments can remain unchanged i.e. a 'wave' is propagated down the body with a constant phase coupling 4. The segment in which the activity starts, the leading segment, is normally located in the rostral third of the fish. Under the present conditions it may also be located in the middle or the caudal part4, 7. This results in a reversed direction of the propagating 'wave' (backwards swimming). In that case the superposition of a movement in the caudal part of the body will often cause the leading segment to be located more rostrally. The imposed movement was limited to the caudal third of the body (i.e. caudal to the clamp). Driving of the efferent activity occurred with movement amplitudes in a range from those encountered during ordinary swimming to movements of only a few millimeters, in a dogfish of 0.75 m. The input is thus very powerful. It should be noted that when the tail is moved e.g. to the left the burst occurs on the left side. This is similar to intact swimming when an active contraction on the left side rather than the experimenter causes the movement to the left. Our study gives as such no information regarding what type of receptor is responsible. One likely candidate is, however, a subcutaneous stretch receptor described by Roberts 14 that would provide an
295
appropriate feedback signal. It is noteworthy that no intramuscular stretch receptor has been described in the dogfish. During natural conditions the speed of swimming (frequency) can be set by a descending control upon the pattern generators 6,7,11. These can be driven within the norma I frequency range - - with maintained intersegmental coordination - - without any phasic afferent signals. During the swimming movements, however, afferent feedback signals will continuously supply the spinal cord with information about the ongoing movement. These signals are clearly potent enough to modify the motor output significantly. It is possible that these signals are not used as long as the movement proceeds according to the central plan, but whenever the movements are slowed down or speeded up due to external events, the reflex input can instantaneously act to modify the central motor command itself (cf. ref. 5). A similar type of control has been implied also in the cat hind limb from receptors influenced by the hip positionS, 15.
1 Brown, T. G., The intrinsic factors in the act of progression in the mammal, Proc. roy. Soc. B, 84 (1911) 308-319. 2 Edgerton, V. R., Grillner, S., SjrstrSm, A. and Zangger, P., Central generation of locomotion in vertebrates. In R. Herman, S. Grillner, P. Stein and D. Stuart (Eds.), Neural Control of Locomotion, Plenum Press, New York, 1976, pp. 439-464. 3 Gray, J. and Sand, A., The locomotory rhythm of the dogfish (Scyllium canicula), J. exp. BioL, 13 (1936) 200-209. 4 Grillner, S., On the generation of locomotion in the spinal dogfish, Exp. Brain Res., 20 (1974) 459470. 5 Grillner, S., Locomotion in vertebrates - - central mechanisms and reflex interaction, PhysioL Rev., 55 (1975) 247-304. 6 Grillner, S. and Kashin, S., On the generation and performance of swimming in fish. In R. Herman, S. Grillner, P. Stein and D. Stuart (Eds.), Neural Control of Locomotion, Plenum Press, New York, 1976, pp. 181-201. 7 Grillner, S., Perret, C. and Zangger, P., Central generation of locomotion in the spinal dogfish, Brain Research, 109 (1976) 255-269. 8 Grillner, S. and Zangger, P., How detailed is the central pattern generator for locomotion? Brain Research, 88 (1975) 367-371. 9 Hoist, E. von, Erregungsbildung und Erregungsleitung im Fischrtickenmark, Pfliigers Arch. ges. PhysioL, 235 (1935) 345-359. 10 Holst, E. von, Die relative Koordination, Ergebn. Physiol., 42 (1939) 228-306. 11 Kashin, S., Feldman, A. G. and Orlovsky, G. N., Locomotion of fish evoked by electrical stimulation of the brain, Brain Research, 82 (1974) 41-47. 12 Lemare, D. W., Reflex and rhythmical movements in the dogfish, J. exp. BioL, 13 (1936) 429-442. 13 Lissmann, H. W., The neurological basis of the locomotory rhythm in the spinal dogfish (Scyllium canicula, dcanthias vulgaris), I. Reflex behaviour, J. exp. BioL, 23 (1946) 143-161. 14 Roberts, B. L., The response of a proprioceptor to the undulatory movements of dogfish, J. exp. BioL, 51 (1969) 775-785. 15 Rossignol, S., Grillner, S. and Forssberg, H., Factors of importance for the initiation of flexion during walking, Neurosci. Abstr., 1 (1975) 181. 16 Selverston, A. 1., Neuronal mechanisms for rhythmic motor pattern generation in a simple system. In R. Herman, S. Grillner, P. Stein and D. Stuart (Eds.), Neural Control of Locomotion, Plenum Press, New York, 1976, pp. 377-399. 17 Wilson, D. M., The origin of the flight-motor command in grasshoppers. In R. F. Reiss (Ed.), Neuronal Theory and Modeling, Stanford University Press, Stanford, Calif., 1964, pp. 331-345.