Experimental Brain Research

Exp. Brain Res. 37, 265-281 (1979)

@ Springer-VerIag 1979

The Placing Reaction in the Standing Cat: A Model for the Study of Posture and Movement M. Coulmance, Y. Gah6ry, J. Massion, and J.E. Swett 1 D6partement de Neurophysiologiegdn6rale, C.N.R.S., INP, 31, chemin Joseph Aiguier, F-13274 Marseille Cedex 2, France

Summary. By measuring the forces applied by each limb supporting the weight of the standing quadruped (cat), before and during elicitation of the placing reaction, it was possible to examine quantitatively and qualitatively the postural events which preceded and accompanied forelimb displacement. The findings are summarized as follows: 1. Postural adjustment consists of a shift from quadrupedal stance to a tripodal stance to permit withdrawal of weight from one forelimb without loss of equilibrium. The animal's weight is not equally distributed between the three supporting limbs but the majority of the weight is supported by the diagonally opposing limb pair. 2. During the isometric phase of the placing reaction, the animal's projected center of gravity moves contralaterally, across the diagonal line between the contralateral forepaw and the ipsilateral hindpaw, and comes to rest within the triangular zone outlined by the three supporting limbs. 3. The diagonal supporting stance is a maneuver of an anticipatory nature which precedes and accompanies the placing reaction. 4. The force changes exhibited by each limb to bring the animal to the stereotyped diagonal supporting stance illustrated that the way to achieve this is consistent within a given animal, but differs from one animal to another. The pattern in the same animal is generally symmetrical when lifting the right or left forepaw. 5. The data from the cat are compared to observations in other quadrupeds and man. Key words: Posture - Movement - Placing reaction Living organisms are perpetually subject to the force of gravity. One of the functions that the motor system serves for the organism is that of counteracting this force, whether the animal is stationary and immobile, or performing a movement. 1 Present address: Department of Anatomy, University of California, Irvine 92717, USA Dr. J. Massion (address see above)

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Postural tonus is the principal means by which the neuromuscular system compensates for the influence of gravitational force and allows standing. Its distribution among the muscles is regulated with great precision by neurophysiological mechanisms to maintain the animal's center of gravity within limits compatible with equilibrium. When an animal performs a movement there is always an associated postural reaction as has been demonstrated in the quadruped by the studies of Brookhart et al. (1965), Ioffe and Andreyev (1969), and Anokhin (1974). This postural adjustment has two fundamental purposes. First, it permits displacement of a limb that was previously supporting a portion of the animal's weight. Then, it compensates the disequilibrium engendered by each movement of the body or its parts. The same principles have been shown to apply to the bipedal human by Belenkiy et al. (1967), Martin (1967), Gurfinkel and Ebner (1973) and Alexeiev and Naidel (1973). The objective of the experiments described in the following pages was to examine the linkage between movement, such as limb displacement, and the postural adjustment which must be associated with it. For this purpose, the standing quadruped is a particularly good preparation because the animal's weight is approximately distributed on four thrust points, the limbs, and every limb movement is necessarily accompanied by a redistribution of weight on three other limbs by way of a postural adjustment. By measuring the weight of each limb, and its changes under various experimental conditions, one can infer what postural changes are taking place. In previous studies (Massion and Smith, 1973; Regis et al., 1976; Smith et al., 1978) we chose to use the contact placing reaction in a standing quadruped, the cat, as the model in which to examine the events associated with postural adjustments and limb displacement. In the previous experiments a hammock was used to restrain the animal; however, this method permitted only qualitatively evaluation of these events. Later, the method of restraining the animals was improved (Haour et al., 1976) so that it became possible to describe in quantitative terms the events associated with movement and posture, the animal's weight being entirely supported by its limbs. This paper will give a description of the biomechanical and electromyographic events which accompany the placing reaction in the standing cat. Changes observed after motor cortical ablation will be reported in a paper in preparation. Methods T h e experiments were carried out on six cats. Each animal was initially trained for 2 - 3 weeks to stand quietly with its weight distributed on all four limbs. Each paw rested on a platform monitored by strain gauges designed to linearly m e a s u r e vertical forces between 0.0 to 2.0 kg (see H a o u r et al., 1976). Three of the animals were held in position over the strain gauge platforms by a harness attached to a vertical sliding rod to restrict horizontal displacement of the animal's shoulder in the antero-posterior and lateral directions without significantly disturbing the natural motions of the animal within predetermined limits. Three animals were tested without the restraining device. The training of five of the six animals was m a d e empirically. The animal received food reinforcement when it stood quietly for 2 s without moving the limbs. However, the force recordings

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from the plates supporting the limbs revealed in many cases that changes of force took place during the apparent immobility of the cat. This necessitated rejection of many trials in which the baseline of force was too variable (see later). During the trials in which the placing reaction was introduced, reinforcement for correct placing was added. Later, for cat ELS, we used an automated training procedure under on-line computer control. The computer calculated the resultant of the forces from the four platforms and delivered milk reward when two conditions were met during a fixed time (usually 2 s): (1) the force exerted on each plate had to be equal to one quarter of the animal's weight + 50%; (2) a speed of displacement of the resultant of the forces (projection of center of gravity) inferior to 20 mm/s. This second procedure yielded a larger proportion of successful trials. The placing reaction was performed in the following way. Two mobile plates, hidden from view of the animal, could be released independently by a remote manual switch. They moved to make physical contact with the anterior surface of the left or right forepaw of the animal. When contact was made the animal lifted the stimulated paw and replaced it on the top of the mobile plate which subsequently entirely covered the platform on which the cat's paw had previously rested. Strain gauges mounted on the leading edges of these mobile plates produced an electrical signal when a contact force attained 20 g between the edge of the plate and the stationary paw. In the course of each testing session a total of 20~40 mechanical stimuli were randomly presented to the right and left forepaws. The electrical and mechanical properties of the strain gauge platforms and the recording system allowed changes in force as small as 20 g to be resolved; its dynamic characteristics permitted resolution of rate of change of force to values slightly above 30 g/ms. The force variations detected by the 4 platforms were permanently recorded by an ink pen E E G apparatus (ALVAR). They were processed by an analog to digital converter and PDP 11/40 computer (Digital Equipment Corporation). The data from each trial were stored in the computer memory from the moment of contact of the mobile plate with one of the forepaws until 1.0 s after application of this mechanical stimulus. The computer sampled and stored the vertical forces generated by each of the animal's limbs at 4 ms intervals and displayed on a graphic terminal a schematic diagram representing the approximate position of the projection of the center of gravity of the animal during any desired 4 ms period. It should be stressed that the animal's true center of gravity is a constantly shifting point in the space above the strain gauge platforms. In fact, the computer calculated the position of the projection of the center of gravity, by determining the resultant of the vertical forces exerted at the level of each platform supporting the limbs. The position so calculated can only be considered as an approximation. First, this calculation is only valid under static conditions, and is undefinite to some extent during dynamic conditions such as the placing reaction. Second, the calculation has not taken into account the precise location of the limbs on the trays, which is another source of imprecision. The terms, "projected center of gravity" or "center of gravity", are used in the text to convey only its approximate location as projected on a two-dimensional surface. Not all trials were kept for analysis of the results. The following criteria determined which trials would be selected and pooled for analysis: (1) a stable posture was required for 2 s preceeding the placing reaction as judged by visually monitoring the DC output of the platforms on an oscilloscope or polygraph recorder. (2) Some uniformity of standing position was sought so that forces on the plates would fall within specified limits at the moment of the stimulation. Ideally, the force generated by each paw would tend to be approximately equal to one fourth of the animal's weight at the moment of mechanical stimulation. The arbitrary limits beyond which data were rejected for analysis were (a) when 1/8, or less, of the animal's weight was placed on any limb, (b) when less than half of the animal's total weight, + 15 %, was present on the forepaws, and (c) when less than half of t h e animal's total weight, _+ 15%, was present on one side of the body. (3) Any trial, in which the placing reaction began at, or just before, the stimulus, was rejected. This occasionally occurred with anticipatory reactions of the animals. Tactile stimulation might have contributed to this because the moving plate touched the hair on the animal's limb before pressure on the skin reached the critical value of 20 g. Taking account of the speed of the moving plate (10 cm/s) and the length of the hairs (4-8 mm), the time elapsed between the hair stimulation and depression of the skin would be in the range of 40-80 ms. In some cases hair stimulation might have triggered the placing movement instead of direct pressure of the plate edge on the skin.

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Fig. 1. Distribution of the calculated Iocations of the centers of gravity in a grouped series of trials

from one animal (PNO). The arrow indicates mechanical stimulation of the left forepaw. The corners of the rectangles represent the position of the animal's paws on the strain-gauge platforms. Each dot represents the center of gravity observed during one trial and is plotted in relation to the scale which indicates the percentage of the animal's weight supported by the forelimbs. The diagram at the left shows that the centers of gravity at stimulus onset were scattered evenly around a relatively central location. The rectangle on the right shows the locations of the calculated centers of gravity at the instant the left (stimulated) forepaw was lifted from the platform. The projections for centers of gravity were found at this moment to be on the contralateral side within a triangular zone defined by the positions of three weight-bearing limbs. The regression line (striped line) calculated from the locations of projections of center of gravity was found significant (p < 0.05). Vertical scale: % of weight on forelimbs. Horizontal scale: 0 value represents equal distribution of weight on left and right limbs; - 5 0 % and + 5 0 % values represent animal's weight on the left and right legs, respectively

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C.G. DISPLACEMENT Fig. 2. Displacement of the center of gravity. The mean values of the projection of the center of gravity for each cat are represented by a different symbol of two sizes. The largest symbol which is the nearest to the midline, indicated by the dashed line (equal weight on the left and right sides), corresponds to the value of the resting position. The smaller symbols indicated the mean value of the projection of the center of gravity at the onset of the displacement of the moving limb. T h e symbols on the right correspond to left placing and those on the left to right placing. The horizontal scale expresses the % of weight shifted to the left or to the right. The vertical scale indicates the % of weight on the forelimbs. Note that the relative positions of "centers of gravity" during left and right placing tend to be symmetrically placed

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With strict adherence to these criteria, about 1/s of the trials were eliminated; 60 of 188 trials for cat NOI, 120 of 292 for PNO, 84 of 208 for N R D , 102 of 298 for R O U , and 106 of 247 trials for G R I were eliminated. The last animal, ELS, trained under computer control had a m u c h better score; only 40 of 240 trials were eliminated.

Results

Representation of the Center of Gravity in the Quietly Standing Cat Each limb of the animal supporting part of the animal's weight may be represented by a corner of a rectangle (Fig. 1). The computer compared the weight on the four platforms, calculated the "center of gravity" and plotted it as one point within a two dimensional image of the rectangle at selected times following the stimulus. The rectangle on the left in Fig. 1 shows the location of the projected center of gravity, as derived from pooled trials of one animal, at the instant of contact of the mobile plate with the left forepaw. This diagram shows that the "center of gravity" is located within a rather circumscribed region that is roughly equidistant from the four paws. The "center of gravity" of the quietly standing cat was measured at the onset of every trial when the mobile plate touched the paw and at 4 ms intervals thereafter for at least 1.0 s. Figure 2 shows summary values of the initial measurements of the centers of gravity obtained in the six animals. The projected center of gravity of the same animal tended to be consistent over time. The values between animals were quite variable. According to the computed means, animal NOI, for example, had 60 % of its weight on its forelimbs, whereas N R D had only 46 % of its weight on its forelimbs. Some animals tended to lean slightly to one side or the other so

270

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Fig. 3. Forces generated by each of the animal's limbs before and during the placing reaction on the left forepaw (cat NOI). The change in force for each limb is displayed in respect to time starting at the instant of mechanical contact of the mobile plate with the paw. This occurs at the intersection of the curve with the ordinate, scaled in kg. A small vertical cursor, which appears on all curves at a latency of about 250 ms, signifies the moment of paw lift-off for the stimulated forelimb. In this example, nearly 90 % of the animal's weight is supported by the diagonally opposed pair of limbs. As with most animals studied, the postural reaction in this case occurred first in the contralateral forelimb. The (+) sign indicates an increase in weight; (-) denotes decrease in weight

that lateral asymmetries appeared in the m e a n positions for the "center of gravity" measurements. The locations of the "center of gravity", as measured at the m o m e n t of contact of the mechanical stimulus, differed little with respect to the side stimulated. The stimulus itself did not contribute to this because measurements of the "center of gravity" during blind trials, in the absence of the stimulus, were comparable to those observed in the same animal at the m o m e n t that the actual stimuli were delivered.

The Placing Reaction Contact of the mobile platform with one of the forelimbs caused a reaction which can be conveniently divided into two phases, an isometric phase, and a displacement phase. The initial isometric phase is present until the vertical forces on the platform of the stimulated limb drop to zero. The displacement phase occurs during the time that the stimulated limb lifts off the strain gauge platform and comes to rest on the mobile plate. During the first phase, the

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Table 1. Influence of the resting position on the isometric phase. Right and left placing tests from the cat ELS were classified according to the resting positio n at the onset of stimulation. Two groups of trials were considered: one with a displacement of the "center of gravity" to the left equal or superior to 4 % of the animal's weight and the other with a displacement to the right equal or superior to 4 % of the weight. The initial weight on the moving limb as determined from the m e a n of all trials was 1016 • 137.5 g for the right forelimb. Note that the greater is the weight supported by the stimulated forelimb, the longer is the duration of the isometric phase Duration of isometric phase

Initial force on the moving limb

(ms)

(g)

Left _< - 4 n = 15

278.9 _+32.4

1 217 _+119

Right ~ + 4 n = 23

244.5 +39.4

953 +128

Left _< - 4 n = 12

228.6 _+21.1

923 + 80

Right ~ + 4 n = 23

272.0 +32.8

1 261 + 86

Position of center of gravity

Left placing

Right placing

stimulated limb showed a decline in force, a slight backwards displacement, and a diagonal postural reaction characterized by an increase of the animal's weight mainly on the contralateral forelimb and ipsilateral hindlimb. This diagonal supporting reaction persists during the displacement phase (Figs. 3 and 4). The postural reaction precedes and accompanies the displacement of the limb. Figure 3 illustrates the general pattern of limb reactions to the mechanical stimulus. At the moment of stimulation, which coincides with the vertical scale of the recorded weight tracings for each limb, the animal's weight was roughly equally distributed with slightly more weight on its forelimbs than its hindlimbs. Later, at the moment the stimulated limb ceased to support weight, indicated by the cursor, approximately 90% of the animal's weight was supported by the diagonally opposing limbs, the contralateral forelimb and the ipsilateral hindlimb. The remaining 10% of the animal's weight was sustained by the hindlimb contralateral to the stimulus. The duration of the isometric phase, as measured between the instant of the mechanical stimulation and the instant that the limb ceased to support any of the animal's weight, varied somewhat from animal to animal, with average values between 180 and 350 ms. For some animals the duration of the isometric phase for the right forelimb differed from that of the left forelimb. The difference might be ascribed to the preferred location of the "center of gravity" at the moment of stimulation of the forepaw. Further information on this problem was obtained from cat ELS with which two groups of trials were considered: one group was composed of trials in which

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M. Coulmance et al.

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Fig. 4. The postural events underlying the development of the placing reaction differ from one animal to another. In comparison with the cat Fig. 3, this animal (cat NRD) tended to stand more on its hindlimbs. This animal achieved the same objective as the previous animal, but the strategy used to relocate its "center of gravity" differed

the "center of gravity" appeared on the left side while the other consisted of trials with the "center of gravity" displaced to the right. As can be seen in Table 1, the duration of the isometric phase is slightly shorter when the animal's weight, at the onset of stimulation, is displaced to the side opposite to the limb stimulated. However, factors other than the weight initially supported by the placing limb come into play. For example, N R D exhibited a "center of gravity" shifted to the left, but the duration of the isometric phase was the same for both left and right placing.

Myographic Correlate Myographic activity of biceps, triceps, and palmaris was recorded in one cat of the series (ELS) and analyzed during five consecutive recording sessions. When the myographic activity is recorded from the stimulated forelimb (Fig. 5), one notes on the averaged traces an increased activity of the three recorded muscles, the onset of which is more or less synchronous and occurs about 40 to 80 ms before the signal indicating contact with the moving plate. This indicates that the effective stimulus for the onset of the myographic activity is not skin indentation, but most probably displacement of the hairs just prior to contact of

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Fig. 5. Myographic activity during the placing reaction. The averaged changes in myographic activity of palmaris (Palm.), biceps (Bi.) and triceps (Tri.) of the supporting and placing forelimbs are represented. Recordings from right forelimb exclusively which is in turn the supporting limb and the placing limb. Seven trials are averaged. The average was made by taking the time of contact of the plate-edge with the limb as reference for all the traces. The signal of the first trace indicated the time of the contact (force of 20 g) of the moving plate against the placing limb. An upward deflexion corresponds to left placing and a downward to right placing. The duration of the signal for each of the seven trials which are summated corresponds to the period of time during which the moving plate is in contact with the limb. Notice that the duration of the isometric phase varies for each trial as indicated by the scale-like termination of the averaged signal. The second trace corresponds to the force record of the platform supporting the right forelimb. Increase in weight is observed when the limb serves as the supporting limb. Decrease in weight to zero is noticed when the limb is the placing limb. The three others traces are integrated myograms with a time constant of l0 ms. For the further comments of the figure see text

t h e p l a t e e d g e a g a i n s t t h e skin. N o specific force c h a n g e s are r e l a t e d to t h e e a r l y myographic activations of the stimulated limb, apparently because an equal c o n t r a c t i o n o f t h e a n t a g o n i s t m u s c l e s t a k e s place. D u r i n g t h e i s o m e t r i c p h a s e o f t h e r e a c t i o n , a r e d u c t i o n o f activity a p p e a r s a n d is m o r e p r o n o u n c e d for t r i c e p s t h a n for biceps 9 T h e u n l o a d i n g o f t h e s t i m u l a t e d f o r e l i m b , w h i c h starts w i t h a d e l a y o f m o r e t h a n 100 m s w i t h r e s p e c t w i t h t h e o n s e t o f m y o g r a p h i c c h a n g e s , c a n n o t b e solely a t t r i b u t e d to t h e a c t i o n of single muscle contraction or inhibition, but coincides with complex m y o g r a p h i c c h a n g e s o f s e v e r a l f o r e l i m b m u s c l e s as well as w i t h m e c h a n i c a l c h a n g e s o f t h e o t h e r f o r e l i m b . W h e n t h e m o m e n t o f lift off is u s e d as a r e f e r e n c e t i m e for a v e r a g i n g i n p l a c e o f t h e t i m e o f s t i m u l a t i o n , o n e n o t e s t h a t a s e c o n d

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Fig. 6. Myographic activity during the placing reaction. Same representation as in Fig. 5, except that the average of the seven trials is made with a reference value corresponding to the time of lift-off (end of contact of the moving platform with the limbs). For further comments see text

burst of activity is seen in biceps, coincident with the placing m o v e m e n t ; the triceps activity remains deeply depressed (Fig. 6, right panel). This second burst of activity was also observed during placing when the animal was partially restrained by a h a m m o c k (Smith et al., 1978; Padel and Steinberg, 1978). During the increased loading of the supporting forelimb, a clearly increased triceps activity can be observed. This always precedes the force increase, by some 12 to 40 ms, and lasts through the isometric phase and well into the displacement phase (Figs. 5 and 6, left panels). E.m.g. changes occur prior to the contact with the moving platform when the limb performs the placing and prior or after the contact when the limb has a supporting function. The myographic changes thus precede the mechanical changes which are observed during the placing reaction in the standing cat.

The Projected Center of Gravity for the Placing Reaction As shown on the left side of Fig. 1, the centers of gravity observed for a group of behavioral trials, at the instant of contact of the mobile plate, appeared in a small zone roughly equidistant from all four limbs. If one now plots the "center

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Fig. 7. Change in the "center of gravity" in respect to time observed in two different animals between the moment of stimulation of the paw (0 ms) and paw lift-off, 256 ms and 204 ms, respectively. These tracings are from the same trials as those shown in Figs. 3 and 4, respectively. On the left (cat NOI), the animal's center of gravity indicated that about 57% of the animal's weight rested on the forelimbs at the time that both events occurred, but the "center of gravity" moved through a circuitous route before returning to a point at which the displacement phase began (256 ms). In the example on the right, 54% of the animal's weight was initially on the forelimbs and the "center of gravity", which lay close to the diagonal line, shifted directly to the right

of gravity" in the same fashion, but at the instant that the displacement of the left limb begins, the centers of gravity for all trials a p p e a r e d contralateral to the diagonal line intersecting the locations of the contralateral f o r e p a w and the ipsilateral hindpaw. As can be seen on Fig. 1, the positions of the center of gravity at the instant of lift-off of the limb are not r a n d o m l y distributed, but m o r e or less g r o u p e d along a line which is roughly parallel with the diagonal. This line (regression line) was calculated by the least squares m e t h o d and was f o u n d significant (P < 0.05) for the set of experimental positions (Fig. 1). This means that the percentage of the b o d y weight s u p p o r t e d by the two diagonally opposite limbs tends to be about the same w h e t h e r or not the " c e n t e r of gravity" is rostrally or caudally located. D a t a for four of six animals revealed a regression line which was nearly parallel with the diagonal line b e t w e e n the contralateral forelimb and ipsilateral hindlimb. The shift in the center of gravity, which must occur if the placing reaction is to take place, can be u n d e r s t o o d by c o m p a r i n g quantitative values in Fig. 2. This shift of the center of gravity can be visually tracked for a single trial by

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PATTERN

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Fig. 8. Comparison of the postural reactions of six animals. The dots at the corners of the dash-lined rectangles represent the position of the four limbs on the strain gauge platforms. The sequence for initiating the postural reaction in each of the limbs is ranked from the shortest latency (1), to the longest (3). All left-limb trials are shown at the left for each animal. With the exception of PNO, the postural reactions with left and right-limb trials tended to be symmetrical. The rank was determined from the latency measurements, using the serial order test of Wilcoxon (1949)

displaying a dot for each 4 ms interval (Fig. 7) from the time that the mechanical stimulus is given until the displacement phase begins. This type of display m o r e readily conveys the dynamic events that transpire following the stimulus and the different ways used by the animals to attain a stable base necessary for lifting the forepaw. In five of six animals the stimulus caused the " c e n t e r of gravity" to shift towards the h e a d for a duration o f about 1 0 0 - 1 5 0 ms after an initial delay of 2 0 - 4 0 ms. This is illustrated in the left-hand example of Fig. 7. T h e m o v e m e n t of the " c e n t e r of gravity" then slowed and r e t u r n e d again rapidly to about the same initial anter0-posterior coordinate but c a m e to lie within the triangle f o r m e d by the contralateral forelimb and the two hindlimbs. T h e m o m e n t a r y forward shift of the " c e n t e r of gravity" o c c u r r e d because the force applied by the non-stimulated f o r e p a w increased before any noticeable change in force a p p e a r e d in the o t h e r limbs. T h e animal in the right-hand example in Fig. 7 achieved the same objective by m o v i n g its " c e n t e r of gravity" in nearly a straight line to a position permitting lift-off of the stimulated paw.

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Comparison of Latencies of Force Changes of the Limbs During the isometric phase of the placing reaction, changes in force in the limbs establishes the diagonal weight-bearing stance on the contralateral forelimb and the ipsilateral hindlimb. The onset of these postural changes varies in time from limb to limb and from cat to cat. For the stimulated forelimb, the latency measurement was made from the time of onset of the unloading of the limb. The unloading was sometimes preceded by a slight transient oscillatory change in weight starting with the mechanical stimulus. Values from 22 to 126 ms were measured. Each animal starts to modify forces in each limb according to a given order which is characteristic for each animal. In order to see whether the order of latency in force changes a matched pairs, signed-ranks test was applied (Wilcoxon, 1949). Figure 8 illustrates the individual limb patterns of latency for the postural reactions in each cat, as revealed by this serial order test. The postural reaction never simultaneously begins in all four limbs: it may first appear in one or more limbs. Initial latencies may occur simultaneously in the fore- and hindlimb of one side of the body (cat NOI), or, as in one case, may first involve both forelimbs (cat NRD). The non-stimulated forelimb, in most cases, was the first limb to show a force change (cats ROU, PNO, NOI, NRD, ELS). It cannot be excluded that the individual patterns of postural responses may been influenced by different mechanical effects of the stimulus depending on the posture and tonus of the cat. Another factor which may have influenced the pattern may be the training procedures; they were not identical for all animals. The animals may have adopted a quiet standing posture in which the "center of gravity" was abnormally positioned. As each animal had a preferred "center of gravity" different from the others, it may explain why the latency patterns of the postural responses also differed for each animal.

Discussion

The common method of testing the placing reaction is for the experimenter to hold the cat and move it forward until the forepaw contacts the edge of a table top. Bard's (1933) classical description of the placing reaction, however, includes other types of placing; one type is performed by the standing animal and resembles the one used in our experiments. Amassian et al. (1972) also described a placing reaction provoked by a moving mechanical stimulus brought into contact with the forelimb. The placing reaction in our experiment served as a model for analyzing the adjustments of posture which accompany a stereotyped movement. Examination of the force changes exerted by the limbs of the standing cat during the placing reaction showed that forepaw lift-off is preceded by, and accompanied by, postural adjustments. These adjustments are necessary to move the animal from a quadrupedal stance, in which its weight rests on all four limbs, to a tripodal stance, in which the three non-stimulated limbs unequally support the animal's weight. In the latter stance, most of the animal's weight is supported by the diagonally opposing limb pair, the contralateral forepaw and

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the ipsilateral hindpaw in relation to the paw lifted. Each animal tested achieved a similar tripodal stance in order to permit forepaw lift-off, but the strategy employed to maneuver from one posture to the other differed for each animal. We shall explore the origin of the pattern of the postural reaction and speculate as to the localization of mechanisms controlling this reaction.

Diagonal Supporting Posture The placing reaction of one forelimb requires that the portion of the animal's weight, supported by the limb to be lifted, must be transferred to the other three limbs, but this weight shift is not equally distributed to the three limbs which support the animal. At the moment that the stimulated limb ceases to bear any weight, most of the animal's weight is supported ,by the diagonally opposed limbs. This diagonal supporting posture is roughly similar to what one would expect to observe if one of four legs of a rectangular table is removed so that only three legs make contact with the ground. The basic difference between the table and the quadruped is that the latter reduces the weight-bearing role of the limb diagonal to the limb lifted in order to place "center of gravity" between the 3 supporting members near the contralateral diagonal to assure stability of a postural "platform" on which one limb can be moved freely in space. It is an arrangement which assures the minimum relocation of the "center of gravity" by the animal to retain equilibrium (Ioffe and Andreyev, 1969; Gah6ry and Nieoullon, 1978). The diagonal supporting pattern was observed in the dog by Brookhart et al. (1965) as the animal spontaneously lifted one of its limbs. The same pattern has also been described in the dog by Ioffe and Andreyev (1969) during flexion movements of a posterior limb induced by nociceptive stimuli, or in the course of movements of the forelimb induced by instrumental conditioning. Gah6ry and Nieoullon (1978) observed the same pattern in cats when limb movement was produced by stimulation of motor cortex. It is worth noting the observation of Dobrzecka (1975) that placing of the left or right forelimb could be elicited with a much greater ease if a conditioned tactile stimulus was applied to the contralateral hindlimb rather than to the other limbs. Although the strategies for postural adjustment in the biped differ from those of the quadruped, it is interesting that displacement forward of one upper extremity is accompanied by contraction of the contralateral triceps surae of the lower extremity, a pattern which constitutes something akin to a diagonal postural supporting reaction (Belenkiy et al., 1967). The postural adjustments required to achieve a diagonal supporting stance are clearly distinguishable from the type of postural reaction provoked by sudden displacement anteriorly or posteriorly of the platform on which the animal is standing for this external disturbance influences hindlimbs and forelimbs in an almost symmetrical and simultaneous degree (Mori and Brookhart, 1968). The asymmetrical character of the diagonal supporting reaction appears to prepare the limbs for movements that are to be made in the direction of the long axis of the body. The diagonal supporting pattern is utilized

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for the trotting gait in which there is a regular alternation of weight support by diagonally opposing limbs (Roberts, 1967; Grillner, 1975; Miller et al., 1975).

The Intrinsic Properties of the Postural Reaction The diagonal supporting posture does not appear suddenly at the moment that forelimb flexion begins for the placing reaction. It precedes and accompanies the unweighting of the stimulated forelimb and the contralateral hindlimb. It is also not an adjustment unleashed by a sensory signal indicating a disturbance in the animal's equilibrium because the stimulus was too weak to produce disequilibrium. The reaction had an anticipatory character in the sense that it appeared before any disequilibrium could be produced by forelimb flexion. These anticipatory postural reactions have been described in man by Belenkyi et al. (1967), Gurfinkel and Ebner (1973), Alexeiev and Naidel (1973). These authors demonstrated electromyographically that activation of the triceps of the limb supplying postural support for the body occurred earlier than activation of muscles of the limb engaged in movement. As emphasized by Gurfinkel (pers. commun.), the anticipatory postural adjustment is quantified in a precise manner in proportion to an estimate of the amount of force that must be provided. This estimate simultaneously takes into account the initial postural condition, and evaluates the disequilibrium which will result from movement from one position to another.

Localization of the "'Postural Program" An interesting problem which deserves comment is the possible location of the "postural program" which must be brought into play before limb displacement can occur. Because there is little information on this point in the literature, it will be necessary to examine several hypotheses. The diagonal supporting reaction can be brought into play in the absence of motor cortex (Ioffe, 1975; R6gis et al., 1976), rubrospinal tract (Ioffe, 1975), and cerebellum (R6gis et al., 1976). Stimulation of forelimb or hindlimb area of motor cortex induces a diagonal support together with limb flexion even after pyramidal tract section (Gah6ry and Nieoullon, 1978; Nieoullon and Gah6ry, 1978). Stimulation of red nucleus also elicits the diagonal supporting reaction together with limb flexion. These observations suggest that the postural program might be located caudal to the red nucleus, at medullary or spinal levels. This hypothesis was suggested by Ioffe (1975). This is further supported by the similarities which exist between the diagonal supporting pattern during the placing reaction and the trotting gait during locomotion (Grillner, 1975; Miller et al., 1975; Viala and Buser, 1971). It is also suggested by the very brief latencies for postural reactions observed in the present study. It is well established that the locomotor pattern exists at the level of the spinal cord. It could be that the diagonal supporting response is brought into play by the same neural circuits utilized for locomotor events. However, it

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r e m a i n s u n c l e a r how the n e u r a l n e t w o r k s , which n o r m a l l y act as "oscillators" r e s p o n s i b l e for the m o b i l i z a t i o n of each limb, w o u l d f u n c t i o n in a flip-flop m a n n e r d u r i n g the d i a g o n a l s u p p o r t i n g stance a n d limb d i s p l a c e m e n t . It is p r o b a b l e that o t h e r c e n t r a l structures, such as n e o c e r e b e l l u m a n d basal ganglia, play a n i m p o r t a n t role in the postural a d j u s t m e n t associated with limb m o v e m e n t . M a r t i n (1967) e.g., suggested that the basal ganglia might be o n e possible location of a p o s t u r a l p r o g r a m a n d s u p p o r t e d his a r g u m e n t by citing the i m p o r t a n t deficits of p o s t u r a l a d j u s t m e n t p r e p a r a t o r y for m o v e m e n t s that occur in patients with P a r k i n s o n ' s disease. F u r t h e r e x p e r i m e n t s are n e e d e d to define the specific c o n t r i b u t i o n s of b r a i n stem a n d spinal m e c h a n i s m s m e d i a t i n g these postural adjustments.

Acknowledgements. The authors are very much indebted to Mr. Haour and Mr. Massarino for their contribution to the building up of the experimental device. This work was supported by the C.N.R.S. (A.T.P. no. 05A1 3618).

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Received November 15, 1978