Dorsal column contributions to motor behavior

EXPERIhIESTAL

KEI.ROLOGY

Dorsal

Column R.

Department

33, 53-68

(1971)

Contributions MELZACK

AIYD

of Psychology,

McGill

Received

to Motor J. A.

BRIDGES

Ukuersity,

May

Behavior 1

Montreal,

Canada

22, 1971

Cats with lesions of the dorsal column projection system were compared to sham-operated controls in their performance on two behavioral tasks: walking and turning on a narrow beam, and jumping to a moving platform. The results show: that cats with lesions of the dorsal columns at the cervical level make frequent errors, such as slipping and falling, during both behavioral tasks; and that lesions of the dorsal columns alone are more disruptive than lesions of the dorsal column nuclei or the lemniscal dccussation. The results suggest that the dorsal column system carries information that is essential for the performance of sequential response programs. A model is proposed in which the selection of a response program in a goal-oriented task is dependent on two possible functions of the dorsal column system: transmission of precise postural and tactile information prior to response; and activation of cognitive processes that evaluate the outcome of alternative response strategies. Introduction

The physiological and anatomical properties of the dorsal column projection system have received considerable attention in recent years (29), yet its functional role in behavior remains a mystery. Phylogenetically, the system has grown apace with the development of the cerebral cortex (2)) so that in man the dorsal columns comprise almost 40% of the cervical spinal cord (41). The system carries information from the largest cutaneous fibers, and from hair follicles, muscles, and joints (4, 5, 25, 32, 40). It has few relays and transmits rapidly to cortex (28). Most of its fibers adapt rapidly (4), so that fast, successive changes in stimulation at the skin are transmitted faithfully to the brain. Moreover, there is a high degree of somatotopic organization throughout the system from spinal cord to its projection in somatosensory and motorsensory cortex (3, 28, 42). The output of the dorsal column nuclei can be modulated by pyramidal (16, 1 This work was supported by Contract Research Projects Agency. We are grateful de Montreal for his generous and valuable appreciate the assistance and suggestions Dr. Bernard0 Dubrovsky.

DAHC 15-68-C-0396 from the Advanced to Dr. Jacques Courville at the Universite assistance in assessing the lesions. We also given by Peter Jaffe, Allan Basbaum, and

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21) and reticular ( 12, 29) projections, but the pyramidal influence is less pronounced in primates than in carnivores (13). On the basis of the available evidence, there are three theories of the role of the dorsal column projection system in behavior : The first theory (28) suggests that the dorsal column projection system is essential for fine tactual discrimination, spatial localization at the skin, and proprioceptive-kinesthetic functions. However, the experimental and clinical evidence, recently reviewed by \;l’all (41), is overwhelmingly against this theory. Animals with total dorsal column section are able to carry out roughness (17) and two-point (20) discrimination, and show no loss in vibration sensitivity (35) or ability to detect limb position (39). Similarly, human patients who have undergone unilateral surgical-section of the dorsal columns rarely show any permanent change in two-point discrimination (6). The second theory maintains that the dorsal column system is essential for projection of the body in extra-personal space. Ferraro and Berrara (9) observed that monkeys with lesions of the dorsal columns or dorsal column nuclei were ataxic and showed a loss of fine grasping movements. Their observation that behavior was more severely disrupted by lesions of the cervical dorsal columns than by lesions of the dorsal column nuclei (DCN) led them to propose that the cervical section (but not the DCN lesions) interrupted proprioceptive fibers going to the external cuneate nucelus and thence to cerebellum. More recently, Gilman and Denny-Brown (11) have shown that monkeys with lesions of the dorsal columns are ataxic, exhibit catatonic stances when deprived of vision, have deficiencies in placing and grasping, and an “inability to initiate exploratory palpating movements of the hands into extra-personal space.” The fact that the monkeys were able to carry out fine movements related to personal space-the body itself-led them to conclude that the dorsal columns are essential for tactile orienting reactions and projected movement into space. The third theory proposes that the dorsal column signals that project to the brain do not evoke “sensation” but activate memory stores that exert control, via centrifugal pathways, over input ascending in the more slowly conducting somatosensory pathways (22-24). Melzack and Wall (24) have proposed that the dorsal column projection system acts as a central control trigger to form the input or “feed-forward” limb of a larger feedback loop in which central control processes and preset response strategies are activated before the input projected up the more slowly conducting pathways produces sensory experience and overt behavior. It is apparent that the last two theories have much in common. Indeed, Wall (41) has recently combined both to suggest that the dorsal column system is necessary for internal search and external exploration. However,

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there is insufficient evidence to support any particular theory. A more detailed analysis of the role of the dorsal column system in behavior is, therefore, required. The purpose of the present study was to examine the effects of lesions of the dorsal column projection system on behavioral tasks that approximate the normal behavior of feline species : coordinated walking and turning on a narrow beam, and jumping to a moving target. Methods Seventeen naive, adult, male cats served as subjects. After the cats were anesthetized with Nembutal. they were placed into a stereotaxic instrument, and the lower medulla and upper cervical spinal cord were exposed under aseptic conditions. Using the dorsal roots or fourth ventricle as guides, lesions were made, using a No. 11 scalpel blade, of the dorsal columns at the Cl-C2 level. In some cats a larger lesion was made to include the dorsal column nuclei. The ventral extent of the lesions was varied to include either the lemniscal or pyramidal decussation. After completion of the lesions, the muscle and skin were sutured, and an antibiotic was administered intramuscularly. Cats chosen randomly from the group were designated as controls, and the muscle and skin were sutured after the dura mater was cut to expose the cord. After surgery, the cats were placed in individual cages for 1-2 weeks, and were observed daily for motor ability, placing, and orienting responses. They were then housed in a large colony room, where they had ample opportunity to run about, climb the wire-mesh walls, jump on and off ledges at several heights, and interact socially with one another. Behavioral testing was begun 2-4 weeks after surgery. Two tests were used. Their choice derived from consideration of the natural behavior of feline species. The first task was suggested by observations that cats often walk or run on the branches of trees to escape dogs or chase birds. The laboratory analogue required the cat to walk along a beam that was 7.6 cm wide, 5.1 cm deep, 305 cm long, and 183 cm above floor level. The beam had a natural warp that, beginning at midpoint, twisted it gradually until the angle reached a maximum of 8”. The cat, after 23-hr food deprivation, was placed on the center of the beam, and its attention was drawn to a small dish of salmon at the warped end by tapping it with a spoon. The cat walked to the dish, ate, and then its attention was drawn to a food dish at the other end. The cat turned, walked the length of the beam, and ate. This procedure comprised one trial. Ten trials were given each day for 6 days. A complete record of behavior was made by two observers. Errors were recorded separately for walking and for turning (which involved the sequence of pivoting, placing, and initiation of walking). The behavioral criteria for errors were slips of the paws on the beam during walking,

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splaying out of the paws, slips of the paws off the edge of the beam, falling off the beam, and thrusting the paws into space. Casual observations of the way the animals walked (crouched low, or body well above the beam) were also recorded. No more than one of each type of error was recorded on each trial. If a cat failed to move after 3 min, it was not tested further on that day, and its performance was scored as 0% perfect trials. The second test-a laboratory analogue of jumping through space toward a moving prey-required each cat to jump from a stationary circular platform (25.4 cm diameter) to a moving platform (25 X 33 cm) that rotated around it. The center platform was 91.4 cm above floor level and the rotating platform was 15.2 cm lower. The cats were first trained to jump to the food-platform when it was kept stationary. All cats were given 10 trials a day for 4 days, The cats were then required to jump from the center to the rotating platform under four conditions : (a) 61 cm distance at a rotational speed of 21.3 cm/set ; (b) 61 cm at 28 cm/set ; (c) 91.4 cm at 57.9 cm/set ; and (d) 91.4 cm at 94.5 cm/set. The original plan to test the cats until they made perfect jumps failed to work because some of the cats made persistent errors, with no sign of improvement. Consequently it was decided to utilize the data on only the first day of each of the four conditions. The criteria for errors were slips of the paws when landing, landing at the edge rather than the center of the rotating platform, splaying out of the legs during landing, and falling or sliding off the platform. After these tests, the cats were examined for orienting responses, and for righting reflexes with and without a hood on the head. The brains were removed after the cats completed the behavioral tasks. Alternate brain sections were stained using cresyl violet or Weil techniques. Histological examination was carried out by light microscopy, and the extent of each lesion was determined by Dr. Jacques Courville at the Universite de Montreal. The lesions were classified into the groups specified in the results below. All behavioral comparisons were then statistically analyzed by using the Mann-Whitney U-test (36). Results

Eight cats had large (SO-100%) lesions at one or more levels of the dorsal column projection system. Three cats had lesions of the dorsal columns at the cervical level, two had lesions of the dorsal column nuclei, two had lesions of both the columns and the nuclei, and one had a total lesion of the lemniscal decussation. Statistical analysis showed that these cats made significantly more errors than the sham-operated controls during walking (P = 002) and turning (p = .002) on the beam, and jumping (p = .025) to the moving platform. Closer analysis, however, indicated differences between the cats with lesions of the dorsal columns alone and,

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those with lesions of the nuclei or their projection through the lemniscal decussation. The analysis below, therefore, treats the two groups separately. Sham-operated Control Group. Figure 1 shows the performance of the four cats that comprise the control group. The percentage of perfect trials for each cat is shown for walking and turning on the beam, and for jumping to the moving platform. It is evident that their performance on the beam ranged from 90-1000/o perfect trials. The cats walked briskly along the beam toward the food, and made surefooted, perfectly placed movements. Errors were rare and consisted mostly of occasional slips of a single paw. They were distributed evenly across the 6 days of testing (Fig. 2). These cats, when turning, pivoted smoothly on the hind paws until the forepaws touched the beam to make a perfectly coordinated rotation. The cats then walked the full length of the beam to food at the other end. This sequence of walking and pivoting movements showed a smoothness and sureness that suggested that the controls “knew” precisely where their limbs were in spatial relation to the beam.

Walking

Turning

Jumping

1234

Cat Numba

1. Sham-operated control group. Right: percentages of perfect (errorless) for walking and turning on the beam, and jumping to the moving platform. cross sections of the brainstem at the level of the dorsal column nuclei and cervical dorsal columns. Abbreviations : cbs, cross bulbospinal tract; CU, n. cuneatis ; anterolateralis ; DC, dorsal columns ; DV, descending trigeminal nucleus ; fal, funiculus GR, n. gracilis ; lbs, lateral bulbospinal tract ; MLX, decussation of medial lemniscus ; mrs, medial reticulospinal tract; PX, decussation of pyramids; rs, rubrospinal tract. (After Verhaart, 38). FIG.

trials Right:

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The control cats’ performance on the jumping apparatus showed a wider range than on the beam. Three cats performed throughout at the 85% level or better. One cat, however, performed at the 100% level when the rotating platform was at the 61-cm distance, but refused to jump when the distance was extended to 91.4 cm and the rotational speeds were increased. Lesions of the Dorsal CO~UWW. The cats with lesions of the dorsal columns (DC group) showed striking behavioral difficulties on both tasks (Figs. 2, 3). These difficulties are best described as a loss of sureness, or precision, or deftness in performing sequential movements. The cats tended to crawl along the beam on their bellies, crouched low, taking one slow step after another. Beam-walking is a complex task, involving balance and proper placing of the paws in sequence on the narrow ledge. The errors were primarily misplacements, usually involving slips of two or more

90

80

70

30

20

10

0 1

2

Days:

3

10 Trials

4

per

5

6

day

FIG. 2. Percentages of perfect walking and turning trials on successive days for the sham-operated controls (0) and two experimental groups: cats with lesions of the dorsal columns (A) ; and cats with lesions of the dorsal column nuclei or lemniscal decussation (0). Walking, solid lines ; turning, broken lines.

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paws. The paws sometimes slipped off the edge oi the beam or were estended into space. At these times, the cats sometimes lost balance and fell off the ledge : cat no. 6 fell off on 24 out of 50 trials (48%). Falling was most common during turning. In contrast to the smooth pivots made by the control cats, the DC group made tentative movements of the forepaws, tried to pivot and failed, or made the movements in a series of approsimations, precariously maintaining balance, and frequently falling off. Statistical analysis of the results showed that the DC group made significantly more errors than the control group during walking ( p = .03) and turning (p = .03) on the beam. The performance of the DC group on the jumping task was erratic. During the shaping trials, the cats jumped with an agility that was comparable to that of the control cats. \Vhen the platform was moving. however, they often hesitated before jumpin g, or made tentative jumping movements that were then aborted. In contrast to the control cats, who jumped within 2 or 3 set after being p!aced on the platform, they characteristically piv-

FIG. 3. Lesions of the dorsal columns. Cats no. 5. 6, and f have total dorsal columns at the cervical level. The percentages of perfect walking, jumping trials are shown for each cat.

lesions of the turninn, and

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oted for a minute or more as they followed the circling platform, before attempting to jump. They frequently landed off-center, and the paws often slipped or splayed out when they landed. Cat 6 refused to jump to the moving platform even though it jumped perfectly when the platform was stationary. Cat no. 5 jumped at the 40% level of perfect trials to the first three speed-distance tests, but refused to jump to the last one. Cat no. 7 showed improvement during the first three tests (from 20% to 100%) but then refused to jump to the last one. Statistical analysis showed that these cats were significantly worse than the controls across the four tests (p = .03). Lesions of the Dorsal Cohnn Nuclei OY Lewniscal Decussation. The location and extent of the lesions is shown in Fig. 4. Cats no. 8 and 9 had

‘“7

Walking

C_Jumping

FIG. 4. Lesions of the dorsal column nuclei (DCN) or no 8 and 9 have lesions of 80-90s of the DCN, and cat the decussation. Cats no. 11 and 12 have lesions of S&90% lesions of the dorsal columns. The percentages of perfect ing trials are shown for each cat.

lemniscal decussation. Cats no. 10 has a total lesion of of the DCN as well as total walking, turning, and jump-

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lesions of SO-90% of the dorsal column nuclei, and Cat no. 10 had a total lesion of the lemniscal decussation. Cats no. 11 and 12 had lesions of 80-90s of the nuclei as well as total lesions of the dorsal columns at the cervical level. Surprisingly, these cats made significantly fewer errors than the DC group during walking (/I = .02 j and turning (p = .02) on the beam. However, they made significantly more errors than the control group during walking (/J = .02) and turning (p = .02 ). The errors were similar to those observed in the DC group, but were not as frequent or severe. These cats showed a wide range in error scores on the jumping task and. as a group, were not significantly different from either the control or DC groups. Note, moreover. that cats no. 11 and 12, with lesions of the dorsal columns in addition to the nuclei do not appear to be different from the remaining three cats with lesions of only the nuclei or their projection through the lemniscal decussation. Supplrwmzta.ry Obshw.~ations. Four cats had partial lesions of the pyramidal decussation (20-90s ) in addition to DCK lesions (75-100%). The behavior of these cats was similar to that of the cats with lesions of the DCN alone. No behavioral pattern emerged to indicate that the partial pyramidal lesion produced a significant additional impairment. However, one cat with a total lesion of the DCN and the pyramidal decussation was so atasic that he continually fell off the beam and could not be tested properly. Tests of orientation to somatic stimuli were also carried out during the experiment. There was no difference between the control cats and any of the groups with lesions. X11 the cats characteristically turned the head to examine the paw or tail Lvhen it was pinched or stroked, and frequently made movements aimed at deflecting the experimenter’s hand. Finally, there were no differences between the cats with lesions and the control group in placing or righting reflexes. These tests were carried out with and without blindfolding, and no differences appeared in either testing condition. Discussion

The results show : that cats with lesions of the dorsal column projection system make frequent errors during walking and turning on a narrow beam and jumping to a moving platform: and that lesions of the dorsal columns alone are more disruptive than larger lesions of the dorsal columns plus the nuclei or of the lemniscal decussation. The nature of the motor difficulties-slips, missteps. splaying of the paws, inability to make smooth whole-body pivots during turning, and errors in jumping and landing-cannot be explained in terms of disruption of orientation-esploration movements. as Gilman and Denny-Brown ( 11 j and IYall (41) have pro-

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posed. Rather, the lesions appear to affect the performance of serial behavior patterns involving many components : initiation of the response from a particular posture ; maintenance of balance ; coordinated sequential placing of the paws; judgment of distance and speed for effective jumping and precision in landing ; and so forth. Dubrovsky et al. (7) have recently obtained similar data which also show that the dorsal column input plays a role in serial, patterned behavior. The dorsal column system, then, can only be understood in terms of its relation to the motor system as a whole. These observations suggest a new model (Fig. 5) of the functions of the dorsal column projection system. It is proposed that the dorsal column projection system plays an important role in the choice of an appropriate behavior program. Let us consider what happens when a cat is placed on the beam or the jumping platform. The motivational state (hunger) and sensory inputs (vision, audition, and possibly smell) would contribute to the selection of a small number of possible output programs (e.g., walk, run or jump, turn left or right, etc.) to get to the food-goal (26). The neural activities representing these programs would have the role of selectively activating (or facilitating) neural circuits for subsequent input and output processing related to the programs. The particular program that is selected, however, must be determined by information on the posture of the body prior to response, and by cognitive activities such as the cat’s earlier experience of the outcome of different response strategies. The dorsal column projection system could play a role in both of these activities. To carry out an appropriate response program, the brain must know the precise posture of the body: the position of the head, trunk and legs; the tension on muscle groups; the angles of the joints; and so forth. It must also know the relation of the body to adjacent environmental surfaces, such as tactile or other inputs acting on the hair and skin. This information may undergo rapid, continuous change, such as occurs in the cat ready to spring at the circling platform and whose body rotates as it readies itself to jump. The dorsal column system is eminently suited to transmit these inputs, which comprise essential information for the choice of the specific response program. It carries precise somatotopic information from the joints, muscles, hair, and skin. Its fibers adapt rapidly to signal sudden postural and cutaneous changes. It also transmits this information rapidly to sensory and motor cortex, which can evaluate the posture at the moment in terms of earlier kinesthetic, cutaneous and visual experience (14, 34). The particular response program which is evoked must also depend on cognitive factors such as past experience, the meaning of the situation, and evaluation of the outcome of different response strategies. Thus, dogs that

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FIG. 5. Schematic model of the functions of the dorsal column projection system. Sensory, motivational, and cognitive activities at a given moment selectively activate neural circuits (Program Selection) that represent a small number of alternative behavior programs to attain a goal. The output of the programs is projected to loci

at several levels of the nervous system. Neuron pools in the dorsal column nuclei are selectively facilitated, and project precise postural and tactile information to (a) regions (Central Control Processes) that evaluate the selected programs in terms of prior experience, and (b) those that activate the final Response Command. Motoneuron pools in the ventral horns, which had been facilitated by the earlier program selection to produce several possible behavior patterns, are selectively activated by the large and small efferent fibers, and produce the final pattern to muscles. The efferent activity to the dorsal column nuclei and the dorsal horn cells may continue to modulate the input during the ensuing motor behavior. Open lines represent the traditional S-R circuit. Solid lines represent the circuits involved in program selection prior to the

central response command that produces overt behavior. repeatedly receive food immediately after a leg is shocked, burned, or cut soon shop anticipatory eating responses (without any signs of pain ) , yet make escape responses when the stinmli are applied to the other legs (30. 31 j. Similarly, tnen wounded in battle often respond to the wound xvithout

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any evidence of pain but make obvious pain responsesto an inept vein puncture ( 1) . The input, then, is localized, identified in terms of its physical properties, evaluated in relation to past experience, and modified before it activates a particular response program. The system performing these complex functions of identification, evaluation and program selection must conduct rapidly to the cortex so that the somatosensory information has the opportunity to activate memory stores and preset response strategies. Moreover, it must be able to exert selective descending control over information being transmitted through the more slowly conducting pathways that synapse in the dorsal horns. Melzack and Wall (24) have proposed that the dorsal column projection system acts as a central control trigger to form the input or “feed-forward” limb of this loop. It is assumed that these signals, carrying precise information about the stimulus, do not evoke “sensation” but contribute to input modulation and to the selection of the appropriate responseprogram. It is proposed that the final response command-that is, activation of a specific response program-occurs as a result of interactions of the postural and tactile input, the central neural processesunderlying evaluation of response strategies in terms of prior experience, and the active neural circuits representing several possible program sequences (Fig. 5). After a program is activated, impulses descending the largest pyramidal fibers could selectively facilitate all the motoneuron pools necessary to carry out the entire sequence (19). These impulses would be below firing threshold for the pools (27). Impulses descending the slower pyramidal and extrapyramidal fibers would then provide the additional excitation to fire the pools in serial order and produce the sequential muscle patterns for overt behavior (19, 27). Once a response program is triggered, the dorsal column output need play no further role. Indeed, the output of the dorsal column nuclei may be actively inhibited after onset of a behavior sequence (J. O’Keefe, personal communication). The specific execution of the program would depend on somatic, visual, and other inputs that act on the more slowly conducting efferent fibers. Feedback from the limbs is not critical, as Lashley (19) has suggested, and as experiments on deafferented monkeys have shown (37). However, the loss of the dorsal column contribution to the selection of the appropriate response program would result in activation of programs that are not precisely adapted to the prevailing conditions of the situation. The organism would still be capable of carrying out sequential behavior programs on the basis of input through the more slowly conducting systems, but there would be a loss in the precision of the response sequence. Delays in onset of the program, slips, missteps, errors in jumping and landing would be expected to occur, and these properties were characteristics of the cats with dorsal column lesions.

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The concept developed here is consistent with the fact that the cats with dorsal colum lesions showed persistent errors on the beam task, but improved in the jumping task. This may be due to differences inherent in the two tasks. One requires prolonged sequences (walking, eating, turning, etc., as well as preparatory behavior for each new phase), while the other requires a shorter pattern (preparation for jumping, the jump, and the landing). The shorter pattern appears to be less disrupted than the longer one by lesions of the dorsal column system. The fact that the cats with lesions of the dorsal column nuclei (DCN) perform better than cats with lesions of the dorsal co1~1m11s alone is paradoxical. However, both lesions would have different effects on the information transmitted to higher levels. If the DCX are spared, the spontaneous activity of DCN neurons as well as activity patterns evoked by pyramidal and reticular inputs to the nuclei would be projected to higher levels. In the absence of input through the dorsal columns. the brain would receive misinformation. This misinformation may account for the greater disturbance. It cannot be attributed to the sparing of a cerebellar projection through the external cuneate nucleus, as Ferraro and l3errara (9) suggested for their monkeys, since two of the DCN cats also had total dorsal column lesions. In contrast, total abolition of information from the DCN could provide the conditions for reorganization (by descending controls) to enhance information transmission through the remaining channels of the somatosensory projection systems. Four features of the model require further consideration. First, the model suggests that several possible response programs, acquired as a result of earlier motor behavior and feedback, may be activated in the presence of a goal. The final response command may comprise one of these programs or selected components from several of them. Thus, a person who is fluently bilingual in French and English may, in the presence of other bilinguals, switch from one language to the other depending entirely on who he is facing at the moment. Obviously two language programs are active at the same time. Another, more common, example is the person who wishes to write to a colleague in another city but instead of reaching for a pen lifts the receiver off the telephone. ,4s Milner (26) has suggested, Lashley’s (19) concept requires an additional stage at a higher level of organization: activation of several programs from which one is selected, and then, at a lower level, facilitation of motoneuron pools that represent the entire program, followed by activity that fires them in the correct sequence. Second. the spatial relationships among the component activities suggest that the activation of several possible program sequences by sensory, motivational, or cognitive activities occurs at a lower anatomical level than the

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areas involved in the final response command. This derives from evidence that brain-stem structures receive convergent inputs from all areas of the brain-sensory, limbic, and cortical-and that stimulation of hypothalamic and midbrain regions produces whole, coordinated behavior sequences (1.5, 33). In contrast, central control processing is assumed to involve predominantly cortical circuits. The response command regions would include motorsensory cortex (3) but would involve more widespread efferent circuits including the pyramidal and extrapyramidal systems and their complex interactions. Third, the time required for the interactions and feedback processes is consistent with behavioral and physiological studies of reaction times. In man, the reaction time for a simple response to a simple stimulus is of the order of 180 msec, and to two stimuli requiring discrimination it increases to about 300 msec ; for discrimination of five or six stimuli, it rises to about 500 msec (43). In the rat, latency to perform a thoroughly trained, highly practiced blackwhite discrimination is 4 set (43). In the awake monkey (S), the time between the presentation of a visual stimulus and the first appearance of motor cortical spikes is 100 msec, and the highly trained response occurs 50-100 msec later. All of these time-durations are sufficiently long to permit the feedback and interaction processes shown in the model. Finally, the point at which awareness enters the process is problematical. It is proposed that the processing up to activation of the response command occurs without any associated awareness. The neural activity that comprises the response command is the awareness of movement, in the absence of any feedback from the limbs. There is convincing evidence that it is the efferent message, rather than the sensory feedback, that may underlie the feeling of active movement ( 10, 18, 25,27, 37). References

1. 2.

3.

H. K. 1959. “Measurement of subjective responses: Quantitative effects of drugs.” Oxford Univ. Press, New York. BISHOP, G. H. 1959. The relation between nerve fiber size and sensory modality: phylogenetic implications of the afferent innervation of cortex. J. Nerw. Mefcl. BEECHER,

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B. O., E. DAVELAAR, and E. GARCIA-RILL. 1971. Role of dorsal c01in serial order behavior. Exj. Srrwol. (in press). EVARTS, E. V. 1968, Relation of pyramidal tract activity to force exerted during voluntary movement. J. Nc~roph)~ioZ. 31 : 14-27. FERRARO, A., and S. E. BERRARA. 1934. Effects of experimental lesions of the posterior columns in hlactrr~s rllcszts monkeys. Brairl 57 : 307-332. FESTINGER, L., C. A. BLTRXHAM, H. 0x0, and D. BAMBER. 1967. Efference and the conscious experience of perception. J. Exp. P.rycho/. Monoyr. 74: l-36. GILMAN, S., and D. DENNY-BROWX. 1966. Disorders of movement and behavior following dorsal column lesions. BY& 89 : 397-418. GUZMAN-FLORES, C., N. BUENDIA, C. ANDERSON, and D. B. LINDSLEY. 1962. Cortical and reticular influences upon evoked responses in dorsal column nuclei. Erp. Nclkrol. 5 : 37-46. HARRIS, F., S. J. JABBUR, R. W. MORSE, and A. L. TOI~VE. 1965. Influence of the cerebral cortex on the cuneate nucleus of the monkey. IVntlkrc Lodon 206: 1215-1216. HEAD, H., and G. HOLMES. 1911-1912. Sensory disturbances from cerebral lesions. Brah 34: 102-254. HESS, W. R. 1957. “The Functional Organization of the Diencephalon.” Grune and Stratton, New York. JABBUR, S. J., and A. L. TOWE. 1960. Effect of pyramidal tract activity on dorsal column nuclei. Scirttcc 132 : 547-548. KITAI, S. T., and J. WEINBERG. 1968. Tactile discrimination study of the dorsal column-medial lemniscal system and spino-cervico-thalamic tract in cat. E.2-p.

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14. 15. 16. 17.

Bra.& RES. 6 : 234-246. 18. 19. 20. 21. 22. 23.

24. 25.

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