- Email: [email protected]
Role of postural deficits in oro-ingestive problems caused by globus pallidus lesions
EXPERIMENTAL
NEUROLOGY
74, 93-110 (1981)
Role of Postural Deficits in Oro-Ingestive Problems by Globus Pallidus Lesions
Caused
T. LABUSZEWSKI, R. LOCKWOOD, F. E. MCMANUS, L. R. EDELSTEIN. AND T. I. LIDSKY’ Department of Psychology, State University of New York, Stony Brook, New York 11794 Received January 15. 1981: revision received April 21. 1981 There is a large literature demonstrating that rats with globus pallidus lesions have ingestional problems. In an effort to understand the bases of these deficits, the ingestional activity of normal and brain-damaged animals was subjected to scrutiny. Rats were trained to lick a spout recessed behind a Plexiglas wall for 8% sucrose solution. The characteristic interlick interval and lick duration distributions observed in normal animals were severely disrupted by globus pallidus lesions. This disturbance was, in large part, due to an inability to correctly position the mouth with respect to the spout and maintain that position for a burst of licks, activities which normally ensure consistently efficient ingestion. After pallidal lesions, animals often miss the spout altogether. When they do find the spout, only the first few licks are on target. The head then drifts away from the correct position and subsequent licks miss the spout. Animals’ ability to continue licking during slow lateral displacement of the spout was also tested. Animals with pallidal lesions showed severe deficits. In addition to problems with head positioning, pallidal animals failed to adapt their body posture to enable licking at different spout locations. In relation to clinical and experimental findings, these data implicate the basal ganglia in feedback-regulated control of axial and proximal muscles.
INTRODUCTION The most striking behavioral effect of globus pallidus (GP) lesions in rats and cats is a disruption of ingestion lasting a few days to several weeks ( 19, 20). In view of the vast literature which implicates the basal ganglia Abbreviations: GP-globus pallidus, VPM-ventralis posteromedialis. ’ The authors gratefully acknowledge B. Federchuck and D. Lederman for assistance in early phases of the experiment and also A. Castaldi, J. Lavery, and G. Sintchak for superb technical help. Please address all reprint requests to T. Lidsky. This research was supported by U.S. Public Health Service grants NS 15328 and NS 16054. 93 0014-4886/81/100093-18$02.00/0 Copyright 0 1981 by Academic Press, Inc. All rights of reproduction in any form reserved.
94
LABUSZEWSKI
ET AL.
in the control of movement, it seems plausible that GP lesion-induced aphagia and adipsia may be due to motor problems. Therefore, it is surprising that although the ingestion problems of GP-damaged animals have been investigated in a variety of ways [e.g., (1, 9, 22)], few studies directly assessed motor capabilities as they apply to oro-ingestive behavior. However, several observations in the course of research addressed to other characteristics of the GP lesion syndrome, suggested movement difficulties. Animals with lesions appeared unable to fully extend the tongue while drinking and seemed unable or unwilling to bite with normal force (17). These observations, although indicating that movement problems might underlie the ingestion disturbance in GP animals, also are rather problematic. It is difficult to understand why GP lesions disturbed licking and chewing inasmuch as these basic movement patterns are organized in the brain stem and can proceed in a normal fashion despite the absence of the entire forebrain including the basal ganglia (3, 7). To better assess the motoric basis of aphagia and adipsia and to eventually proceed beyond the general category of “motor” to a more precise understanding of the processes mediated by the GP, it is necessary to obtain a detailed description of the changes in motor patterns caused by damage in this brain region. To do this, methodologies are required which are tailored to the relatively rapid temporal characteristics of ingestive behavior. It was the aim of the present work to provide some of this descriptive information. METHODS The experiments used male albino rats weighing 220 to 240 g at the commencement of testing. The animals were their own controls: observations made prior to surgery were compared with observations of that same animal’s behavior after it had received the lesion. Using standard stereotaxic techniques, electrolytic lesions were made in the GP of nine rats. Because the gustatory thalamocortical projection originating in nucleus ventralis posteromedialis (VPM) traverses the GP (1 l), the VPM was lesioned in five additional animals to control for the effects of damaging these fibers of passage. Testing Procedures. To assess licking behavior, rats were placed in a Plexiglas cage (L: 30 cm, W: 26 cm, H: 20 cm) in which a 2-cm diameter hole in one wall allowed access to a stainless-steel tube from which an 8% sucrose solution was continuously available. To ensure that animals drank steadily throughout the 16-min test session, they were reduced to 90% of ad libitum weight and maintained to gain 5 g/week. The drinking tube was mounted on a rack and pinion device which allowed the tube to be
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
95
recessed through the hole in the cage wall. Observations were made when the tube was recessed between 0 and 5 mm with respect to the outside surface of the Plexiglas wall and the center of the aperture. Because of the orientation of the spout with respect to the hole in the cage wall, the animals had to assume a head position during drinking which prevented them from seeing the spout (Fig. 3). The drinking tube was also mounted on a lead screw and positioned perpendicular to its longitudinal axis (Fig. 1). The lead screw was attached to a DC digital stepping motor. Activation of this motor caused smooth lateral movement of the drinking tube and was used to assess the rat’s tracking ability. Stepping speed, number of steps, and step direction were all controlled by the experimenter to obtain lateral drinking tube displacements of reproducible velocity, magnitude, and direction. Tracking ability was tested in a subgroup composed of five GP and three VPM animals. Data concerning the characteristics of individual licks were obtained with a specially designed drinkometer (15) which signaled both when the animal’s tongue first contacted the drinking tube and also the duration of tongue-tube contact. Current passed by this device was considerably less than the ~-IA minimum which can be sensed by rats. The behavior (e.g., head position, body posture, etc.) was observed directly for every animal during all test sessions. To verify and make a more permanent record of these observations, the actions of five GP and three VPM rats were filmed before and after placing the lesions. Several different camera angles were used with each rat to record accuracy of head and body position as well as tongue movement. Filming speed varied with the behavior to be filmed and ranged from 18 to 36 frames per second. Data Analysis. All drinkometer data were stored on tape for later anal-
FIG. I. Schematic of moveable drinking tube used to assesstracking behavior. Shown is a top view and only the front portion of the test chamber is included. Arrows indicate possible directions of drinking tube movement. Abbreviations: A-aperture; C.W.-cage wall, D.T.drinking tube, G.F.-grid floor, L.S.-lead screw, R. & P.-rack and pinion device, S.M.stepping motor.
96
LABUSZEWSKI
ET AL.
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
98
LABUSZEWSKI
ET AL.
ysis by a laboratory computer (Cromemco Corp). Lick duration was defined as the period beginning with the tongue contacting the drinking tube and ending when contact was broken. Interlick interval was the time elapsed between the tongue breaking contact with the drinking tube and making contact again on successive licks. Population histograms of lick durations and interlick intervals were calculated with associated means and standard deviations. Filmed sequences were assessed with standard frame by frame analysis. At the completion of testing, the animals were deeply anesthetized and perfused with formol-saline. The brains were sectioned (40pm) and stained with cresyl violet for histological analysis. RESULTS Histology. The data presented below describing the effects of pallidal damage were derived from observations of animals with bilateral lesions in the GP. In all cases, more than 50% of the GP was destroyed on each side. Other regions damaged by these lesions were the internal capsule and the neostriatum. However, extrapallidal damage was typically quite minor (Fig. 2) and varied from animal to animal particularly with regard to bilaterality. In addition to the nine rats with bilateral GP lesions, two rats had only unilateral GP damage. These unilaterally operated animals showed none of the ingestional difficulties described in the following paragraphs. Thus, behavioral effects were correlated with bilateral destruction of the GP. Animals included in the VPM group had large thalamic lesions which destroyed at least 75% of the VPM. In three of the five rats, the lesion extended dorsally to cause substantial (20 to 40%) damage in the centre medianurn. Slight unilateral damage to the medial portion of nucleus ventralis pasterolateralis was also caused in two rats. The sequelae of thalamic damage observed in the ingestional testing were associated only with VPM damage. Acute Effects of Lesions. GP animals showed transient aphagia and adipsia lasting from several days to several weeks. The precise point at which animals resumed ingestion was difficult to specify because food and water were always available in the home cage. Unless an animal was actually seen to be eating or drinking, decreases in the amount of food or water present could have been due to spillage and evaporation. To facilitate recovery, the animals were given palatable foods (e.g., chocolate chip cookies) in an easily chewable form (wet mash) in addition to the normal supply of pellet food. During the period of aphagia and adipsia, GP rats always showed considerable interest in the cookie mash. When a fresh supply was put in the cage, the animal typically came over to the dish to investigate although it did not eat.
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
99
If aphagia and adipsia lasted more than 2 days, GP animals were maintained by forcing liquified food into the back of the mouth with a plastic tube and syringe. Food introduced in this way elicited licking, chewing, and swallowing. This reflexive licking and chewing were of seemingly normal speed and vigor, although quantitative measures were not taken. Tactile stimulation of the perioral and intraoral tissue during forced feeding caused the animals to turn away from the plastic tube. These animals showed no signs of sensory neglect (16). However, when GP animals first began to eat of their own volition, they exhibited considerable difficulty in efficiently manipulating the food with the mouth as evidenced by the large quantities of food which were dropped during chewing. This problem gradually disappeared during the next few days. During the entire period of aphagia and adipsia, GP animals did not groom. This behavior reappeared in conjunction with eating and drinking. After GP animals recovered sufficiently to increase their body weights beyond preoperative levels, there were no obvious lasting signs of brain damage (except those noted during formal testing for ingestion behaviorsee below). At this time, animals were given food only in pellet form and ingestion patterns in the home cage were normal. Posture, locomotion, grooming, and other movement patterns were apparently normal. VPM animals were neither aphagic nor adipsic and experienced no weight losses. However, these animals initially displayed problems in efficiently manipulating food with the mouth which were similar to the problems of GP animals. As with GP lesions, food spillage lasted only a few days. In contrast to animals with GP lesions, VPM animals began grooming within hours of recovery from anesthesia. Ingestive behavior was tested both prior to surgery and also after recovery from the acute effects of lesions. Rats with VPM lesions showed no abnormalities during ingestion testing. Therefore, to facilitate description of lesion-induced deficits, behavior of GP rats will be contrasted only with that of normal rats. Normal Rats-Stationary Spout. At the beginning of the test session, each animal exhibited similar patterns of orientational activity. The rat approached the aperture in the Plexiglas wall, sniffed, and then tapped the tip of the drinking tube with the tip of the nose. Immediately afterward, the rat positioned itself close to the aperture and began to lick. In the large majority of cases, the initial licks were on target (Fig. 3); however, if the first lick missed the drinking tube, the animal made slight adjustments of head position so that subsequent licks were accurate. Animals typically licked continuously for the first half of the test session. For the remainder of the period, bursts of licking (- 30 s) were interspersed with bouts of
RAT 201: PRE-LESION A
8
B
C
FIG. 3. Filmed sequences of licking behavior before and after globus pallidus lesions. Spout is recessed. A-prelesion. Note relative invariance of head position and accuracy of tongue contact with spout. I-R-postlesion. In I and J, rat tapped drinking tube with front of snout. K-Rdrinking behavior. Note drift of head upward, away from spout and inaccuracy of tongue placement. Tongue never contacted spout as indicated by drop of water which hangs undisturbed from tip of tube. To increase contrast, the tip of the nose and the upper portion of the aperture have been outlined, in the photograph, with black ink.
RAT 201: POST-LESION
102
LABUSZEWSKI
ET AL.
grooming or exploratory behavior. When licking was resumed after a pause, the orienting behavior characterized by sniffing and nose tapping was typically not observed. Such responses were seen only at the beginning of the session. Frame by frame analysis of filmed sequences of ingestive behavior revealed a number of characteristics of licking that could not easily be detected in other ways. All animals displayed almost imperceptible rhythmic movements of the head and body that were time-locked to the activity of the tongue. As the tongue was extended from the mouth, both head and body rocked forward; after contact with the drinking tube, head and body moved backward as the tongue returned into the mouth. In addition, the path of the tongue’s movement during a lick bore an almost constant relationship to the position of the head (Fig. 3). Therefore, the accuracy of licking was largely determined by correct head orientation. Licking speed and the duration of the tongue’s contact with the drinking tube showed little variability as illustrated in the distributions calculated from the drinkometer output (Figs. 4, 5). The magnitude of these measures of licking varied with changes in the accessibility of the drinking tube. In comparison with conditions in which the tube was relatively easy to reach (Fig. 4, “spout not recessed”), interlick intervals increased when the tube was made less accessible (Fig. 4, “spout recessed”). Lick durations decreased as the drinking tube was made more difficult to reach (Fig. 5, “spout not recessed” vs “spout recessed”). For a given spout position, interlick interval and lick duration distributions varied little from day to day in each animal. Normal Rats-Moving Spout. On separate trials, the starting position of the spout was either the center, extreme left, or extreme right of the aperture. Regardless of spout position, typical orienting behavior was displayed at each new position (sniffing and nose tapping). When the animal licked successfully for several seconds, the spout was moved laterally at a speed of 2 mm/s for distances from 5 to 15 mm. Normal rats were able to accurately lick the moving drinking tube by tracking it with integrated movements of head and body. As the spout neared either the left or right extreme of the aperture, large postural adjustments were made without interruption of ongoing accurate licking (Fig. 6). GP Rats-Stationary Spout. The GP animals had great difficulty licking the spout when it was recessed through the aperture in the test chamber wall. Prior to lesion, the rats were shaped to lick the recessed spout by gradually withdrawing the tube 1 to 2 mm/day, starting from a position within the chamber and ending with the tip of the spout 5 mm outside the chamber. Normal rats all acquired this behavior within 6 days. Animals with GP lesions took significantly longer to learn to lick the recessed spout
POSTURAL
DEFICITS
FROM PALLIDAL
loo
>I50 t35
103
LESIONS
cn30 Y 0
535
INTER-LICK
INTERVAL
loo
>I50
(MSEC)
FIG. 4. Distributions of interlick intervals (time elapsing from end of a lick until the beginning of the next lick) for two animals prelesion (open histograms) and after bilateral globus pallidus lesions (solid histograms). Note changes in histograms postlesion and increased variability in the distributions postlesion in the spout “not recessed” position. The increased variability was probably due to increased contact with the spout by other body parts after the lesion. Prelesion, the animal primarily touched the spout only with the tongue. Postlesion, the animal seemed to try to maintain contact with the spout with the nose or paws, while drinking. This was easily done in the unrecessed spout position, and probably accounted for the longer intervals and increased variability.
(mean 16 days, P < 0.01). In addition, some GP animals (three of nine) were never able to consistently lick the spout when it was recessed more than 4 mm; all normal animals could lick with the spout recessed 5 mm. Those animals which did not steadily lick when the spout was recessed beyond 4 mm, however, extended the tongue quite far. This was evidenced by the fact that when the spout was recessed 5 mm, they were able to occasionally contact the tube with the tongue. After 50 to 100 accurate licks (and many more which missed), these animals simply stopped responding. Attempts to reinstate licking by increasing food deprivation were not successful. Interlick interval distributions for GP rats differed markedly from prele-
104
LABUSZEWSKI SPOUT
ET AL.
RECESSED
SPOUT NOT RECESSED
RAT
RAT
I
205
IL-l100&k 50
LICK
DURATION
100
(MSEC)
FIG. 5. Distributions of durations of tongue contact with the spout (for unrecessed and recessed spout positions) for two animals, before (open histograms) and after (solid histograms) bilateral globus pallidus lesions. Note changes in mean durations after lesion and increased variability in durations after lesion in the “spout not recessed” position. The increased variability was probably due to increased contact of body parts (other than the tongue) with the spout, as explained in Fig. 3.
sion data (Fig. 4). Postoperatively, the animals showed longer intervals than normal when the tube was difficult to reach and abnormally short intervals when the tube was readily accessible. Lick duration distributions were also affected (Fig. 5). Animals with lesions had shorter than normal durations when the spout was recessed and longer than normal durations when the spout was not recessed. In addition, variability was increased postoperatively in both the interval and also the duration distributions. The abnormal interval and duration distributions as well as the aforementioned difficulty of animals with lesions in reaching the recessed spout suggested buccolingual motor problems. However, direct observation of GP animals’ ingestion patterns suggested that the major source of their difficulties lay elsewhere. The GP lesion rats, like normal rats, approached the aperture, sniffed
POSTURAL
DEFIClTS
FROM PALLIDAL
LESIONS
105
FIG. 6. Diagrams of rats’ position when drinking. A-body and head position of normal rat when spout is centered and recessed. B and C-the postural adjustments the normal rat makes while tracking the spout as it moves to the extreme left and right positions shown. The animal makes these adjustments while continuously licking, with no problems. D-the head and body position of an animal with bilateral globus pallidus lesions, when the spout is centered and recessed. E and F-the typical response of the animal with lesion to the moving spout. The head moves in the appropriate direction, without the concomitant body adjustments that make licking possible. Abbreviations: C.W.-cage wall, D.T.-drinking tube.
or tapped the spout with the nose, positioned head and body, and then began to lick. It was at this point that grossly abnormal behavior first became evident. Licking was either off-target from the beginning (Fig. 3) or, if initiated accurately, rapidly drifted off target. This deficit was not due to abnormalities in the control of the tongue. The path of tongue movement with respect to the head, the degree of tongue extension, and speed of licking were within normal limits as revealed in frame by frame analysis of filmed sequences of licking. Rather, inaccuracies of tongue movement were primarily due to incorrect positioning of the head. Bouts of licks that missed the spout from the outset resulted from the animals’ failure to correctly align the head with the drinking tube after orienting behavior. Licking that was initially accurate became inaccurate because the animals failed to stabilize the head in the appropriate orientation. A salient feature of the GP syndrome in all lesion rats was an inability to stabilize the head during licking; the head gradually drifted to a position
106
LABUSZEWSKI
ET AL.
from which it was impossible to contact the spout with the tongue (Fig. 3). The GP animals were never observed to correct inaccuracies during an ongoing burst of licks. Instead, the animal would make 5 to 10 unrewarded licks and then pause. Before attempting to lick again, the animal once more engaged in orienting behavior. This sequence of activities stands in marked contrast to that of normal rats. Their very occasional inaccuracies of licking were corrected during an ongoing burst. Orienting behavior was observed only at the beginning of the test session with normal animals. With the exception of the problems involving head movement, frame by frame analysis revealed no other obvious abnormalities. In addition to the seemingly normal tongue movements cited above, the rhythmic rocking movements of the head and body which were time-locked to the lick cycle were also undisturbed by GP lesions. However, many animals with lesions assumed bizarre postures while drinking, an observation that has been made previously by other investigators (10). GP Rats-Moving Spout. Animals with GP lesions, although showing many components of normal tracking, failed to accurately lick the moving spout. These animals verified the starting position of the spout with normal nose tapping and sniffing activities. Spout displacement triggered head movements which were in the appropriate direction. However, invariably these tracking movements were started too late and were of insufficient speed to keep up with the moving tube. In addition to the problems with head movement, difficulties involving movements of the trunk were also observed. As noted above, normal animals typically readjusted the position of the body when the spout had moved into a new position. In contrast, when a GP lesion rat had settled into a particular body posture at the start of the test session, it failed to readjust this posture regardless of changes in the spout’s position (Fig. 6). DISCUSSION The primary difficulty evidenced by rats with GP lesions involved the control of postural movements. Animals with lesions could neither accurately position nor stabilize the head during licking. Consequently, the head was not aligned correctly with the drinking tube and tongue movements were off-target. Movements involving the head were not the only ones affected by GP damage. Animals with lesions adopted bizarre body postures during drinking and failed to adjust the position of the trunk during tracking behavior. These postural difficulties were observed against a background of movement that was essentially devoid of abnormalities. Movements of the tongue
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
107
as well as rhythmic rocking of the head and body during licking seemed normal. Moreover, limb movement and posture during locomotion and grooming appeared undisturbed. Indeed, head movements during grooming and locomotion also seemed quite normal. Therefore, the problems with postural movement could not be attributed to any simplistic motor deficit. The present results do not rule out some role of the GP in movements of the jaw and tongue. During the early phase of recovery of feeding behavior after lesions, GP animals spilled large quantities of food while chewing. These deficits were probably due to an inability to manipulate the food with the tongue, lips, and jaws while eating. At the time that animals with lesions were formally tested they were maintaining their body weight and such deficits may no longer have been present. Some aspects of the GP lesion rats’ behavior were suggestive of sensory loss; when licking was off-target, rats with lesions continued to lick the air seemingly oblivious of the fact that their tongues did not touch the drinking tube. However, several observations rule out sensory deficits as an explanation. The GP lesion animals were clearly sensitive to somatosensory inputs as indicated by their vigorous head movements elicited by tactile stimulation of the face during force-feeding. In spite of inability of animals with lesions to stabilize their heads, they were able to discriminate between movements of the drinking tube and those of their head during tracking; movement of the spout triggered appropriately directed head movements. Moreover, lesions in the VPM, the thalamic component of the lemniscal system, surely produced somatosensory problems in control rats but resulted in none of the postural impairments experienced by rats with GP lesions. The deficits of postural movements were not general to all types of postural activities. Antigravity responses during a variety of behaviors (e.g., standing, walking, grooming) were normal. Only those postural movements which served to provide an operating base for accurate tongue movements were impaired. A distinguishing characteristic of these movements was the constellation of sensory stimuli which control them. Specifically, correct orientation of the head and body can be programmed based on olfactory and tactile signals generated by the orienting behavior (sniffing and tapping the spout with the nose) which precedes licking. Success of head positioning is signaled by the gustatory and somatosensory stimulation caused by the tongue contacting the spout during subsequent licking. Animals with GP lesions seemed unable to use this type of sensory input to program movements which would appropriately situate the animal for licking. The preceding interpretation of the data suggests that the GP mediates the feedback-modulated postural targeting movements necessary for ingestion. If this supposition is correct, then presumably the basal ganglia would
108
LABUSZEWSKl
ET AL.
have access to the types of sensory information which guide such movements. The results of acute and chronic electrophysiological studies demonstrated that, at least with regard to the somatosensory modality, the basal ganglia are influenced by such input. Neurons in the striatum (14), globus pallidus ( 12), entopeduncular nucleus (13), and substantia nigra (8) were all highly responsive to tactile stimulation applied to the face. Furthermore, striatal units in behaving animals had response properties that suggest the encoding of a stimulus’s relative position on the face with respect to the front of the mouth. Such cells had large receptive fields which always included perioral tissue. When stimulation was applied within various portions of the receptive field, the largest responses were always evoked at the front of the mouth. Some cells were responsive only to moving tactile stimulation; stimuli which moved along a path directed toward the front of the mouth evoked enhanced responding (23). Information of this nature clearly would be important to a neural system which is involved in programming the postural movements that enable ingestion. The movement deficits described in this paper may be indicative of a particular relationship between basal ganglia functioning and control of the proximal and axial muscles. Anatomic, electrophysiologic, and clinical findings also are suggestive of such a relationship. The preponderance of corticostriatal afferent fibers from motor cortex originate in regions which control proximal muscles (6). A higher proportion of striatal and GP units changed firing rate during postural adjustments (2) rather than limb movements (4). In addition, virtually all movement disorders associated with basal ganglia pathology in humans are characterized by abnormal postural control as a primary symptom (18). A primary basal ganglia involvement in the control of certain kinds of postural movement would explain several interesting experimental observations. As pointed out by Anderson (2), the greater proportion of striatal neurons which seemed related to ramp movements (5) could be attributed to the greater involvement of proximal muscles in such movements. The paradoxical responses of GP neurons which showed activity related to both limb and mouth movements (21) may have been due to the postural activities common to both limb and mouth responses. Finally, the bizarre head and body positions adopted by rats with GP lesions during licking (see Results) would also be explicable. Similar types of movement patterns are shown by humans with basal ganglia disorders. These responses reinforce labyrinthine and proprioceptive inputs and are typically adopted by patients with Parkinson’s disease as a strategy for gaining control of postural reflexes ( 18). It would not be implausible to assume that rats with GP lesions use similar responses to achieve postural fixation. The present findings suggest that involvement in ingestion is not a unique
POSTURAL
DEFICITS
FROM
PALLIDAL
LESIONS
109
aspect of basal ganglia motor functioning. Rather, the unifying theme of postural control is’common to the basal ganglia’s role in both limb and also oropharyngeal movements. As a result, further insights into the nature of basal ganglia-oropharyngeal interactions should be relevant to understanding the more general role of the basal ganglia in motor processes. REFERENCES 1. ALBERT, D. J.. L. H. STORLIEN, D. J. WOOD, AND G. K. EHMAN. 1970. Further evidence for a complex system controlling feeding behavior. Physiol. Behav. 5: 1075-1082. 2. ANDERSON, M. E. 1977. Discharge patterns of basal ganglia neurons during active maintenance of postural stability and adjustment to chair tilt. Bruin Rex 143: 325-338. 3. BIGNALL, K. E., AND L. SCHRAM. 1974. Behavior of chronically decerebrated kittens. Exp. Neural. 42: 519-531. 4. DELONG, M. R. 1971. Activity of pallidal neurons during movement. J. Neurophysiol. 34.414-427. 5. DELONG, M. R., AND P. L. STRICK. 1974. Relation of basal ganglia, cerebellum and motor cortex units to ramp and ballistic limb movements. Brain Res. 71: 327-335. 6. GARCIA-RILL, E., A. NIETO, A. ADINOLFI, C. D. HULL, AND N. A. BUCHWALD. 1979. Projections to the neostriatum from the cat precruciate cortex. Anatomy and physiology. Brain Res. 170: 393-407. 7. GRILL, H. J. 1980. Production and regulation of ingestive consummatory behavior in the chronic decerbrate rat. Brain Res. Bull. (Suppl. 4) 5: 79-87. 8. HARPER, J. A., T. LABUSZEWSKI, AND T. I. LIDSKY. 1979. Trigeminal influences upon the substantia nigra. Exp. Neurol. 65: 462-470. 9. LENARD, L., J. SARKISIAN, AND 1. SZABO. 1975. Sex-dependent survival of rats after bilateral pallidal lesions. Physiol. Behav. 15: 389-397. 10. LEVINE, M. S., N. FERGUSON,C. J. KREINICK, J. W. GUSTAFSON, AND J. S. SCHWARTZBAUM. 197 1. Sensorimotor dysfunctions and aphagia and adipsia following pallidal lesions in rats. J. Comp. Physiol. Psycho!. 77: 282-293. 1I. LEVINE, M. S., AND J. S. SCHWARTZBAUM. 1973. Sensorimotor functions of the striatopallidal system and lateral hypothalamus and consummatory behavior in rats. J. Comp. Physiol. Psychol. 85: 615-635. 12. LIDSKY, T. I., N. A. BUCHWALD. C. D. HULL, AND M. S. LEVINE. 1975. Pallidal and entopeduncular single unit activity in cats during drinking. Electroenceph. Cfin. Neurophysiol. 39: 79-84. 13. LIDSKY, T. I., J. H. ROBINSON, F. J. DENARO, AND P. M. WEINHOLD. 1978. Trigeminal influences on entopeduncular units. Brain Res. 141: 227-234. 14. LIDSKY, T. I., T. LABUSZEWSKI, M. J. AVITABLE, AND J. H. ROBINSON. 1979. The effects of stimulation of trigeminal sensory afferents upon caudate units in cats. Bruin Res. Bull. 4: 9- 14. 15. MACGREGOR, S. JR., AND T. I. LIDSKY, 1977. An economical device for the microanalysis of licking. Physiol. Behav. 18: 549-550. 16. MARSHALL, J. F., B. H. TURNER, AND P. TEITELBAUM. 197 I. Sensory neglect produced by lateral hypothalamic damage. Science 174: 523-525. 17. MARSHALL, J. F., J. S. RICHARDSON, AND P. TEITELBAUM. 1974. Nigrostriatal bundle damage and the lateral hypothalamic syndrome. J. Comp. Physiof. Psychol. 8’7: 808830. 18. MARTIN, J. P. 1967. The Bosul Ganglia and Posture. Lippincott, Philadelphia.
110
LABUSZEWSKI
ET AL.
L. 0. 1927. The corpus striatum. A study of secondary degenerations following lesions in man and of symptoms and acute degenerations following experimental lesions in cats. Arch. Neural. Psychiat. 18: 495-549. 20. MORGANE, P. J. 1961. Alterations in feeding and drinking behavior of rats with lesions in globi pallidi. Am. J. Physiol. 201: 420-428. 21. NEAFSEY, E. J., C. D. HULL, AND N. A. BUCHWALD. 1978. Preparation for movement in the cat. II. Unit activity in the basal ganglia and thalamus. Electroenceph. C/in. Neurophysiol. 44: 7 14-723. 22. NEILL, D. B., AND C. L. LINN. 1975. Deficits in consummatory responses to regulatory challenges following basal ganglia lesions in rats. Physiol. Behav. 14: 617-624. 23. SCHNEIDER, J. S., AND T. I. LIDSKY. 1981. Processing of somatosensory information in the striatum of behaving cats. J. Neurophysiol. 45: 841-851. 19.
MORGAN,
NEUROLOGY
74, 93-110 (1981)
Role of Postural Deficits in Oro-Ingestive Problems by Globus Pallidus Lesions
Caused
T. LABUSZEWSKI, R. LOCKWOOD, F. E. MCMANUS, L. R. EDELSTEIN. AND T. I. LIDSKY’ Department of Psychology, State University of New York, Stony Brook, New York 11794 Received January 15. 1981: revision received April 21. 1981 There is a large literature demonstrating that rats with globus pallidus lesions have ingestional problems. In an effort to understand the bases of these deficits, the ingestional activity of normal and brain-damaged animals was subjected to scrutiny. Rats were trained to lick a spout recessed behind a Plexiglas wall for 8% sucrose solution. The characteristic interlick interval and lick duration distributions observed in normal animals were severely disrupted by globus pallidus lesions. This disturbance was, in large part, due to an inability to correctly position the mouth with respect to the spout and maintain that position for a burst of licks, activities which normally ensure consistently efficient ingestion. After pallidal lesions, animals often miss the spout altogether. When they do find the spout, only the first few licks are on target. The head then drifts away from the correct position and subsequent licks miss the spout. Animals’ ability to continue licking during slow lateral displacement of the spout was also tested. Animals with pallidal lesions showed severe deficits. In addition to problems with head positioning, pallidal animals failed to adapt their body posture to enable licking at different spout locations. In relation to clinical and experimental findings, these data implicate the basal ganglia in feedback-regulated control of axial and proximal muscles.
INTRODUCTION The most striking behavioral effect of globus pallidus (GP) lesions in rats and cats is a disruption of ingestion lasting a few days to several weeks ( 19, 20). In view of the vast literature which implicates the basal ganglia Abbreviations: GP-globus pallidus, VPM-ventralis posteromedialis. ’ The authors gratefully acknowledge B. Federchuck and D. Lederman for assistance in early phases of the experiment and also A. Castaldi, J. Lavery, and G. Sintchak for superb technical help. Please address all reprint requests to T. Lidsky. This research was supported by U.S. Public Health Service grants NS 15328 and NS 16054. 93 0014-4886/81/100093-18$02.00/0 Copyright 0 1981 by Academic Press, Inc. All rights of reproduction in any form reserved.
94
LABUSZEWSKI
ET AL.
in the control of movement, it seems plausible that GP lesion-induced aphagia and adipsia may be due to motor problems. Therefore, it is surprising that although the ingestion problems of GP-damaged animals have been investigated in a variety of ways [e.g., (1, 9, 22)], few studies directly assessed motor capabilities as they apply to oro-ingestive behavior. However, several observations in the course of research addressed to other characteristics of the GP lesion syndrome, suggested movement difficulties. Animals with lesions appeared unable to fully extend the tongue while drinking and seemed unable or unwilling to bite with normal force (17). These observations, although indicating that movement problems might underlie the ingestion disturbance in GP animals, also are rather problematic. It is difficult to understand why GP lesions disturbed licking and chewing inasmuch as these basic movement patterns are organized in the brain stem and can proceed in a normal fashion despite the absence of the entire forebrain including the basal ganglia (3, 7). To better assess the motoric basis of aphagia and adipsia and to eventually proceed beyond the general category of “motor” to a more precise understanding of the processes mediated by the GP, it is necessary to obtain a detailed description of the changes in motor patterns caused by damage in this brain region. To do this, methodologies are required which are tailored to the relatively rapid temporal characteristics of ingestive behavior. It was the aim of the present work to provide some of this descriptive information. METHODS The experiments used male albino rats weighing 220 to 240 g at the commencement of testing. The animals were their own controls: observations made prior to surgery were compared with observations of that same animal’s behavior after it had received the lesion. Using standard stereotaxic techniques, electrolytic lesions were made in the GP of nine rats. Because the gustatory thalamocortical projection originating in nucleus ventralis posteromedialis (VPM) traverses the GP (1 l), the VPM was lesioned in five additional animals to control for the effects of damaging these fibers of passage. Testing Procedures. To assess licking behavior, rats were placed in a Plexiglas cage (L: 30 cm, W: 26 cm, H: 20 cm) in which a 2-cm diameter hole in one wall allowed access to a stainless-steel tube from which an 8% sucrose solution was continuously available. To ensure that animals drank steadily throughout the 16-min test session, they were reduced to 90% of ad libitum weight and maintained to gain 5 g/week. The drinking tube was mounted on a rack and pinion device which allowed the tube to be
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
95
recessed through the hole in the cage wall. Observations were made when the tube was recessed between 0 and 5 mm with respect to the outside surface of the Plexiglas wall and the center of the aperture. Because of the orientation of the spout with respect to the hole in the cage wall, the animals had to assume a head position during drinking which prevented them from seeing the spout (Fig. 3). The drinking tube was also mounted on a lead screw and positioned perpendicular to its longitudinal axis (Fig. 1). The lead screw was attached to a DC digital stepping motor. Activation of this motor caused smooth lateral movement of the drinking tube and was used to assess the rat’s tracking ability. Stepping speed, number of steps, and step direction were all controlled by the experimenter to obtain lateral drinking tube displacements of reproducible velocity, magnitude, and direction. Tracking ability was tested in a subgroup composed of five GP and three VPM animals. Data concerning the characteristics of individual licks were obtained with a specially designed drinkometer (15) which signaled both when the animal’s tongue first contacted the drinking tube and also the duration of tongue-tube contact. Current passed by this device was considerably less than the ~-IA minimum which can be sensed by rats. The behavior (e.g., head position, body posture, etc.) was observed directly for every animal during all test sessions. To verify and make a more permanent record of these observations, the actions of five GP and three VPM rats were filmed before and after placing the lesions. Several different camera angles were used with each rat to record accuracy of head and body position as well as tongue movement. Filming speed varied with the behavior to be filmed and ranged from 18 to 36 frames per second. Data Analysis. All drinkometer data were stored on tape for later anal-
FIG. I. Schematic of moveable drinking tube used to assesstracking behavior. Shown is a top view and only the front portion of the test chamber is included. Arrows indicate possible directions of drinking tube movement. Abbreviations: A-aperture; C.W.-cage wall, D.T.drinking tube, G.F.-grid floor, L.S.-lead screw, R. & P.-rack and pinion device, S.M.stepping motor.
96
LABUSZEWSKI
ET AL.
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
98
LABUSZEWSKI
ET AL.
ysis by a laboratory computer (Cromemco Corp). Lick duration was defined as the period beginning with the tongue contacting the drinking tube and ending when contact was broken. Interlick interval was the time elapsed between the tongue breaking contact with the drinking tube and making contact again on successive licks. Population histograms of lick durations and interlick intervals were calculated with associated means and standard deviations. Filmed sequences were assessed with standard frame by frame analysis. At the completion of testing, the animals were deeply anesthetized and perfused with formol-saline. The brains were sectioned (40pm) and stained with cresyl violet for histological analysis. RESULTS Histology. The data presented below describing the effects of pallidal damage were derived from observations of animals with bilateral lesions in the GP. In all cases, more than 50% of the GP was destroyed on each side. Other regions damaged by these lesions were the internal capsule and the neostriatum. However, extrapallidal damage was typically quite minor (Fig. 2) and varied from animal to animal particularly with regard to bilaterality. In addition to the nine rats with bilateral GP lesions, two rats had only unilateral GP damage. These unilaterally operated animals showed none of the ingestional difficulties described in the following paragraphs. Thus, behavioral effects were correlated with bilateral destruction of the GP. Animals included in the VPM group had large thalamic lesions which destroyed at least 75% of the VPM. In three of the five rats, the lesion extended dorsally to cause substantial (20 to 40%) damage in the centre medianurn. Slight unilateral damage to the medial portion of nucleus ventralis pasterolateralis was also caused in two rats. The sequelae of thalamic damage observed in the ingestional testing were associated only with VPM damage. Acute Effects of Lesions. GP animals showed transient aphagia and adipsia lasting from several days to several weeks. The precise point at which animals resumed ingestion was difficult to specify because food and water were always available in the home cage. Unless an animal was actually seen to be eating or drinking, decreases in the amount of food or water present could have been due to spillage and evaporation. To facilitate recovery, the animals were given palatable foods (e.g., chocolate chip cookies) in an easily chewable form (wet mash) in addition to the normal supply of pellet food. During the period of aphagia and adipsia, GP rats always showed considerable interest in the cookie mash. When a fresh supply was put in the cage, the animal typically came over to the dish to investigate although it did not eat.
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
99
If aphagia and adipsia lasted more than 2 days, GP animals were maintained by forcing liquified food into the back of the mouth with a plastic tube and syringe. Food introduced in this way elicited licking, chewing, and swallowing. This reflexive licking and chewing were of seemingly normal speed and vigor, although quantitative measures were not taken. Tactile stimulation of the perioral and intraoral tissue during forced feeding caused the animals to turn away from the plastic tube. These animals showed no signs of sensory neglect (16). However, when GP animals first began to eat of their own volition, they exhibited considerable difficulty in efficiently manipulating the food with the mouth as evidenced by the large quantities of food which were dropped during chewing. This problem gradually disappeared during the next few days. During the entire period of aphagia and adipsia, GP animals did not groom. This behavior reappeared in conjunction with eating and drinking. After GP animals recovered sufficiently to increase their body weights beyond preoperative levels, there were no obvious lasting signs of brain damage (except those noted during formal testing for ingestion behaviorsee below). At this time, animals were given food only in pellet form and ingestion patterns in the home cage were normal. Posture, locomotion, grooming, and other movement patterns were apparently normal. VPM animals were neither aphagic nor adipsic and experienced no weight losses. However, these animals initially displayed problems in efficiently manipulating food with the mouth which were similar to the problems of GP animals. As with GP lesions, food spillage lasted only a few days. In contrast to animals with GP lesions, VPM animals began grooming within hours of recovery from anesthesia. Ingestive behavior was tested both prior to surgery and also after recovery from the acute effects of lesions. Rats with VPM lesions showed no abnormalities during ingestion testing. Therefore, to facilitate description of lesion-induced deficits, behavior of GP rats will be contrasted only with that of normal rats. Normal Rats-Stationary Spout. At the beginning of the test session, each animal exhibited similar patterns of orientational activity. The rat approached the aperture in the Plexiglas wall, sniffed, and then tapped the tip of the drinking tube with the tip of the nose. Immediately afterward, the rat positioned itself close to the aperture and began to lick. In the large majority of cases, the initial licks were on target (Fig. 3); however, if the first lick missed the drinking tube, the animal made slight adjustments of head position so that subsequent licks were accurate. Animals typically licked continuously for the first half of the test session. For the remainder of the period, bursts of licking (- 30 s) were interspersed with bouts of
RAT 201: PRE-LESION A
8
B
C
FIG. 3. Filmed sequences of licking behavior before and after globus pallidus lesions. Spout is recessed. A-prelesion. Note relative invariance of head position and accuracy of tongue contact with spout. I-R-postlesion. In I and J, rat tapped drinking tube with front of snout. K-Rdrinking behavior. Note drift of head upward, away from spout and inaccuracy of tongue placement. Tongue never contacted spout as indicated by drop of water which hangs undisturbed from tip of tube. To increase contrast, the tip of the nose and the upper portion of the aperture have been outlined, in the photograph, with black ink.
RAT 201: POST-LESION
102
LABUSZEWSKI
ET AL.
grooming or exploratory behavior. When licking was resumed after a pause, the orienting behavior characterized by sniffing and nose tapping was typically not observed. Such responses were seen only at the beginning of the session. Frame by frame analysis of filmed sequences of ingestive behavior revealed a number of characteristics of licking that could not easily be detected in other ways. All animals displayed almost imperceptible rhythmic movements of the head and body that were time-locked to the activity of the tongue. As the tongue was extended from the mouth, both head and body rocked forward; after contact with the drinking tube, head and body moved backward as the tongue returned into the mouth. In addition, the path of the tongue’s movement during a lick bore an almost constant relationship to the position of the head (Fig. 3). Therefore, the accuracy of licking was largely determined by correct head orientation. Licking speed and the duration of the tongue’s contact with the drinking tube showed little variability as illustrated in the distributions calculated from the drinkometer output (Figs. 4, 5). The magnitude of these measures of licking varied with changes in the accessibility of the drinking tube. In comparison with conditions in which the tube was relatively easy to reach (Fig. 4, “spout not recessed”), interlick intervals increased when the tube was made less accessible (Fig. 4, “spout recessed”). Lick durations decreased as the drinking tube was made more difficult to reach (Fig. 5, “spout not recessed” vs “spout recessed”). For a given spout position, interlick interval and lick duration distributions varied little from day to day in each animal. Normal Rats-Moving Spout. On separate trials, the starting position of the spout was either the center, extreme left, or extreme right of the aperture. Regardless of spout position, typical orienting behavior was displayed at each new position (sniffing and nose tapping). When the animal licked successfully for several seconds, the spout was moved laterally at a speed of 2 mm/s for distances from 5 to 15 mm. Normal rats were able to accurately lick the moving drinking tube by tracking it with integrated movements of head and body. As the spout neared either the left or right extreme of the aperture, large postural adjustments were made without interruption of ongoing accurate licking (Fig. 6). GP Rats-Stationary Spout. The GP animals had great difficulty licking the spout when it was recessed through the aperture in the test chamber wall. Prior to lesion, the rats were shaped to lick the recessed spout by gradually withdrawing the tube 1 to 2 mm/day, starting from a position within the chamber and ending with the tip of the spout 5 mm outside the chamber. Normal rats all acquired this behavior within 6 days. Animals with GP lesions took significantly longer to learn to lick the recessed spout
POSTURAL
DEFICITS
FROM PALLIDAL
loo
>I50 t35
103
LESIONS
cn30 Y 0
535
INTER-LICK
INTERVAL
loo
>I50
(MSEC)
FIG. 4. Distributions of interlick intervals (time elapsing from end of a lick until the beginning of the next lick) for two animals prelesion (open histograms) and after bilateral globus pallidus lesions (solid histograms). Note changes in histograms postlesion and increased variability in the distributions postlesion in the spout “not recessed” position. The increased variability was probably due to increased contact with the spout by other body parts after the lesion. Prelesion, the animal primarily touched the spout only with the tongue. Postlesion, the animal seemed to try to maintain contact with the spout with the nose or paws, while drinking. This was easily done in the unrecessed spout position, and probably accounted for the longer intervals and increased variability.
(mean 16 days, P < 0.01). In addition, some GP animals (three of nine) were never able to consistently lick the spout when it was recessed more than 4 mm; all normal animals could lick with the spout recessed 5 mm. Those animals which did not steadily lick when the spout was recessed beyond 4 mm, however, extended the tongue quite far. This was evidenced by the fact that when the spout was recessed 5 mm, they were able to occasionally contact the tube with the tongue. After 50 to 100 accurate licks (and many more which missed), these animals simply stopped responding. Attempts to reinstate licking by increasing food deprivation were not successful. Interlick interval distributions for GP rats differed markedly from prele-
104
LABUSZEWSKI SPOUT
ET AL.
RECESSED
SPOUT NOT RECESSED
RAT
RAT
I
205
IL-l100&k 50
LICK
DURATION
100
(MSEC)
FIG. 5. Distributions of durations of tongue contact with the spout (for unrecessed and recessed spout positions) for two animals, before (open histograms) and after (solid histograms) bilateral globus pallidus lesions. Note changes in mean durations after lesion and increased variability in durations after lesion in the “spout not recessed” position. The increased variability was probably due to increased contact of body parts (other than the tongue) with the spout, as explained in Fig. 3.
sion data (Fig. 4). Postoperatively, the animals showed longer intervals than normal when the tube was difficult to reach and abnormally short intervals when the tube was readily accessible. Lick duration distributions were also affected (Fig. 5). Animals with lesions had shorter than normal durations when the spout was recessed and longer than normal durations when the spout was not recessed. In addition, variability was increased postoperatively in both the interval and also the duration distributions. The abnormal interval and duration distributions as well as the aforementioned difficulty of animals with lesions in reaching the recessed spout suggested buccolingual motor problems. However, direct observation of GP animals’ ingestion patterns suggested that the major source of their difficulties lay elsewhere. The GP lesion rats, like normal rats, approached the aperture, sniffed
POSTURAL
DEFIClTS
FROM PALLIDAL
LESIONS
105
FIG. 6. Diagrams of rats’ position when drinking. A-body and head position of normal rat when spout is centered and recessed. B and C-the postural adjustments the normal rat makes while tracking the spout as it moves to the extreme left and right positions shown. The animal makes these adjustments while continuously licking, with no problems. D-the head and body position of an animal with bilateral globus pallidus lesions, when the spout is centered and recessed. E and F-the typical response of the animal with lesion to the moving spout. The head moves in the appropriate direction, without the concomitant body adjustments that make licking possible. Abbreviations: C.W.-cage wall, D.T.-drinking tube.
or tapped the spout with the nose, positioned head and body, and then began to lick. It was at this point that grossly abnormal behavior first became evident. Licking was either off-target from the beginning (Fig. 3) or, if initiated accurately, rapidly drifted off target. This deficit was not due to abnormalities in the control of the tongue. The path of tongue movement with respect to the head, the degree of tongue extension, and speed of licking were within normal limits as revealed in frame by frame analysis of filmed sequences of licking. Rather, inaccuracies of tongue movement were primarily due to incorrect positioning of the head. Bouts of licks that missed the spout from the outset resulted from the animals’ failure to correctly align the head with the drinking tube after orienting behavior. Licking that was initially accurate became inaccurate because the animals failed to stabilize the head in the appropriate orientation. A salient feature of the GP syndrome in all lesion rats was an inability to stabilize the head during licking; the head gradually drifted to a position
106
LABUSZEWSKI
ET AL.
from which it was impossible to contact the spout with the tongue (Fig. 3). The GP animals were never observed to correct inaccuracies during an ongoing burst of licks. Instead, the animal would make 5 to 10 unrewarded licks and then pause. Before attempting to lick again, the animal once more engaged in orienting behavior. This sequence of activities stands in marked contrast to that of normal rats. Their very occasional inaccuracies of licking were corrected during an ongoing burst. Orienting behavior was observed only at the beginning of the test session with normal animals. With the exception of the problems involving head movement, frame by frame analysis revealed no other obvious abnormalities. In addition to the seemingly normal tongue movements cited above, the rhythmic rocking movements of the head and body which were time-locked to the lick cycle were also undisturbed by GP lesions. However, many animals with lesions assumed bizarre postures while drinking, an observation that has been made previously by other investigators (10). GP Rats-Moving Spout. Animals with GP lesions, although showing many components of normal tracking, failed to accurately lick the moving spout. These animals verified the starting position of the spout with normal nose tapping and sniffing activities. Spout displacement triggered head movements which were in the appropriate direction. However, invariably these tracking movements were started too late and were of insufficient speed to keep up with the moving tube. In addition to the problems with head movement, difficulties involving movements of the trunk were also observed. As noted above, normal animals typically readjusted the position of the body when the spout had moved into a new position. In contrast, when a GP lesion rat had settled into a particular body posture at the start of the test session, it failed to readjust this posture regardless of changes in the spout’s position (Fig. 6). DISCUSSION The primary difficulty evidenced by rats with GP lesions involved the control of postural movements. Animals with lesions could neither accurately position nor stabilize the head during licking. Consequently, the head was not aligned correctly with the drinking tube and tongue movements were off-target. Movements involving the head were not the only ones affected by GP damage. Animals with lesions adopted bizarre body postures during drinking and failed to adjust the position of the trunk during tracking behavior. These postural difficulties were observed against a background of movement that was essentially devoid of abnormalities. Movements of the tongue
POSTURAL
DEFICITS
FROM PALLIDAL
LESIONS
107
as well as rhythmic rocking of the head and body during licking seemed normal. Moreover, limb movement and posture during locomotion and grooming appeared undisturbed. Indeed, head movements during grooming and locomotion also seemed quite normal. Therefore, the problems with postural movement could not be attributed to any simplistic motor deficit. The present results do not rule out some role of the GP in movements of the jaw and tongue. During the early phase of recovery of feeding behavior after lesions, GP animals spilled large quantities of food while chewing. These deficits were probably due to an inability to manipulate the food with the tongue, lips, and jaws while eating. At the time that animals with lesions were formally tested they were maintaining their body weight and such deficits may no longer have been present. Some aspects of the GP lesion rats’ behavior were suggestive of sensory loss; when licking was off-target, rats with lesions continued to lick the air seemingly oblivious of the fact that their tongues did not touch the drinking tube. However, several observations rule out sensory deficits as an explanation. The GP lesion animals were clearly sensitive to somatosensory inputs as indicated by their vigorous head movements elicited by tactile stimulation of the face during force-feeding. In spite of inability of animals with lesions to stabilize their heads, they were able to discriminate between movements of the drinking tube and those of their head during tracking; movement of the spout triggered appropriately directed head movements. Moreover, lesions in the VPM, the thalamic component of the lemniscal system, surely produced somatosensory problems in control rats but resulted in none of the postural impairments experienced by rats with GP lesions. The deficits of postural movements were not general to all types of postural activities. Antigravity responses during a variety of behaviors (e.g., standing, walking, grooming) were normal. Only those postural movements which served to provide an operating base for accurate tongue movements were impaired. A distinguishing characteristic of these movements was the constellation of sensory stimuli which control them. Specifically, correct orientation of the head and body can be programmed based on olfactory and tactile signals generated by the orienting behavior (sniffing and tapping the spout with the nose) which precedes licking. Success of head positioning is signaled by the gustatory and somatosensory stimulation caused by the tongue contacting the spout during subsequent licking. Animals with GP lesions seemed unable to use this type of sensory input to program movements which would appropriately situate the animal for licking. The preceding interpretation of the data suggests that the GP mediates the feedback-modulated postural targeting movements necessary for ingestion. If this supposition is correct, then presumably the basal ganglia would
108
LABUSZEWSKl
ET AL.
have access to the types of sensory information which guide such movements. The results of acute and chronic electrophysiological studies demonstrated that, at least with regard to the somatosensory modality, the basal ganglia are influenced by such input. Neurons in the striatum (14), globus pallidus ( 12), entopeduncular nucleus (13), and substantia nigra (8) were all highly responsive to tactile stimulation applied to the face. Furthermore, striatal units in behaving animals had response properties that suggest the encoding of a stimulus’s relative position on the face with respect to the front of the mouth. Such cells had large receptive fields which always included perioral tissue. When stimulation was applied within various portions of the receptive field, the largest responses were always evoked at the front of the mouth. Some cells were responsive only to moving tactile stimulation; stimuli which moved along a path directed toward the front of the mouth evoked enhanced responding (23). Information of this nature clearly would be important to a neural system which is involved in programming the postural movements that enable ingestion. The movement deficits described in this paper may be indicative of a particular relationship between basal ganglia functioning and control of the proximal and axial muscles. Anatomic, electrophysiologic, and clinical findings also are suggestive of such a relationship. The preponderance of corticostriatal afferent fibers from motor cortex originate in regions which control proximal muscles (6). A higher proportion of striatal and GP units changed firing rate during postural adjustments (2) rather than limb movements (4). In addition, virtually all movement disorders associated with basal ganglia pathology in humans are characterized by abnormal postural control as a primary symptom (18). A primary basal ganglia involvement in the control of certain kinds of postural movement would explain several interesting experimental observations. As pointed out by Anderson (2), the greater proportion of striatal neurons which seemed related to ramp movements (5) could be attributed to the greater involvement of proximal muscles in such movements. The paradoxical responses of GP neurons which showed activity related to both limb and mouth movements (21) may have been due to the postural activities common to both limb and mouth responses. Finally, the bizarre head and body positions adopted by rats with GP lesions during licking (see Results) would also be explicable. Similar types of movement patterns are shown by humans with basal ganglia disorders. These responses reinforce labyrinthine and proprioceptive inputs and are typically adopted by patients with Parkinson’s disease as a strategy for gaining control of postural reflexes ( 18). It would not be implausible to assume that rats with GP lesions use similar responses to achieve postural fixation. The present findings suggest that involvement in ingestion is not a unique
POSTURAL
DEFICITS
FROM
PALLIDAL
LESIONS
109
aspect of basal ganglia motor functioning. Rather, the unifying theme of postural control is’common to the basal ganglia’s role in both limb and also oropharyngeal movements. As a result, further insights into the nature of basal ganglia-oropharyngeal interactions should be relevant to understanding the more general role of the basal ganglia in motor processes. REFERENCES 1. ALBERT, D. J.. L. H. STORLIEN, D. J. WOOD, AND G. K. EHMAN. 1970. Further evidence for a complex system controlling feeding behavior. Physiol. Behav. 5: 1075-1082. 2. ANDERSON, M. E. 1977. Discharge patterns of basal ganglia neurons during active maintenance of postural stability and adjustment to chair tilt. Bruin Rex 143: 325-338. 3. BIGNALL, K. E., AND L. SCHRAM. 1974. Behavior of chronically decerebrated kittens. Exp. Neural. 42: 519-531. 4. DELONG, M. R. 1971. Activity of pallidal neurons during movement. J. Neurophysiol. 34.414-427. 5. DELONG, M. R., AND P. L. STRICK. 1974. Relation of basal ganglia, cerebellum and motor cortex units to ramp and ballistic limb movements. Brain Res. 71: 327-335. 6. GARCIA-RILL, E., A. NIETO, A. ADINOLFI, C. D. HULL, AND N. A. BUCHWALD. 1979. Projections to the neostriatum from the cat precruciate cortex. Anatomy and physiology. Brain Res. 170: 393-407. 7. GRILL, H. J. 1980. Production and regulation of ingestive consummatory behavior in the chronic decerbrate rat. Brain Res. Bull. (Suppl. 4) 5: 79-87. 8. HARPER, J. A., T. LABUSZEWSKI, AND T. I. LIDSKY. 1979. Trigeminal influences upon the substantia nigra. Exp. Neurol. 65: 462-470. 9. LENARD, L., J. SARKISIAN, AND 1. SZABO. 1975. Sex-dependent survival of rats after bilateral pallidal lesions. Physiol. Behav. 15: 389-397. 10. LEVINE, M. S., N. FERGUSON,C. J. KREINICK, J. W. GUSTAFSON, AND J. S. SCHWARTZBAUM. 197 1. Sensorimotor dysfunctions and aphagia and adipsia following pallidal lesions in rats. J. Comp. Physiol. Psycho!. 77: 282-293. 1I. LEVINE, M. S., AND J. S. SCHWARTZBAUM. 1973. Sensorimotor functions of the striatopallidal system and lateral hypothalamus and consummatory behavior in rats. J. Comp. Physiol. Psychol. 85: 615-635. 12. LIDSKY, T. I., N. A. BUCHWALD. C. D. HULL, AND M. S. LEVINE. 1975. Pallidal and entopeduncular single unit activity in cats during drinking. Electroenceph. Cfin. Neurophysiol. 39: 79-84. 13. LIDSKY, T. I., J. H. ROBINSON, F. J. DENARO, AND P. M. WEINHOLD. 1978. Trigeminal influences on entopeduncular units. Brain Res. 141: 227-234. 14. LIDSKY, T. I., T. LABUSZEWSKI, M. J. AVITABLE, AND J. H. ROBINSON. 1979. The effects of stimulation of trigeminal sensory afferents upon caudate units in cats. Bruin Res. Bull. 4: 9- 14. 15. MACGREGOR, S. JR., AND T. I. LIDSKY, 1977. An economical device for the microanalysis of licking. Physiol. Behav. 18: 549-550. 16. MARSHALL, J. F., B. H. TURNER, AND P. TEITELBAUM. 197 I. Sensory neglect produced by lateral hypothalamic damage. Science 174: 523-525. 17. MARSHALL, J. F., J. S. RICHARDSON, AND P. TEITELBAUM. 1974. Nigrostriatal bundle damage and the lateral hypothalamic syndrome. J. Comp. Physiof. Psychol. 8’7: 808830. 18. MARTIN, J. P. 1967. The Bosul Ganglia and Posture. Lippincott, Philadelphia.
110
LABUSZEWSKI
ET AL.
L. 0. 1927. The corpus striatum. A study of secondary degenerations following lesions in man and of symptoms and acute degenerations following experimental lesions in cats. Arch. Neural. Psychiat. 18: 495-549. 20. MORGANE, P. J. 1961. Alterations in feeding and drinking behavior of rats with lesions in globi pallidi. Am. J. Physiol. 201: 420-428. 21. NEAFSEY, E. J., C. D. HULL, AND N. A. BUCHWALD. 1978. Preparation for movement in the cat. II. Unit activity in the basal ganglia and thalamus. Electroenceph. C/in. Neurophysiol. 44: 7 14-723. 22. NEILL, D. B., AND C. L. LINN. 1975. Deficits in consummatory responses to regulatory challenges following basal ganglia lesions in rats. Physiol. Behav. 14: 617-624. 23. SCHNEIDER, J. S., AND T. I. LIDSKY. 1981. Processing of somatosensory information in the striatum of behaving cats. J. Neurophysiol. 45: 841-851. 19.
MORGAN,