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Rigidity and Motor Attention
RIGIDITY AND MOTOR ATTENTION E. Ferrari (Clinica delle Malattie Nervose e MentaJi, Universita di Napoli)
La maladie est une experimentation de l' ordre le plus sub til, instituee par la niiture, .. . avec des procedes dont l'art humaine ne dispose pas. Th. Ribot
Under the meaningful title "The riddle of the Parkinson syndrome," Aring (1962) has very recently reviewed the difficulties encountered by all hypotheses intended to explain the physiopathological mechanism producing the Parkinson symptom-complex. As far as rigidity is concerned, however, some clinical changes following therapeutic stereotactic lesions, and recently obtained data on the neurophysiology of muscle tone (Buchwald, Heuser, Wyers and Lauprecht, 1961 ; Granit, 1955; Paillard, 1955, 1959) do suggest a new hypothesis which affords an apparently coherent interpretation: plastic rigidity appears as a malfunction, an excess of a mechanism serving to pattern body posture to subserve attentive readiness to action. If one wishes to paraphrase the classical sentence of Sherrington (1915): "Reflex tonus is postural contraction; decerebrate rigidity is reflex standing," the hypothesis proposed here can be synthetically expressed by the statement: "Parkinsonian rigidity is attentive posture." The' data supporting this interpretation are outlined under the following three headings: a) clinical observations; b) experimental findings in man; c) experimental results in animals.
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Clinical observations
Parkinson rigidity appears to the neurologist as a well defined type of hypertonicity: a) it is plastic in quality; b) it is equally distributed in agonist and antagonist muscles; c) it has the same qualities at all segmental levels. Rigidity can be topographically distributed over the entire body, or on one side only (hemisomatic). After surgical lesion of some basal ganglia areas, rigidity disappears completely in the contralateral side of the body and improves only slightly ipsilaterally. Therefore, we must say that the neuronal mechanism sustaining rigidity has a "subcortical" location and exerts tone facilitating influences which are 1) distributed mainly contralaterally to one body side; 2) "panmetameric" (i.e. affecting equally all segmental levels ); 3) "aspecific" (i.e. uniformly affecting all muscles, without regard to agonist-antagonist reciprocal innervation). Beneficial effects upon rigidity have been obtained by lesions of: 1) substantia nigra (Meyers, 1958; Meyers et aI., 1959); 2) globus pallidus (Narabayashi et aI., 1956; Spiegel and Wycis, 1956); 3) ansa lenticularis (Spiegel and Wycis, 1954, 1958; Fenelon, 1955); 4) thalamic ventrolateral nucleus (Cooper, 1961; Hassler, 1959; Krayenbiihl, Siegfried and Yasargil, 1963); 5) internal capsule (Norholm and Tygstrup, 1963). Furthermore, the exact site and size of stereotactic lesions cannot be defined with certainty, except in rare cases (Cooper, Bergmann and Caracalos, 1963; Norholm and Tygstrup, 1963) that can be, in time, verified at autopsy. Therefore, the anatomical identification of the neuronal system maintaining rigidity remains uncertain. Most probably it is not a "center" in the anatomical sense but a "system" of neurons scattered throughout several structures of the base of the brain. The lesions that affect this system and thereby improve rigidity do not cause any neurologically detectable impairment of tone regulation. This fact elicits the question of what is the "physiological" significance of a system of neurons that reveals itself only in a pathological state, and only in man, as subserving a well defined type of tone facilitation which is "panmetameric, aspecific and hemisomatic. " The data reported below suggest that the tone regulating function of this system belongs to the realm of the psychological aspects of
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motility, the "psychomotor" components, rather than to that of "neurological" motility. In particular, it serves the motor aspect of conative attention. In 1928 and 1929 Froment and coworkers had already underlined the relationships between rigidity and attention in a series of papers one of which had the significant title: "La rigidite parkinsonienne varie au bras, des que l'attention prend une direction nouvelle." Later, Claude and Baruk (1931), Denny-Brown (1962), Subczynski, Matsumoto, Hullin and Cooper (1963) noted and commented upon the facilitation of rigidity - as well as of other dystonic and dyskinetic extrapyramidal symptoms - in relation to willingness-toact. Conversely, but with identical significance, there stand out the temporary remissions or improvements of rigidity occurring when attention weakens. The most striking example of such an event is the complete effacement of Parkinsonian symptomatology under hypnosis. Disertori (1939) has described the illuminative case of an acrobat, forced by Parkinsonian rigidity to abandon his activity, who could temporarily reacquire acrobatic agility under hypnosis. Aring (1962) has recently reported similar clinical instances that stress the relationships between level of awareness and rigidity and that point to "conative attentiveness" as an essential factor for facilitation of plastic hypertonus: "conative attentiveness" appears as a component of attentive function, exclusively pertaining to "homo sapiens." Furthermore, the intensity of rigidity fluctuates in aSSOClatIOn with emotional changes, but in such a manner as to appear clearly related to attentiveness levels. In fact, emotional states, so violent and tempestuous as to release automatic motility patterns, with diminution of lucid awareness, as in panic states or in disaster situations (Aring, 1962), induce temporary but complete disappearance of Parkinson symptoms. Conversely, moderate emotional reactions, that are usually associated with augmented awareness, worsen rigidity. While all the above mentioned clinical observations demonstrate the existence of relationships between extrapyramidal rigidity and attention, they leave undetermined the significance and directness of such relations. The following data indicate that the ties between attention and plastic rigidity are strict and direct in nature.
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In first place the facies of Parkinsonism is strikingly similar, as Richter has noted, to the facial expression of attentiveness (fig. 1).
Fig. 1 -
The facies of Parkinsonism (from Andre-Thomas and Ajuriaguerra, 1951, pag. 552) is similar to the facial expression of attentiveness.
In second place, the global body posture of Parkinson patients (fig. 2c) reproduces the posture of one who, suddenly apprehending some signal of dangerous significance, automatically takes a position (startle pattern) of tense readiness to perform in any manner suitable
a Fig. 2 -
b
c
The posture of Parkinsonism (c, from Andre-Thomas and Ajuriaguerra, 1951) is similar to the "startle pattern" (b, from Landis and Hunt, 1939) and the posture of the athlete ready for motor performance (a).
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to deal with any menace, from any direction (fig. 2b). This posture is similar to that of the athlete who, in concentrated attention and conscious expectation, stays ready for a motor performance of any type, in any direction, at any moment (fig. 2a). A global patterning of muscle tone, similar to that of the above described postural situations, pathologically prevails in the "rigid" subject. The persistence of such patterning of tone distribution impedes the selective and specifically directed performance of individual motor regions, whose selective performance is, however, "per se" intact, as it reemerges in complete normality in one half of the body when a stereotactic lesion is followed by disappearance of the excessive tonic facilitation, aspecific in quality and panmetameric in distribution. In other words, all these analogies, derived from clinical observations, suggest that rigidity is the abnormally persistent plastic shaping of the motor system into a pattern that is the postural correlate of "motor attention." In support of this hypothesis we can summon the alterations of attentive function in Parkinsonian patients, as reported in psychological studies by Aubrun (1937), Veit (1927) and by Riklan et aI. (1959; 1960a, 1960b; 1961; 1962). These alterations are not a secondary consequence of rigidity; in fact they persist, and even worsen, after disappearance of rigidity following a stereotactic lesion (Proctor et al., 1963; Riklan et aI., 1960a, 1960b). Therefore, such abnormalities of attention are to be considered as the psychological consequence of lesions of the same basal ganglia neurons involved in a particular kind of tone regulation. This kind of tone regulation is not related to the specific motor performances that can be tested at a neurological examination and which remain normal after thalamic or pallidal lesions. It is, instead, a refined type of tone regulating function, a true psychomotor function (Nielsen and Thompson, 1947), inextricably tied or, better, coextensive with psychological attention and intention, i.e., motivational readiness to performance. In fact, the only defects demonstrable by psychological testing of Parkinson subjects, before and after stereotactic lesions, are in the area of the "motivational functions" (Riklan et aI., 1960b). As the physiological abnormality underlying Parkinsonian rigidity seems to involve functions that are psychomotor and not simply
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motor in nature, we must give great significance to the fact that a rigidity of this type appears only in man. Drugs capable of rapidly inducing a severe Parkinson syndrome in man, never produce rigidity in experimental animals. In our hypothesis this fact is explained as follows: conative attention is a function developed at a significant degree only in man; in a parallel manner, the specific neuronal organization, the alteration of which produces plastic rigidity, exists ·only in man in a full morphological and functional sense. Most likely, the predominantly hemisomatic and contralateral distribution of tone-facilitating effects exerted by the rigidityproducing system finds its significance in the great development reached in man by the use of the hands in motor performance; this obviously requires focussing attention to one half of the body at a time. In conclusion, the clinical characteristics of rigidity and its changes following therapeutic surgical lesions suggest the following hypothesis: "plastic" rigidity is the manifestation, at the "neurological" level, of functional derangement in a neuronal system that physiologically presides over "psychological" aspects of motor function. b) Experimental findings in man
In normal situations, the existence of relationships between attention and motor function has been proposed since the last century. Ribot, in 1889, stated that motor phenomena are "les conditions necessaires, les elements constitutifs, les facteurs indispensables de l'attention. Si l'on supprimait totalement les mouvements, on supprimerait totalement l' attention." The subject was later investigated with ingenious techniques by Courts (1939), who showed significant relations between muscle tension and learning, and Woodworth (1914) who, while studying the connection between attentive muscle tension and reaction times, clarified the concept of "motor attention." Recently Paillard (1955; 1959) has furnished excellent psychophysiological data concerning the neuromuscular correlates of attentive function derived from studies of metameric spinal cord
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physiology. Paillard's work is an extrapolation to man of Leksell's (1945) and Granit's (1955) findings in animals relative to the physiology of muscle spindles and the related gamma motoneuron system. According to Paillard, the differential analysis of mechanical stretch reflexes (initiated by direct stimulation of muscle spindles) and monosynaptic reflexes evoked by electrical stimulation of afferent fibers (thus bypassing muscle spindles) yields information on the state of excitability of the proprioceptive receptor itself: the so-called "spindle tonus" or "fusimotor tonus" expressing the gamma motoneurons' level of activity. In experiments based on such premise, Paillard has shown that the state of attentiveness has a constant somatic correlate. Fluctuations of attention are accompanied by parallel fluctuations of "spindle tonus," therefore of the gamma motoneurons' "tonic" activity. Paillard's findings and interpretation, although submitted to conceptual critique by Pinelli and Valle (1960) and to methodological critique by Landau and his coworkers (1960, 1964a, 1964b) have been confirmed by later experiments, conducted with revised technique, with findings that support the participation of the gamma motor system in attentive processes (Ferrari and Sanna, 1965). This is very important for understanding the relationship between rigidity and attention, as, in fact, disturbances of gamma function have been discovered in patients with plastic rigidity. Barraquer-Bordas (1957, 1961a, 1961b) gave the first interpretation of rigidity as an abnormal excess of tonic influences mediated by the gamma system. Rushworth (1960) experimentally confirmed this view by showing that partial procaine block of mixed nerves (which selectively blocks conduction of gamma motor fibers) causes disappearance of rigidity without loss of motor power in the corresponding muscles. Jung and Hassler (1960) believe, by contrast, that in rigidity there is a defect rather than an excess of fusimotor activity. Hassler's opinion derives from the fact that facilitation of "deep" reflexes induced by Jendrassik manoeuver - through an augmentation of fusimotor gamma activity - is absent or defective in Parkinson subjects. This proves, according to Hassler, that there is a depression of fusimotor activity (Arrigo, Cosi and Savoldi, 1963). The opposite opinions of the Spanish and the German workers have elicited a debate which is still active (Barraquer-Bordas, 1961a).
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The problem is further bemuddled by the findings of Hofmann (1962) and Angel and Hofmann (1963) who deny any alteration of the Jendrassik effect in Parkinsonism and by those of Landau and his coworkers (1960, 1964a, 1964b) who doubt the intervention of the gamma system in producing the Jendrassik effect. However, daily clinical experience contradicts Hofmann's findings, and data experimentally obtained by us (Ferrari and Sanna, 1965) dispel the doubts elicited by Landau and his coworkers (1964a, 1964b). Finally, Guidetti (1962) has advanced an interpretation, supported by the experimental findings of Di Perri and Giaquinto (1962), that may reconcile the opposition between the views of Barraquer-Bordas and Hassler. According to Guidetti (1962) the lack of the Jendrassik phenomenon in Parkinson patients may be the result of an "occlusion" effect at the spinal level since the gamma motor pool is already under excessive supraspinal facilitation. We can accept as a fact that the function of the gamma system is altered, in Parkinson patients, even if the details of this abnormality remain as yet unclear. Furthermore the gamma system appears to be the physiological mediator of tone regulation in attentive processes. Further experimental data relating attention to rigidity are afforded by the electromyographic observations of Matsumoto, Rossmann, Lin and Cooper (1963). They have shown that the best technique for facilitating the appearance of a clinically appreciable plastic rigidity in doubtful Parkinson cases is to have the patient perform fine movements with the controlateral limbs. When we remember the observations of Paillard (1959) on the diffuse nature of the tone regulation accompanying attention we can see the importance of Matsumoto's findings in demonstrating the relationships between rigidity and attention. Some data relating to this problem have been obtained also from analyses, in man, of the state of function of supraspinal systems. In EEG studies of Parkinson patients we have observed (Ferrari, Puca and Margherita, 1964) that, while the waking record appear to be practically normal, tracings obtained during sleep show, clearly and constantly, scarce or absent spindling in the C phase of Loomis. The poverty of sleep spindles, which are thought to express activity of subcortical structures of inhibitory (Magoun, 1961) significance, has probably the same meaning as the findings of
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Housepian and Purpura (1963). These authors have been unable to evoke cortical spindles from stimulation of the pallidum and/or thalamus in patients with extrapyramidal syndromes with depth electrodes, using the same techniques that readily cause spindling in carnivores (Buchwald, Wyers, Okuma and Heuser, 1961a; Demetrescu and Demetrescu, 1962; Hongo, Kubota and Shimazu, 1963). On the other hand it is easy to evoke" alerting" of the cortical electrical activity and contemporary augmentation of dystonic and dyskinetic manifestations by electrical stimulation of subcortical structures, the subsequent coagulation of which causes disappearance of rigidity and improvement of other dystonic disorders (Jung and Hassler, 1960; Spiegel and Wycis, 1956). These facts are another, although indirect, confirmation of the strict relationships between systems subserving attentive activations and extrapyramidal dystonic disorders. c) Data from animal experimentation
The observations of animal experimentation can be referred to as having only an indirect significance in relation to the pathological physiology of plastic rigidity, a dystonic condition occurring only in man. Some data, however, concerning the function of brainstem and other subcortical "extrapyramidal" structures, belonging to the so called "diffuse projection systems," are of interest in discussing our interpretation of rigidity. The reticular formation of the brainstem (Rossi and Zanchetti, 1957) is a typical example of a structure that controls behavioral and electroencephalographic alertness with its cephalad projections, and muscle tone with its caudad projections. The two groups of effects are interrelated in a complex and reciprocal manner, as reported by Hugelin and Bonvallet (1957). More rostrally the thalamic portion of systems of diffuse projection subserves, according to Lindsley (1960), attentive function as a particular aspect of awareness. According to Buchwald et al. (1961c), neurons of the striatum also participate in this mechanism, especially in the maintenance of a correlated muscle tone background. Buchwald et al. (1961a) have observed that electrical stimulation, with specific parameters, of the "caudate" nucleus causes
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the appearance of spindles in the corticogram from the ipsilateral hemisphere and loss of muscle tone in controlateral limbs. The loss of tone is associated with (1961c) behavioral "motor inattention" in the affected limbs. These effects seem to be brought about through a strio-thalamo-cortical pathway. Electrical stimulation at various sites along this pathway may produce, with other parameters of stimulation, the opposite effects of electricorticographic and behavioral alerting, augmentation of postural tone and increased efficiency of psychomotor performances. The findings of Buchwald et aI., as well as the similar data of Demetrescu (1962), agree with the pioneer observations of Hess (1954) in showing that the striatum is inessential for muscle tone regulation of any consequence in the realm of neurological motility in the strict sense of the word (Kennard, 1944; Ranson and Berry, 1941; Rioch, 1940; Wilson, 1914). The striatum is involved instead, in carnivores as well as in pri~ates, in mediating muscle tone changes intimately bound to the state of behavioral and electroencephalographic alertness. Laursen (1963) has recently criticized these researches from a methodological point of view, and cast doubts on the identification of the subcortical structures from which the effects attributed to the caudate were obtained. Laursen maintains the effects were due to stimulation of fibers in the internal capsule. These doubts are to be added to many others still to be dispelled in this area of neurophysiological endeavour. The obscurities involve mainly the relation between specific and aspecific subcortico-cortical projection systems (Landau, Bishop and Clare, 1961; Purpura, Shaser and Musgrave, 1964; Macchi and Arduini, 1957), the relative interactions of facilitatory and inhibitory effects (Tissot and Monnier, 1959) and the interrelations between the different subcortical centers (Johnson, 1961; Johnson and Clemente, 1959; Macchi and Arduini, 1957). We can say, however, that if one follows this area of research attempting to apply the resulting data to clinical problems, one can accept the following concept as sufficiently valid. Two distinct systems exist in the organisation of subcorticocortical relationships (Buchwald et aI., 1961c; Tissot and Monnier, 1959), one with facilitating and one with inhibiting effects; both systems participate in regulating attentive alertness and muscle tonus.
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Even if one accepts the critical view of Laursen (1963) with respect to the data of Buchwald and coworkers, the fact remains that spindles in the electrocorticogram, produced by stimulation of corticipetal fibers from basal nuclei, are certainly associated with behavioral inattention and inhibition of tonus in the contralateral limbs. Laursen himself accepts that the "extrapyramidal" subcortical centers preside not over elementary motility but over complex psychomotor integration. The observations of Stern and Ward (1960) and of Shimazu and coworkers (1962a, 1962b) are related to the same problem. All these studies indicate that tonic effects mediated through the gamma route can be elicited by stimulation of pallidum, substantia nigra and thalamus. Shimazu and his coworkers (Yanagisawa, Narabayashi and Shimazu, 1963) transfer tbese experimental data to the interpretation of the surgical treatment of Parkinsonism by saying that a lesion in the thalamus ameliorates rigidity by destroying neurons that maintain a facilitation of tonus distributed hemisomatically to all segmental levels in non-reciprocal manner via the gamma system. The view of the Japanese authors is in obvious agreement with our interpretation of rigidity since strict relations exist between motor attention and the tonic effects of the gamma system, which even participates in the learning processes (Buchwald and coworkers, 1962a, 1962b).
DISCUSSION
The clinical observations, ~ade before and after stereotactic lesions (section a), suggest that plastic rigidity is an expression of an excess of attentive facilitation of tonus. This view finds sufficient support in the experimental findings (sections b and c) proposed for consideration by both the neurologist and the neurophysiologist. According to this view a parallel can be drawn between decerebrate rigidity and plastic rigidity. Decerebrate rigidity can de described as an excess of tonic facilitatory influences exerted by the brainstem reticular formatiQn. Such facilitation of tone is distributed diffusely to body musculature and is physiologically connected to the other functional aspect of the reticular formation: the maintenance of a basic awareness, of an elementary level of consciousness.
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Plastic rigidity, instead, can be described as an excess of tonic facilitatory influences exerted by part of the basal ganglia. Such facilitation of tone is distributed to one half of the body and is physiologically connected to the processes of conative motor attention. Motility, in man, involves intention, attention and scope-directed guidance. These psychological aspects find their neuromuscular correlation in adjustments of tonic influences that anticipate, sustain and favor kinetic muscle performance. This "psychomotor," more than purely "motor," function is instrumented by a system of "extrapyramidal" neurons. When this system actively persists it causes plastic rigidity; when it is destroyed, only slight disturbances of attentiveintentive psychomotility appear without damage of "neurological" motility. Our interpretation of rigidity leaves open three important questions: a) What mechanism is responsible for the persistence of the rigidity-causing, "facilitating" system? b) What is the pathway that conveys the "facilitatory" influences to the spinal motor level? c) Why is a lesion of the "facilitatory" system followed by improvement not only of rigidity but also of tremor and of dyskinetic manifestations other than Parkinsonism? a) To explain the persistence of the "facilitatory" system some writers have postulated an "irritation" of its neurons, due to "sprouting" or "denervation" hypersensitivity (Guidetti, 1962; Ward et aI., 1958; Cooper, 1961). Others (Bergamini and Schiffer, 1961; Balbi, 1962) invoke a "release" mechanism, through a selective loss of "inhibitory" neurons, assuming that the unchecked action of facilitatory elements is due to imbalance in a normally equilibrated system. The existence of pharmacologically induced Parkinson syndromes, which rapidly regress after discontinuation of the drug, is proof against the hypotheses of "sprouting" or "denervation hypersensitivity" (Ferrari, 1963). On the contrary, many histological, physiological and pharmacological data (Ferrari, 1963) favor the view that a selective involvement of "inhibitory" neurons with secondary release of "facilitatory" elements is at play. The EEG observation that the "sleep spindles" are depressed in Parkinson patients is an indirect proof of the latter view, as the "sleep spindles" are thought (Magoun, 1961) to express the activity
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of subcortical systems with inhibitory influences in general and upon the gamma motor neurons in particular (Hongo, Kubota and ShimaZU, 1963). The brain structures (substantia nigra, medial pallidum, ansa lenticularis, ventrolateral thalamus) in which the pathological lesions of Parkinsonism are located, are the same as those in which a surgical coagulation induces effective control of rigidity. This fact forces us to admit that inhibitory" and facilitatory" neurons are intermingled in the same topographical areas. This pattern of location of cells, with opposite functional significance in regard to tonic effects, is not surprising as it has been shown to exist in other centers (Dow and Motuzzi, 1958). II
II
b) The pathway of tonic facilitating influences is thought by some (Spuler, Szekely and Spiegel, 1962; Shimazu, Hongo and Kubota, 1962a) to descend directly to the cord, while others (Buchwald et al., 1961c; Lindsley, 1960; Maspes, 1960; Monnier and Tissot, 1958; Purpura et al., 1958, 1961 , 1964) believe that it loops first through a cortical relay. The two views are not mutually exclusive. In any case, if plastic rigidity is in fact the somatic correlate of motor attention, it is highly improbable for the facilitatory neurons not to have very close bonds with motor and premotor cortex. Several anatomical and physiological findings (Macchi and Arduini, 1957; Tissot and Monnier, 1959) verify the existence of such bonds. c) Parkinsonian tremor, as well as many extrapyramidal dyskinetic and dystonic manifestations, are ameliorated by the same surgical lesions that remove rigidity. If we consider Parkinsonian tremor a somatic expression of emotional psychomotility, its complete stereotactic relief can be explained in the same way proposed for rigidity (Ferrari, 1963). However, all extrapyramidal symptoms other than Parkinson's syndrome are improved only in their intensity. Therefore, it seems that the therapeutic lesions do not involve directly the mechanism of production of tics, torsion spasms and choreic and athetoid movements. All these manifestations also abate spontaneously but temporarily in all conditions of psychosensory rest (most clearly in sleep). It is therefore very likely that their amelioration after a subcortical lesion is also due to the loss of the "hemisomatic aspecific facilitation" correlated with motor attention. This loss probably duplicates a
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situation of rest, at least as far as the tonic substrate of psychomotility is concerned. The three questions that we have discussed and many other uncertain points have to wait further data from experiment and clinical observation before they are settled. For the moment we attach to the interpretation proposed here only the heuristic value of calling the attention of research workers to plastic rigidity as a unique "experimentum naturae." Through it we have under observation the selective lesion of a system of neurons involved in a "psychomotor" function, such as motor attentiveness, exclusively pertaining to "Homo sapiens." Thereby nature offers us the chance to study and understand some "neurological" aspects of "psychic" functions.
SUMMARY
The physiological significance of tone-regulation subserved by the substantia nigra, globus pallidus, ansa lenticularis and nucleus ventralis lateralis of the thalamus is discussed. As a matter of fact lesions of these " extrapyramidal" structures improve rigidity without causing any "neurologically" detectable impairment of muscular tone. Clinical and experimental data are reported which suggest that the tone-regulating function of these structures belongs to the realm of the psychological aspect of motility rather than to the neurological one. At the light of the data discussed, rigidity appears to be a malfunction, an excess, of a tone-regulating mechanism subserving attentive readiness to action. The implications of this interpretation of rigidity are discussed in relation to the effects on extrapyramidal dystonias and dyskinesias of stereotaxic surgery of the basal ganglia.
REFERENCES
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The University of Minnewta Press, Minneapolis. FENELON, F. (1955) La neuro-chirurgie de l'anse lenticulaire dans les dyskinesies el la maladie de Parkinson, "Sem. Hop. Paris." 31, 1835. FERRARI, E. (1963) Il controllo extrapiramidale del tono muscolare: patologia, "Acta neurol.," 18, 309-356. - , PUCA, F., and MARGHERITA, G. (1964) Le anomalie dei fusi da sonno nei parkinsoniani, "Riv. neurol.," 34, 48-55. - , and SANNA, G. (1965) "Acta neurol.," 20 (in press). FROMENT, ]., PAUFIQUE, L., and THIERS, H. (1928a) La rigidite parkinsonienne se deplace quand changent la direction des yeux et Ie point qu'ils fixent, "Rev. Neur.," 50, 912-913. - , and TIDERS, H. (1928b) Les attitudes du bras qui tendent it maintenir la rigidite parkinsonienne sont celles qui commandent vigilance et logique statique, "Rev. neur.," 50, 909-912. - , and DUBBOS, P. (1929) Rigidite parkinsonienne et rigidite de desequilibre varient
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au bras, des que l'attention prend une direction nouvelle, "Rev. Neur.," 51, 255-257. GRANIT, R. (1955) Receptors and Sensory Perception. Yale University Press., New Haven. GUIDETTI, B. (1962) Considerazioni ed ipotesi patogenetiche suI tremore parkinsoniano, in Atti XIV Congr. Soc. It. Neurol., 163-194, Tied, Siena. HASSLER, R. (1959) Stereotactic brain surgery for extrapyramidal motor disturbances, in Introduction to Stereotaxis, 472, ed. by G. Schaltenbrand and P. Bailey, G. Thieme, Stuttgard. HESS, W. R. (1954) Diencephalon: Autonomic and Extrapyramidal Functions. Grune and Stratton, New York. HEUSER, G., BUCHWALD, N. A., WYERS, E. J. (1962) The "caudate spindle," II. Facilitatory and inhibitory caudate-cortical pathways, "EEG and Clin. Neurophysiol.," 13, 519-524. HOFMANN, W. W. (1962) Observations on peripheral servomechanisms in parkinsonian rigidity, "J, Neurol. Neurosurg. psychiat.," 25, 203-207. HONGO, T., KUBOTA, K., and SHIMAZU, H. (1963) EEG-spindle and depression of gamma motor activity, "J. Neurophysiol.," 26, 568-580. HOUSEPIAN, E. M., and PURPURA, D. P. (1963) Electrophysiological studies of subcortical-cortical relations in man, "EEG and Clin. Neurophysiol.," 15, 20-28. HUGELIN, A., and BONVALLET, M. (1957) Tonus cortical et controle de la facilitation motrice d'origine reticulaire, "J. Physiologie," 47, 1171. HUNT, R. S., MELTZER, G. E., and LANDAU, W. M. (1963) Fusimotor function. Part I: Spinal shock of the cat and the monkey, "Arch. Neurol.," 9, 120-126. JOHNSON, T. N. (1961) Fiber connections between the dorsal thalamus and corpus striatum in the cat, "Expt. neurol.," 3, 556-559. - , and CLEMENTE, C. D. (1959) An experimental study of the fiber connections between the putamen, globus pallidus, ventral thalamus and midbrain tegmentum in cat, "J. Compo Neurol.," 113, 83-101. JUNG, R., and HASSLER, R. (1960) The extrapyramidal motor system, in Handbook of Physiology. Section I, vol. II, 863-927. Am. Physiol. Soc., Washington. KENNARD, M. A. (1944) Experimental analysis of the functions of the basal ganglia in monkeys and chimpanzees, "J. Neurophysiol.," 7, 127-147. KRAYENBUHL, H., SIEGFRIED, ]., and YASARGIL, M. G. (1963) Resultats tardifs des operations stereotaxiques dans Ie traitment de la maladie de Parkinson, "Rev. Neurol.," 108, 485-494. LANDAU, W. M., WEAVER, R. A., and HORNBEIN, TH. F. (1960) Fusimotor nerve function in man, "Arch. Neurol.," 3, 12-45. - , BISHOP, G. H., and CLARE, M. H. (1961) The interactions of several varieties of evoked responses in visual and association cortex of the cat, "EEG and Clin. Neurophysiol.," 13, 43-53. - , and CLARE, M. H. (1964a) Fusimotor function. IV, Reinforcement of the H-reflex in normal sub;ects, "Arch. Neurol.," 10, 117-122. - , (1964b) Reflex reinforcement under fusimotor block in normal sub;ects, "Arch. Neurol.," 10, 122-127. LANDIS, c., and HUNT, W. A. (1939) The Startle Pattern, Farrar and Rinehart, New York. LANGFITT, T. W., KAMEl, K., KOFF, G. Y., and PEACOCK, S. M. (1963) Gamma neuron control by thalamus and globus palZidus, "Arch. Neurol.," 9, 593-606. LAURSEN, A. M. (1963) Physiology of the corpus striatum, in The so-called Extrapyramidal System, Scandinavian University Books. LEKSELL, L. (1945) The action potential and excitatory effects of the small ventral root fibres to skeletal muscle, "Acta physiol. scand.," suppl. 31, 10, 1. LINDSLEY, D. B. (1960) Attention, consciousness, sleep and wakefulness, in Handbook of Physiology: Section 1, Neurophysiology, 1, 1553-1593, Am. Physiol. Soc., Washington. MACCHI, G., and ARDUINI, A. (1957) Organizzazione anatomo-funzionale dei rapporti talamo-corticali, in Atti della Soc. It. Anatomia, XVIII Convegno Sodale, 25, 124, Macri, Firenze.
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MAGOUN, H.i W. (1961) Brain mechanism for internal inhibition, in Proceedings of the Third World Congress of Psychiatry, 1, 6-16, McGill University Press, Montreal. MASPES, P. E. (1960) Orientamenti attuali della neurochirurgia, "Minerva neurochir.," 4,57. MATSUMOTO, K., ROSSMANN, F., LIN, T. H., and COOPER, J. S. (1963) Studies on induced exacerbation of Parkinsonian rigidity. The effect of contralateral voluntary activity, "J. neurol. neurosurg. psychiat.," 26, 27-32. MEYERS, R. (1958) Historical background and personal experiences in the surgical relief of hyperkinesia and hypertonus, in Pathogenesis and Treatment of Parkinsonism, 229, ed by W. S. Fields, c.c. Thomas. Springfield, Ill. - , FRY, F. ]., DREYER, L. L., SCHULTZ, D . F., and NOYES, R. F. (1959) Early experience with ultrasonic irradiation of the pallidofugal and nigral complexes in hyperkinetic and hypertonic disorders, "J. Neurosurg.," 16, 32-34. MONNIER, M., and TIS SOT, R. (1958) Correlated effects in behavior and electrical brain activity evoked by stimulation of the reticular system, thalamus and rhinencephalon in the conscious animal, in Neurological Basis of Behavior, ed. by Wolstenholme G. E. and O. Connor C. M., Little, Boston. NARABAYASHI, H., OKUMA, T., and SHIKIBA, S. (1956) Procaine oil blocking of the globus pallidus, "Arch. Neurol. Psychiat.," 75, 36-48. NIELSEN, J. M., and THOMPSON, G .N. (1947) The Engrammes of Psychiatry, C. C. Thomas, Springfield, II!. NORHOLM, T. H., and TYGSTRUP, 1. J1963) Correlation between the clinical effect of stereotactic operations and brain autopsy findings, in The so-called Extrapyramidal System, 196-203, Scandinavian University Books. PAILLARD, J. (1955) Reflexes et regulations d'origine proprioceptive chez fhomme, Etude neuro-physiologique et psycho-physiologique, These de Paris, Arnette, Paris. - , (1959) Functional organization of afferent innervation of muscle studied in man by monosynaptic testing, "Amer. J. phys. Med.," 38, 239-247. . PINELLI, P. (1963) 1l clinico di fronte al problema della spasticita, "Riv. Spero Freniatr.," 80, 623-638. - , and VALLE, M. (1960) Studio fisiopatologico dei riflessi muscolari nelle paresi spastiche (sui tests per la misura della spasticita), "Arch. Scien. Med.," 110, 77-202. PROCTOR, R., RIKLAN, M., COOPER,!. S., and TEUBER, H. L. (1963) Somatosensory status of Parkinsonian patients before and after chemothalamectomy, "Neurology," 13, 906-912. PURPURA, D. P., HOUSEPIAN, E. M., and GRUNDFEST, H. (1958) Analysis of caudatecortical connection, "Arch. Bio!.," 96, 145-167. - , - (1961) Alterations in corticospinal neuron activity associated with thalamocortical recruiting responses, "EEG and din. neurophysiol.," 13, 365-381. - , SHASER, R. Y., and MUSGRAVE, F. S. (1964) Cortical intracellular potentials during augmenting and recruiting responses, "J. neurophysiol.," 27, 133-151. RANSON, S. W., and BERRY, C. (1941) Observations on monkeys with bilateral lesions of the globus pallidus, "Arch. Neurol. Psychiat.," 46, 504. RIBOT, TH. (1889) Psychologie de fattention, Paris. RICHTER, P. - see Souques. RIKLAN, M., WEINER, H., and DILLER, L. (1959) Somata-psychologic studies in Parkinson's disease, uJ. nerv. ment. dis.," 129, 263-272. - , DILLER, L., WEINER H ., and COOPER, 1. S. (1960a) Psychological studies on effects of chemosurgery of the basal ganglia in Parkinsonism, I, "Arch. Gen. Psychiat.," 2, 22-31. . - , - , - , - (1960b) Psychological studies on the effects of chemosurgery of the basal ganglia in Parkinsonism: II, Aspects of personality, "Arch. Gen. Psychiat.," 3,267-275. - , - , - , - (1961) Visual motor performances before and after chemosurgery of the basal ganglia in Parkinsonism, "J. nerv. ment. dis.," 132, 307-314. - , ZAHN, T. P., and DILLER, L. (1962) Human figure drawing before and after chemosurgery of the basal ganglia in Parkinsonism, "J. nerv. ment. dis.," 135, 500-506.
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RIOCH, D. (1940) Neurophysiology of the corpus striatum and globus pallidus, "Psychiatry," 3, 119. ROSSI, G. F., and ZANCHETTI, A. (1957) The brain stem reticular formation, anatomy and physiology, "Arch. it. biol.," 95, 199-435. RUSHWORTH, G. (1960) Spasticity and rigidity: an experimental study and review, "J. Neurol. Neurosurg. Psychiatr.," 23, 99-118. SHERRINGTON, C. S. (1915) Postural activity of muscle and nerve, "Brain," 38, 191-234. SHIMAZU, H., HONGO, T., and KUBOTA, K. (1962a) Two types of central influences on gamma motor system, "J. Neurophysiol.," 25, 309-323. - , - , - , and NARABAYASHI, H. (1962b) Rigidity and spasticity in man, "Arch. Neurol.," 6, 10-17. SOUQUES, M. A. (1921) Rapport sur les syndromes parkinsoniens, "Rev. Neurol.," 37, 534-570. SPIEGEL, E. A., and WYCIS, H. T. (1954) Ansotomy in paralysis agitans, "A.M.A. Arch. Neurol. Psychiat.," 71, 598-614. - , - (1956) Stimulation of brain stem and basal ganglia in man, in Symposium on Brain Stimulation, ed. by Sheer D. E., 487-497, University of Texas Press, Austin. - , - , BAIRD, H. W., ROVNER, D., and THUR, C. (1956) Pallidum and muscle tone, "Neurology," 6, 350-356. - , - , - , and SZEKELY, E. G. (1957) Physiopathologic observations on the basal ganglia, in Ier Congr. Int. Sci. Neurol., Rapports et Discussion, Vol. 5, 118, Editions Acta Med. Belgica, Brussels. - , - (1958) Pallido-ansotomy: anatomic-physiologic foundation and histopathologic control, in Pathogenesis and Treatment of Parkinsonism, ed. by W. S. Fields, 86, C. C. Thomas, Springfield, Ill. SPULER, H., SZEKELY, E. G., and SPIEGEL, E. A. (1962) Stimulation of ventrolateral region of the thalamus, "Arch. neurol.," 2, 208-219. STERN, J., and WARD, A. A. (1960) Inhibition of the muscle spindle discharge by ventral thalamic stimulation, "Arch. neurol.," 97, 193-204. SUBCZYNSKI, J., MATSUMOTO, K., HULLIN, T., and COOPER, 1. S. (1963) The influence of various stimuli upon Parkinsonian tremor and rigidity, "J. Neural. Neurosurg. Psychiat.," 26, 269-274. TALLAND, G. A. (1962) Cognitive function in Parkinson's disease, "J. nerv. Ment. Dis.," 135, 196-205. TISSOT, R., and MONNIER, M. (1959) Dualite du systeme thalamique de projection diffuse, "EEG and Clin. Neurophysiol.," 11, 675-686. VEIT, H. (1927) La parkinsonisme consecutif aux encephalites epidemiques dans la conception formelle de Rorschach, "Zschr. Ges. Neur. Psych.," 110, 301-324. WARD, A. A. JR., Mc CULLOCH, W. S., and MAGOUN, H. W. (1958) Physiological basis of involuntary movement, in Pathogenesis and Treatment of Parkinsonism, 106, Charles C. Thomas, Springfield, Ill. WATKINS, E. S., and OPPENHEIMER, D. R. (1962) Mental disturbances after thalamolysis, "J. Neurol. neurosurg. Psychiat.," 25, 243-250. WEAVER, R. A., LANDAU, W. W., and HIGGINS, J. F. (1963) Fusimotor function. Part. II. Evidence of fusimotor depression in human spinal shock, "Arch. Neurol.," 90, 127-132. WILSON, S. A. K. (1914) An experimental research into the anatomy and physiology of the corpus striatum, "Brain," 36, 427-492. WOODWORTH, H. (1914) The measurement of attention, "Psychological Monographs," 17,5. YANAGISAWA, N., NARABAYASHI, H., and SHIMAZU, H. (1963) Thalamic influences on the gamma motor system, "Arch. Neurol.," 9, 348-357.
Dott. Eugenio Ferrari, Clinica delle Malattie Nervose e Mentali dell'Universit' di Napoli, Piazza Miraglia 2, Napoli, Italy.
La maladie est une experimentation de l' ordre le plus sub til, instituee par la niiture, .. . avec des procedes dont l'art humaine ne dispose pas. Th. Ribot
Under the meaningful title "The riddle of the Parkinson syndrome," Aring (1962) has very recently reviewed the difficulties encountered by all hypotheses intended to explain the physiopathological mechanism producing the Parkinson symptom-complex. As far as rigidity is concerned, however, some clinical changes following therapeutic stereotactic lesions, and recently obtained data on the neurophysiology of muscle tone (Buchwald, Heuser, Wyers and Lauprecht, 1961 ; Granit, 1955; Paillard, 1955, 1959) do suggest a new hypothesis which affords an apparently coherent interpretation: plastic rigidity appears as a malfunction, an excess of a mechanism serving to pattern body posture to subserve attentive readiness to action. If one wishes to paraphrase the classical sentence of Sherrington (1915): "Reflex tonus is postural contraction; decerebrate rigidity is reflex standing," the hypothesis proposed here can be synthetically expressed by the statement: "Parkinsonian rigidity is attentive posture." The' data supporting this interpretation are outlined under the following three headings: a) clinical observations; b) experimental findings in man; c) experimental results in animals.
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Clinical observations
Parkinson rigidity appears to the neurologist as a well defined type of hypertonicity: a) it is plastic in quality; b) it is equally distributed in agonist and antagonist muscles; c) it has the same qualities at all segmental levels. Rigidity can be topographically distributed over the entire body, or on one side only (hemisomatic). After surgical lesion of some basal ganglia areas, rigidity disappears completely in the contralateral side of the body and improves only slightly ipsilaterally. Therefore, we must say that the neuronal mechanism sustaining rigidity has a "subcortical" location and exerts tone facilitating influences which are 1) distributed mainly contralaterally to one body side; 2) "panmetameric" (i.e. affecting equally all segmental levels ); 3) "aspecific" (i.e. uniformly affecting all muscles, without regard to agonist-antagonist reciprocal innervation). Beneficial effects upon rigidity have been obtained by lesions of: 1) substantia nigra (Meyers, 1958; Meyers et aI., 1959); 2) globus pallidus (Narabayashi et aI., 1956; Spiegel and Wycis, 1956); 3) ansa lenticularis (Spiegel and Wycis, 1954, 1958; Fenelon, 1955); 4) thalamic ventrolateral nucleus (Cooper, 1961; Hassler, 1959; Krayenbiihl, Siegfried and Yasargil, 1963); 5) internal capsule (Norholm and Tygstrup, 1963). Furthermore, the exact site and size of stereotactic lesions cannot be defined with certainty, except in rare cases (Cooper, Bergmann and Caracalos, 1963; Norholm and Tygstrup, 1963) that can be, in time, verified at autopsy. Therefore, the anatomical identification of the neuronal system maintaining rigidity remains uncertain. Most probably it is not a "center" in the anatomical sense but a "system" of neurons scattered throughout several structures of the base of the brain. The lesions that affect this system and thereby improve rigidity do not cause any neurologically detectable impairment of tone regulation. This fact elicits the question of what is the "physiological" significance of a system of neurons that reveals itself only in a pathological state, and only in man, as subserving a well defined type of tone facilitation which is "panmetameric, aspecific and hemisomatic. " The data reported below suggest that the tone regulating function of this system belongs to the realm of the psychological aspects of
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motility, the "psychomotor" components, rather than to that of "neurological" motility. In particular, it serves the motor aspect of conative attention. In 1928 and 1929 Froment and coworkers had already underlined the relationships between rigidity and attention in a series of papers one of which had the significant title: "La rigidite parkinsonienne varie au bras, des que l'attention prend une direction nouvelle." Later, Claude and Baruk (1931), Denny-Brown (1962), Subczynski, Matsumoto, Hullin and Cooper (1963) noted and commented upon the facilitation of rigidity - as well as of other dystonic and dyskinetic extrapyramidal symptoms - in relation to willingness-toact. Conversely, but with identical significance, there stand out the temporary remissions or improvements of rigidity occurring when attention weakens. The most striking example of such an event is the complete effacement of Parkinsonian symptomatology under hypnosis. Disertori (1939) has described the illuminative case of an acrobat, forced by Parkinsonian rigidity to abandon his activity, who could temporarily reacquire acrobatic agility under hypnosis. Aring (1962) has recently reported similar clinical instances that stress the relationships between level of awareness and rigidity and that point to "conative attentiveness" as an essential factor for facilitation of plastic hypertonus: "conative attentiveness" appears as a component of attentive function, exclusively pertaining to "homo sapiens." Furthermore, the intensity of rigidity fluctuates in aSSOClatIOn with emotional changes, but in such a manner as to appear clearly related to attentiveness levels. In fact, emotional states, so violent and tempestuous as to release automatic motility patterns, with diminution of lucid awareness, as in panic states or in disaster situations (Aring, 1962), induce temporary but complete disappearance of Parkinson symptoms. Conversely, moderate emotional reactions, that are usually associated with augmented awareness, worsen rigidity. While all the above mentioned clinical observations demonstrate the existence of relationships between extrapyramidal rigidity and attention, they leave undetermined the significance and directness of such relations. The following data indicate that the ties between attention and plastic rigidity are strict and direct in nature.
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In first place the facies of Parkinsonism is strikingly similar, as Richter has noted, to the facial expression of attentiveness (fig. 1).
Fig. 1 -
The facies of Parkinsonism (from Andre-Thomas and Ajuriaguerra, 1951, pag. 552) is similar to the facial expression of attentiveness.
In second place, the global body posture of Parkinson patients (fig. 2c) reproduces the posture of one who, suddenly apprehending some signal of dangerous significance, automatically takes a position (startle pattern) of tense readiness to perform in any manner suitable
a Fig. 2 -
b
c
The posture of Parkinsonism (c, from Andre-Thomas and Ajuriaguerra, 1951) is similar to the "startle pattern" (b, from Landis and Hunt, 1939) and the posture of the athlete ready for motor performance (a).
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to deal with any menace, from any direction (fig. 2b). This posture is similar to that of the athlete who, in concentrated attention and conscious expectation, stays ready for a motor performance of any type, in any direction, at any moment (fig. 2a). A global patterning of muscle tone, similar to that of the above described postural situations, pathologically prevails in the "rigid" subject. The persistence of such patterning of tone distribution impedes the selective and specifically directed performance of individual motor regions, whose selective performance is, however, "per se" intact, as it reemerges in complete normality in one half of the body when a stereotactic lesion is followed by disappearance of the excessive tonic facilitation, aspecific in quality and panmetameric in distribution. In other words, all these analogies, derived from clinical observations, suggest that rigidity is the abnormally persistent plastic shaping of the motor system into a pattern that is the postural correlate of "motor attention." In support of this hypothesis we can summon the alterations of attentive function in Parkinsonian patients, as reported in psychological studies by Aubrun (1937), Veit (1927) and by Riklan et aI. (1959; 1960a, 1960b; 1961; 1962). These alterations are not a secondary consequence of rigidity; in fact they persist, and even worsen, after disappearance of rigidity following a stereotactic lesion (Proctor et al., 1963; Riklan et aI., 1960a, 1960b). Therefore, such abnormalities of attention are to be considered as the psychological consequence of lesions of the same basal ganglia neurons involved in a particular kind of tone regulation. This kind of tone regulation is not related to the specific motor performances that can be tested at a neurological examination and which remain normal after thalamic or pallidal lesions. It is, instead, a refined type of tone regulating function, a true psychomotor function (Nielsen and Thompson, 1947), inextricably tied or, better, coextensive with psychological attention and intention, i.e., motivational readiness to performance. In fact, the only defects demonstrable by psychological testing of Parkinson subjects, before and after stereotactic lesions, are in the area of the "motivational functions" (Riklan et aI., 1960b). As the physiological abnormality underlying Parkinsonian rigidity seems to involve functions that are psychomotor and not simply
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motor in nature, we must give great significance to the fact that a rigidity of this type appears only in man. Drugs capable of rapidly inducing a severe Parkinson syndrome in man, never produce rigidity in experimental animals. In our hypothesis this fact is explained as follows: conative attention is a function developed at a significant degree only in man; in a parallel manner, the specific neuronal organization, the alteration of which produces plastic rigidity, exists ·only in man in a full morphological and functional sense. Most likely, the predominantly hemisomatic and contralateral distribution of tone-facilitating effects exerted by the rigidityproducing system finds its significance in the great development reached in man by the use of the hands in motor performance; this obviously requires focussing attention to one half of the body at a time. In conclusion, the clinical characteristics of rigidity and its changes following therapeutic surgical lesions suggest the following hypothesis: "plastic" rigidity is the manifestation, at the "neurological" level, of functional derangement in a neuronal system that physiologically presides over "psychological" aspects of motor function. b) Experimental findings in man
In normal situations, the existence of relationships between attention and motor function has been proposed since the last century. Ribot, in 1889, stated that motor phenomena are "les conditions necessaires, les elements constitutifs, les facteurs indispensables de l'attention. Si l'on supprimait totalement les mouvements, on supprimerait totalement l' attention." The subject was later investigated with ingenious techniques by Courts (1939), who showed significant relations between muscle tension and learning, and Woodworth (1914) who, while studying the connection between attentive muscle tension and reaction times, clarified the concept of "motor attention." Recently Paillard (1955; 1959) has furnished excellent psychophysiological data concerning the neuromuscular correlates of attentive function derived from studies of metameric spinal cord
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physiology. Paillard's work is an extrapolation to man of Leksell's (1945) and Granit's (1955) findings in animals relative to the physiology of muscle spindles and the related gamma motoneuron system. According to Paillard, the differential analysis of mechanical stretch reflexes (initiated by direct stimulation of muscle spindles) and monosynaptic reflexes evoked by electrical stimulation of afferent fibers (thus bypassing muscle spindles) yields information on the state of excitability of the proprioceptive receptor itself: the so-called "spindle tonus" or "fusimotor tonus" expressing the gamma motoneurons' level of activity. In experiments based on such premise, Paillard has shown that the state of attentiveness has a constant somatic correlate. Fluctuations of attention are accompanied by parallel fluctuations of "spindle tonus," therefore of the gamma motoneurons' "tonic" activity. Paillard's findings and interpretation, although submitted to conceptual critique by Pinelli and Valle (1960) and to methodological critique by Landau and his coworkers (1960, 1964a, 1964b) have been confirmed by later experiments, conducted with revised technique, with findings that support the participation of the gamma motor system in attentive processes (Ferrari and Sanna, 1965). This is very important for understanding the relationship between rigidity and attention, as, in fact, disturbances of gamma function have been discovered in patients with plastic rigidity. Barraquer-Bordas (1957, 1961a, 1961b) gave the first interpretation of rigidity as an abnormal excess of tonic influences mediated by the gamma system. Rushworth (1960) experimentally confirmed this view by showing that partial procaine block of mixed nerves (which selectively blocks conduction of gamma motor fibers) causes disappearance of rigidity without loss of motor power in the corresponding muscles. Jung and Hassler (1960) believe, by contrast, that in rigidity there is a defect rather than an excess of fusimotor activity. Hassler's opinion derives from the fact that facilitation of "deep" reflexes induced by Jendrassik manoeuver - through an augmentation of fusimotor gamma activity - is absent or defective in Parkinson subjects. This proves, according to Hassler, that there is a depression of fusimotor activity (Arrigo, Cosi and Savoldi, 1963). The opposite opinions of the Spanish and the German workers have elicited a debate which is still active (Barraquer-Bordas, 1961a).
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The problem is further bemuddled by the findings of Hofmann (1962) and Angel and Hofmann (1963) who deny any alteration of the Jendrassik effect in Parkinsonism and by those of Landau and his coworkers (1960, 1964a, 1964b) who doubt the intervention of the gamma system in producing the Jendrassik effect. However, daily clinical experience contradicts Hofmann's findings, and data experimentally obtained by us (Ferrari and Sanna, 1965) dispel the doubts elicited by Landau and his coworkers (1964a, 1964b). Finally, Guidetti (1962) has advanced an interpretation, supported by the experimental findings of Di Perri and Giaquinto (1962), that may reconcile the opposition between the views of Barraquer-Bordas and Hassler. According to Guidetti (1962) the lack of the Jendrassik phenomenon in Parkinson patients may be the result of an "occlusion" effect at the spinal level since the gamma motor pool is already under excessive supraspinal facilitation. We can accept as a fact that the function of the gamma system is altered, in Parkinson patients, even if the details of this abnormality remain as yet unclear. Furthermore the gamma system appears to be the physiological mediator of tone regulation in attentive processes. Further experimental data relating attention to rigidity are afforded by the electromyographic observations of Matsumoto, Rossmann, Lin and Cooper (1963). They have shown that the best technique for facilitating the appearance of a clinically appreciable plastic rigidity in doubtful Parkinson cases is to have the patient perform fine movements with the controlateral limbs. When we remember the observations of Paillard (1959) on the diffuse nature of the tone regulation accompanying attention we can see the importance of Matsumoto's findings in demonstrating the relationships between rigidity and attention. Some data relating to this problem have been obtained also from analyses, in man, of the state of function of supraspinal systems. In EEG studies of Parkinson patients we have observed (Ferrari, Puca and Margherita, 1964) that, while the waking record appear to be practically normal, tracings obtained during sleep show, clearly and constantly, scarce or absent spindling in the C phase of Loomis. The poverty of sleep spindles, which are thought to express activity of subcortical structures of inhibitory (Magoun, 1961) significance, has probably the same meaning as the findings of
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Housepian and Purpura (1963). These authors have been unable to evoke cortical spindles from stimulation of the pallidum and/or thalamus in patients with extrapyramidal syndromes with depth electrodes, using the same techniques that readily cause spindling in carnivores (Buchwald, Wyers, Okuma and Heuser, 1961a; Demetrescu and Demetrescu, 1962; Hongo, Kubota and Shimazu, 1963). On the other hand it is easy to evoke" alerting" of the cortical electrical activity and contemporary augmentation of dystonic and dyskinetic manifestations by electrical stimulation of subcortical structures, the subsequent coagulation of which causes disappearance of rigidity and improvement of other dystonic disorders (Jung and Hassler, 1960; Spiegel and Wycis, 1956). These facts are another, although indirect, confirmation of the strict relationships between systems subserving attentive activations and extrapyramidal dystonic disorders. c) Data from animal experimentation
The observations of animal experimentation can be referred to as having only an indirect significance in relation to the pathological physiology of plastic rigidity, a dystonic condition occurring only in man. Some data, however, concerning the function of brainstem and other subcortical "extrapyramidal" structures, belonging to the so called "diffuse projection systems," are of interest in discussing our interpretation of rigidity. The reticular formation of the brainstem (Rossi and Zanchetti, 1957) is a typical example of a structure that controls behavioral and electroencephalographic alertness with its cephalad projections, and muscle tone with its caudad projections. The two groups of effects are interrelated in a complex and reciprocal manner, as reported by Hugelin and Bonvallet (1957). More rostrally the thalamic portion of systems of diffuse projection subserves, according to Lindsley (1960), attentive function as a particular aspect of awareness. According to Buchwald et al. (1961c), neurons of the striatum also participate in this mechanism, especially in the maintenance of a correlated muscle tone background. Buchwald et al. (1961a) have observed that electrical stimulation, with specific parameters, of the "caudate" nucleus causes
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the appearance of spindles in the corticogram from the ipsilateral hemisphere and loss of muscle tone in controlateral limbs. The loss of tone is associated with (1961c) behavioral "motor inattention" in the affected limbs. These effects seem to be brought about through a strio-thalamo-cortical pathway. Electrical stimulation at various sites along this pathway may produce, with other parameters of stimulation, the opposite effects of electricorticographic and behavioral alerting, augmentation of postural tone and increased efficiency of psychomotor performances. The findings of Buchwald et aI., as well as the similar data of Demetrescu (1962), agree with the pioneer observations of Hess (1954) in showing that the striatum is inessential for muscle tone regulation of any consequence in the realm of neurological motility in the strict sense of the word (Kennard, 1944; Ranson and Berry, 1941; Rioch, 1940; Wilson, 1914). The striatum is involved instead, in carnivores as well as in pri~ates, in mediating muscle tone changes intimately bound to the state of behavioral and electroencephalographic alertness. Laursen (1963) has recently criticized these researches from a methodological point of view, and cast doubts on the identification of the subcortical structures from which the effects attributed to the caudate were obtained. Laursen maintains the effects were due to stimulation of fibers in the internal capsule. These doubts are to be added to many others still to be dispelled in this area of neurophysiological endeavour. The obscurities involve mainly the relation between specific and aspecific subcortico-cortical projection systems (Landau, Bishop and Clare, 1961; Purpura, Shaser and Musgrave, 1964; Macchi and Arduini, 1957), the relative interactions of facilitatory and inhibitory effects (Tissot and Monnier, 1959) and the interrelations between the different subcortical centers (Johnson, 1961; Johnson and Clemente, 1959; Macchi and Arduini, 1957). We can say, however, that if one follows this area of research attempting to apply the resulting data to clinical problems, one can accept the following concept as sufficiently valid. Two distinct systems exist in the organisation of subcorticocortical relationships (Buchwald et aI., 1961c; Tissot and Monnier, 1959), one with facilitating and one with inhibiting effects; both systems participate in regulating attentive alertness and muscle tonus.
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Even if one accepts the critical view of Laursen (1963) with respect to the data of Buchwald and coworkers, the fact remains that spindles in the electrocorticogram, produced by stimulation of corticipetal fibers from basal nuclei, are certainly associated with behavioral inattention and inhibition of tonus in the contralateral limbs. Laursen himself accepts that the "extrapyramidal" subcortical centers preside not over elementary motility but over complex psychomotor integration. The observations of Stern and Ward (1960) and of Shimazu and coworkers (1962a, 1962b) are related to the same problem. All these studies indicate that tonic effects mediated through the gamma route can be elicited by stimulation of pallidum, substantia nigra and thalamus. Shimazu and his coworkers (Yanagisawa, Narabayashi and Shimazu, 1963) transfer tbese experimental data to the interpretation of the surgical treatment of Parkinsonism by saying that a lesion in the thalamus ameliorates rigidity by destroying neurons that maintain a facilitation of tonus distributed hemisomatically to all segmental levels in non-reciprocal manner via the gamma system. The view of the Japanese authors is in obvious agreement with our interpretation of rigidity since strict relations exist between motor attention and the tonic effects of the gamma system, which even participates in the learning processes (Buchwald and coworkers, 1962a, 1962b).
DISCUSSION
The clinical observations, ~ade before and after stereotactic lesions (section a), suggest that plastic rigidity is an expression of an excess of attentive facilitation of tonus. This view finds sufficient support in the experimental findings (sections b and c) proposed for consideration by both the neurologist and the neurophysiologist. According to this view a parallel can be drawn between decerebrate rigidity and plastic rigidity. Decerebrate rigidity can de described as an excess of tonic facilitatory influences exerted by the brainstem reticular formatiQn. Such facilitation of tone is distributed diffusely to body musculature and is physiologically connected to the other functional aspect of the reticular formation: the maintenance of a basic awareness, of an elementary level of consciousness.
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Plastic rigidity, instead, can be described as an excess of tonic facilitatory influences exerted by part of the basal ganglia. Such facilitation of tone is distributed to one half of the body and is physiologically connected to the processes of conative motor attention. Motility, in man, involves intention, attention and scope-directed guidance. These psychological aspects find their neuromuscular correlation in adjustments of tonic influences that anticipate, sustain and favor kinetic muscle performance. This "psychomotor," more than purely "motor," function is instrumented by a system of "extrapyramidal" neurons. When this system actively persists it causes plastic rigidity; when it is destroyed, only slight disturbances of attentiveintentive psychomotility appear without damage of "neurological" motility. Our interpretation of rigidity leaves open three important questions: a) What mechanism is responsible for the persistence of the rigidity-causing, "facilitating" system? b) What is the pathway that conveys the "facilitatory" influences to the spinal motor level? c) Why is a lesion of the "facilitatory" system followed by improvement not only of rigidity but also of tremor and of dyskinetic manifestations other than Parkinsonism? a) To explain the persistence of the "facilitatory" system some writers have postulated an "irritation" of its neurons, due to "sprouting" or "denervation" hypersensitivity (Guidetti, 1962; Ward et aI., 1958; Cooper, 1961). Others (Bergamini and Schiffer, 1961; Balbi, 1962) invoke a "release" mechanism, through a selective loss of "inhibitory" neurons, assuming that the unchecked action of facilitatory elements is due to imbalance in a normally equilibrated system. The existence of pharmacologically induced Parkinson syndromes, which rapidly regress after discontinuation of the drug, is proof against the hypotheses of "sprouting" or "denervation hypersensitivity" (Ferrari, 1963). On the contrary, many histological, physiological and pharmacological data (Ferrari, 1963) favor the view that a selective involvement of "inhibitory" neurons with secondary release of "facilitatory" elements is at play. The EEG observation that the "sleep spindles" are depressed in Parkinson patients is an indirect proof of the latter view, as the "sleep spindles" are thought (Magoun, 1961) to express the activity
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of subcortical systems with inhibitory influences in general and upon the gamma motor neurons in particular (Hongo, Kubota and ShimaZU, 1963). The brain structures (substantia nigra, medial pallidum, ansa lenticularis, ventrolateral thalamus) in which the pathological lesions of Parkinsonism are located, are the same as those in which a surgical coagulation induces effective control of rigidity. This fact forces us to admit that inhibitory" and facilitatory" neurons are intermingled in the same topographical areas. This pattern of location of cells, with opposite functional significance in regard to tonic effects, is not surprising as it has been shown to exist in other centers (Dow and Motuzzi, 1958). II
II
b) The pathway of tonic facilitating influences is thought by some (Spuler, Szekely and Spiegel, 1962; Shimazu, Hongo and Kubota, 1962a) to descend directly to the cord, while others (Buchwald et al., 1961c; Lindsley, 1960; Maspes, 1960; Monnier and Tissot, 1958; Purpura et al., 1958, 1961 , 1964) believe that it loops first through a cortical relay. The two views are not mutually exclusive. In any case, if plastic rigidity is in fact the somatic correlate of motor attention, it is highly improbable for the facilitatory neurons not to have very close bonds with motor and premotor cortex. Several anatomical and physiological findings (Macchi and Arduini, 1957; Tissot and Monnier, 1959) verify the existence of such bonds. c) Parkinsonian tremor, as well as many extrapyramidal dyskinetic and dystonic manifestations, are ameliorated by the same surgical lesions that remove rigidity. If we consider Parkinsonian tremor a somatic expression of emotional psychomotility, its complete stereotactic relief can be explained in the same way proposed for rigidity (Ferrari, 1963). However, all extrapyramidal symptoms other than Parkinson's syndrome are improved only in their intensity. Therefore, it seems that the therapeutic lesions do not involve directly the mechanism of production of tics, torsion spasms and choreic and athetoid movements. All these manifestations also abate spontaneously but temporarily in all conditions of psychosensory rest (most clearly in sleep). It is therefore very likely that their amelioration after a subcortical lesion is also due to the loss of the "hemisomatic aspecific facilitation" correlated with motor attention. This loss probably duplicates a
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situation of rest, at least as far as the tonic substrate of psychomotility is concerned. The three questions that we have discussed and many other uncertain points have to wait further data from experiment and clinical observation before they are settled. For the moment we attach to the interpretation proposed here only the heuristic value of calling the attention of research workers to plastic rigidity as a unique "experimentum naturae." Through it we have under observation the selective lesion of a system of neurons involved in a "psychomotor" function, such as motor attentiveness, exclusively pertaining to "Homo sapiens." Thereby nature offers us the chance to study and understand some "neurological" aspects of "psychic" functions.
SUMMARY
The physiological significance of tone-regulation subserved by the substantia nigra, globus pallidus, ansa lenticularis and nucleus ventralis lateralis of the thalamus is discussed. As a matter of fact lesions of these " extrapyramidal" structures improve rigidity without causing any "neurologically" detectable impairment of muscular tone. Clinical and experimental data are reported which suggest that the tone-regulating function of these structures belongs to the realm of the psychological aspect of motility rather than to the neurological one. At the light of the data discussed, rigidity appears to be a malfunction, an excess, of a tone-regulating mechanism subserving attentive readiness to action. The implications of this interpretation of rigidity are discussed in relation to the effects on extrapyramidal dystonias and dyskinesias of stereotaxic surgery of the basal ganglia.
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Dott. Eugenio Ferrari, Clinica delle Malattie Nervose e Mentali dell'Universit' di Napoli, Piazza Miraglia 2, Napoli, Italy.