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The importance of visual feedback on the accuracy of jaw and finger positioning in man
OS.00+ 0.00 0003~9969192
A&U 0~1 Biol. Vol. 37. NO. 9, pp. 677483, 1992 Copyright 0
Printed in Great Britain. All righu reserved
1992 Pergamon Press Ltd
THE IMPORTANCE OF VISUAL FEEDBACK ON THE ACCURACY OF JAW AND FINGER POSITIONING IN MAN REI;~;HILDEJACOBS,DANIEL VAN STEENBERGHE and AN SCHOITE Department of Periodontology, Laboratory of Oral Physiology, Faculty of Medicine, Catholic University of Leuven, B-3000 Leuven. Belgium (Received
30 October
1991; accepted
I2 May 1992)
Summary-The anatomical position of the mandible means that direct visual feedback is not possible. To clarify the role of visual information, several jaw- and finger-positioning tasks were designed, both in a ‘free-movement’ and an ‘isolated’ (arm or head fixed) state, with or without a visual feedback display of the target position. The subjects had to position the mandible or the index finger of the preferred hand on to a movable metal bar and to maintain a defined position coinciding with the target level provided on an oscilloscope screen. The position signal was tape recorded and computer analysed off-line. Digital filtering differentiated between the drift and the oscillations around the target (root mean square). The results demonstrated a lack of precision in the free-movement, finger-positioning task after withdrawal of visual feedback. For jaw opening and closing muscles, position control was less impaired when a visual feedback display was abolished. It was suggested that the efficiency of jaw positioning is not primarily determined by visual feedback. Key words: proprioception,
finger tremor, jaw position, visual feedback, trigeminal system.
INTRODUCTION
MATERIALS
Subjects
The trigeminal system provides precise position control during size-discrimination tasks (Van Willigen and Broekhuijsen, 1983; Van Willigen, Broekhuijsen and Van Der Meer, 1987). Jaw separations are recognized fairly well with an imagined, a verbally specifited or a physically imposed standard (Van Willigen and Broekhuijsen, 1983). On the other hand, when subjects have to reproduce a particular reference bite force “a mechanism controlling bite-force with any degree of precision is absent in the jaw system” (Van Willigen et al., 1987). We have found that motor control of jaw muscles is less developed than that of limb muscles during isometric contraction, when the target force level was presented by means of visual feedback (van Steenberghe ef nl., 1991). As, unlike limbs, one cannot see one’s own jaw, this may explain the poor performance. Accuracy of limb movement is improved by visual feedback (Adams, 1976). For tracking performance of limb muscles, two types of visual feedback are usually available: visual feedback of the target and direct visual feedback of the moving limb itself. For the jaw, evidently only the former applies. The assumption is that jaw position control is not dependent on visual feedback. To confirm this model, we have now sought to clarify the role of visual cues in a jaw-positioning task. Abbreviarions:
The subjects were 32 healthy volunteers (21 females, 11 males; 19-29 yr of age, mean age 21). half of them dental students, without clinical evidence of occlusal abnormalities or craniomandibular dysfunction. They all gave informed consent without being aware of the purpose of the experiment. Experimental procedure
To compare equivalent muscle groups in both motor systems, the experiment involved positioning tasks with flexor or extensor muscles of the preferred index finger and jaw depressor or elevator muscles, either in an isolated or a free-movement condition (Table 1). Subjects were seated comfortably on a dental chair in a dark room in an upright position in front of the positioning device. They had to position the index finger of the preferred hand [Fig. l(A)] or the mandible [Fig. l(B)] on to a movable metal bar. Isolated versus free-movement finger position [Fig. f(A)]. In the free-movement finger-positioning
tasks, flexor or extensor muscles were activated while the upper arm was kept vertically down by the body and the forearm at 90” to the body. Thus, only the hand and the fingers could be moved. Then, the finger had to position the bar 18 mm upwards, counteracting a 0.12-O. 15 N load. In the isolated finger-positioning tasks, the forearm was fixed in a plastic cylinder and the wrist and the fingers, except for the metacarpophalangeal joint of the index finger, were immobilized by a strap. The
ANOVA, analysis of variance; LVDT, linear
variable-displacement
AND METHODS
transducer. 677
678
FSINHILDEJACOBS
er al.
Table I. Comparison of jaw and finger muscles with an equivalent function Free-movement positioning (s) Finger
Extensor
Visual feedback ;:; (b) (d)
No visual feedback
Isolated positioning (s)
Flexor O-30 60-90 30-60 90-120
k”,’ (b) (d)
Free-movement positioning (s) Jaw
Elevator
Visual feedback
O-30 i:,’ 60-90 (b) 30-60 (d) 90420
No visual feedback
Flexor O-30 60-90 3cMo 90-120
Isolated positioning (s)
Depressor No No No No
Extensor
test* test test test
Elevator i:; (b) (d)
Depressor O-30 60-90 30-60 90-120
For each muscle group, two trials were made. A trial consisted of a standard run of 30 s with visual feedback provided (a, c) followed by a 30 s-run without visual feedback (b. d). The error score during the visual feedback task was expressed as a proportion of the error score during the non-visual feedback condition. The vi/nv ratios for the r.m.s., amplitude and drift
error were computed as follows: error(a)/error(b), error(c)/error(d). *The jaw depressor muscles were not tested in the free-movement condition.
stretched index finger was held against gravity and had to align the finger signal with the horizontal baseline on the oscilloscope screen by activating either the flexor or extensor muscles. Isolated [Fig. I(B)].
versus
free-movement
jaw
position
In the free-movement, jaw-positioning task, the head rested against an occipital support while subjects had to keep the vertical head position stable. The metal bar was directed upwards by the mandible from a 30-35 mm to a 12-17 mm degree of mouth opening. The isolated jaw-positioning task consisted of activating the elevator muscles while the head was fixed to the headrest and the neck muscles were inactivated by means of a strap. Finally, to evaluate feedback on the jaw-opening muscles, the subjects lay supine with the head in hyperextension (= isolated positioning task). They were instructed to maintain a defined jaw position while the bar was resting on the lower border of the chin. The jaw opening varied between 5 and 10 mm. An LVDT contacted the opposite side of the metal bar and monitored movement in a vertical plane. The vertical displacements were monitored by means of an LVDT connected to the bar. The transducer was able to detect a displacement of 25 pm. The output of the LVDT was displayed on an oscilloscope screen set at eye level 1 m in front of the subjects. An LVDT displacement of 1 mm corresponded to 12 mm displacement on the screen. Subjects had to align the finger or jaw signal with a stationary horizontal baseline presented on the screen, which meant that the limb studied counteracted gravity and the small load of the transducer (0.12-O. 15 N). Only visual feedback of the target and the subject’s output signal were available. There was no direct visualization of the moving limb. For each muscle group, two trials were made. A trial consisted of a standard run of 30 s, with visual feedback, followed by a 30-s run without visual feedback, while subjects kept their eyes closed. Test trials were separated by a 10-s rest.
To avoid learning bias, the subjects were familiarized with the procedure before the actual experiments and for a few seconds only (Poulton, 1974). The testing sequence of all muscle groups was randomized. Calculations and statistics
Data were collected on an Ampex PR 2230 tape recorder and A/D converted at a sample frequency of 1000 Hz to transfer voltages in the -2/f 2 V range to binary values for analysis on an AT computer. The overall efficiency of performance was evaluated by means of the root mean square (r.m.s.) error calculation, which is compatible with parametric statistical tests (Poulton, 1974). It calculated the difference in position between the target level and the output of the transducer after digital high-pass filtering to get rid of the low-set signal (drift). Thus, the r.m.s. error was estimated very precisely from a central 16-s section of the record of the filtered signal, which oscillated around the target level. To exclude large positioning errors (large r.m.s. values) the preceding and following 7-s sections were discarded. Additional measures of error were the amplitude error (subtracting the minimal from the maximal amplitude of the subject’s response) and the drift (low-set signal). The drift indicated that the average response was above or below the target level. However, if the subject’s response changed direction over time, this value was not very useful. All statistical calculations were made with the statistical analysis system. A level of significance of 5% was chosen, unless otherwise stated. The ANOVA multiple comparisons method (Bonferronni correction) was applied to detect differences between the performance with and without visual feedback for each particular muscle group. Afterwards, the error score during the visual feedback task (=vi) was expressed as a proportion of the error score without visual feedback (= nv) for all variables considered (r.m.s., amplitude and drift). The ratio of
Accuracy of jaw and finger positioning
679
(4
'SJLATED CONOiTION
TED CONCiliON
UD A9 LA C K
(8) ISOLATED
C0t401T10~
CONDITION
i ~SOCATEII
CONDI’ION
AB L A C K
Fig. 1. A positioning task consisted of positioning the index finger of the preferred hand (A) or the mandible (B) on to a movable metal bar. Vertical displacements were monitored by linear variable displacement transducer LVDT connected to the bar. All signals were digitalized and high-pass filtered to get rid of the low-set signal (path I). The output of the LVDT was also displayed on an oscilloscope screen (path II). Subjects had to align their positioning signal with a stationary horizontal baseline presented on the screen. Afterwards, the visual display was abolished, while subjects closed their eyes. (A) In the free-movement finger-positioning tasks (unrestrained condition), flexor or extensor muscles were activated. Only the hand and the fingers could be moved. In the isolated finger-positioning task, the upper arm was fixed in a plastic cylinder with the wrist and fingers immobilized by a strap (isolated condition). (B) In the free-movement jaw-positioning task, the head rested against an occipital support, while the subject kept the vertical head position stable (unrestrained condition). In the isolated jaw-positioning task, the head was fixed to the headrest of a dental chair, while the neck muscles were immobilized by means of a strap (isolated condition). In the experimental set-up for the jaw depressor muscles, the subject lay supine (isolated condition). The metal bar was supported by the lower chin border.
680
REINHILDE
performances with/without visual feedback (vi/nv ratio) were compared for jaw- and finger-muscle groups with an equivalent function-jaw elevator (depressor) muscles versus limb extensor (flexor) muscles (ANOVA multiple comparisons method; Bonferronni correction). Finally, a one-way blocks ANOVA was used to evaluate the influence of the dental students’ manual dexterity. RESULTS Eflect of visual feedback
Data were first analysed by means of the ANOVA multiple comparisons method (Bonferronni correction: p < 0.001). For both free-movement finger positionings, visual feedback significantly reduced the positioning error (r.m.s., amplitude). No such differences were detected when considering the isolated positioning tasks or when evaluating jaw positioning tasks (Table 2). Several oscillations during the imposed positioning prevented any significant difference in the drift values (p > 0.05). This measure was considered as less sensitive and omitted from further statistical analysis.
Jacoas et al. which was significantly lower than the ratio for the jaw depressor muscles [ 1.2 (0. l)]. A comparison between the extensor muscles of the hand and the elevator muscles of the jaw revealed significantly higher jaw vi/nv ratios only in the free movements (p < 0.01). In these, vi/nv ratios for the finger were often smaller than I, indicating an increased error score when visual feedback was absent (Fig. 2). On the other hand, all vi/nv ratios for the jaw positioning were approximately equal to or greater than 1 (Fig. 2). Furthermore, r.m.s. vi/nv ratios were significantly higher in the isolated jaw-depressor muscle trials than in the isolated elevator muscle trials. However, both values were larger than 1, which indicated non-reliance on visual feedback in either the jaw elevator or depressor positioning task. Dental students’ dexterity By one-way blocks ANOVA for the influence of dental students’ dexterity on error scores, a similar ratio was found for both the dentist and non-dentist group (p > 0.05). Only the amplitude ratio in the flexor finger positioning of the dental student group was significantly below that of the non-dentist group (p < 0.05).
Finger versus jaw positioning
Mean vi/nv ratios of the two consecutive trials were compared for equivalent jaw and finger positionings. The r.m.s. and amplitude ratio for finger flexor muscles were significantly smaller than those for jaw depressor muscles (ANOVA multiple comparisons; Bonferronni correction, p < 0.01). In the free-movement positioning task, the mean r.m.s. ratio (SEM) for the finger flexor was 0.6 (0.01); and in the isolated condition, 0.9 (0.1). Both values were significantly lower than the ratio for the jaw depressor muscles [ 1.3 (0.2)]. Similarly, the mean amplitude ratio (SEM) for the finger flexor was 0.6 (0.01) in the free-movement condition and 0.9 (0.6) in the isolated condition,
DISCUSSION Effect of visual feedback on finger positioning
For both free-movement finger-positioning tasks, the positioning error was significantly reduced when visual feedback became available. These data confirmed that the accuracy of limb movement is improved by visual feedback (Adams, 1976; Viallet er al., 1987). The absence of significant differences in the drift variable indicated its lower discriminative power. When only a single joint was kept free while the
rest of the limb was isolated, the similarity between
Table 2. Evaluation of absolute positioning errors with or without visual feedback Mean amplitude* @EM) Finger
Visual feedback No visual feedback Jaw
Visual feedback No visual feedback Mean r.m.s.* GEM)
Isolated positioning
Free-movement positioning Flexor 9.6 (1.1) 14.5 (1.3) ____
Extensor
Flexor
4.0 (0.5) 3.6 (0.7)
4.1 (0.6) 4.6 (0.6)
Elevator
Depressor
Elevator
Depressor
7.9 (0.6) 6.6 (0.6)
-
3.9 (0.5) 2.8 (0.5)
6.2 (0.8) 5.1 (0.6)
Extensor I I.3 (0.8) -12.9 (O.S)t
Isolated positioning
Free-movement positioning
Extensor
Flexor
Visual feedback No visual feedback
2.3 (0.2)
1.9 (0.2)
1.2 (0.2)
0.9 (0. I)
-3.3 (0.2)
-3.5 (0.4)
I.0 (0.1)
1.0 (0.1)
Jaw Visual feedback No visual feedback
Eimator 1.4 (0.1) 1.6 (o.ij
Depressor -
Elevator I.3 (0.1) 0.8 (0.1)
Depressor 1.2 (0.2) I.1 (0.1)
Finger
Extensor
Flexor
-
*Both r.m.s. and amplitude variables are expressed in mm. TUnderlined values for the ‘no visual feedback’ condition indicate that the accuracy of the positioning task was significantly impaired after withdrawal of the visual feedback display.
681
Accuracy of jaw and finger positioning
Extehs6r
verws rlev$tor muscbr r.m.e. ratio (Wnv)
I
2
A)
- __-- _-.__.
__............_. ---
0
I
finger(free)
I
I
finger (boleted)
Extensor
versus
iaw (free)
elevator
I
isw (tie@
muscles
2 :B)
.o
H
2 9
_-
1
0
fingei (free)
finger (isolated)
jaw ifree)
-_.-._.
._.
jaw (is&ted)
Fig. 2. A comparison between the performance of finger extensor and jaw elevator muscles in either the free-movement or the isolated positioning task. The mean vi/nv ratio (SEM) was calculated for both the r.m.s. and amplitude error in all subjects. When the performance with or without visual feedback was similar, the ratio vi/nv was approximately equal to 1 (dashed line). (A) For either the free-movement or the isolated positioning, mean r.m.s. ratios for jaw muscles were higher than for finger muscles. (B) For either the free-movement or the isolated positioning, mean amplitude ratios for jaw muscles were higher than for finger muscles.
682
REINHILDE JACOBS et
the error scores of positioning with or without visual feedback suggested a reduced importance of visual information. The error score of the isolated positioning tasks was much smaller than in the free movements, which made any supplementary reduction of instability negligible. The finger-positioning tasks were carried out without direct visualization of the finger, in accordance with the lack of visual guidance during natural jaw movements. Tracking of an external visual target while the hand is not visible is less accurate than ocuiomotor tracking of the hand (Gauthier and Hofferer, 1976). Eflect of visual feedback on jaw positioning
Visual feedback is known to compensate for the destabilizing effect of gravity when subjects are standing upright (HlavaEka and Saling, 1986). For the head position, visual feedback acting at the level of the neck muscles may increase the positional stability. However, for the jaw, error with visual feedback was equal to or higher than with non-visual feedback, so visual cues seemed unimportant for obtaining accurate jaw positioning while the head was kept immobile. Finger versus jaw positioning
Clear-cut differences in the positioning error were found between jaw and finger muscles, especially in free movements. Comparing the vi/nv ratio for equivalent conditions of jaw and finger performance revealed significantly higher scores for the jaw, even when the positioning tasks of the isolated jawdepressor and finger-flexor muscles were compared. The small vi/ni ratio in the free-movement, fingerpositioning tasks indicated increased error after withdrawal of visual feedback. These data demonstrated the need for visual feedback in order to hold a position accurately with the finger when using either flexor or extensor muscles (Adams, 1976; Viallet et al., 1987). For the jaw-positioning tasks, vi/nv ratios were equal to or higher than 1. Thus, withdrawal of visual feedback did not affect jaw-positioning performance. When considering the isolated positioning tasks, mean vi/nv ratios for the finger were smaller than those of the jaw, although, only for the isolated flexor muscles only, the accuracy of the positioning task was impaired after withdrawal of visual feedback (vi/nv ratio < 1). Pathways
As with limb movements, control of jaw muscles could be modulated from a variety of central regions such as the amygdala, the cerebellum, the somatosensory or orbital areas of the cerebral cortex (Sessle, 1977). Connections between precentral cortex and afferent muscle feedback may be involved in voluntary jaw movements and precise control of mastication (Luschei and Goodwin, 1975; Hoffman and Luschei, 1980). Whereas oculo-manual interactions are well established in man (Gauthier and Hofferer, 1976; Gauthier et al., 1988), the existence of visuo-trigeminal pathways has been demonstrated only in the cat (Tamari
al.
et al., 1974). Tamari et al. (1974) found that photic
stimuli inhibit neurones in the pars oralis of the cat trigeminal nucleus. Nevertheless, the non-visible location of the perioral region in the mouse implies that visual inputs to the superior colliculus are absent, while perioral, somatosensory inputs to the superior colliculus are integrated in tactile-dependent behaviours (Wiener and Hartline, 1987). These findings may explain the absence of a significant impairment of jaw positioning after withdrawal of visual feedback. Accurate jaw positioning seems principally determined by muscular proprioceptive inputs. Indeed, as dentate and edentulous subjects score similarly when matching jaw positions, periodontal or temporomandibular-joint mechanoreceptors do not seem to be essential for sensing jaw position (Christensen and Morimoto, 1977; Lindauer and Gay, 1985; Van Willigen and Broekhuijsen, 1983). One could argue that as the muscle-spindle supply is rather different for jaw and limb muscles, this could explain the different outcome for antigravitational positioning tasks in the two systems. Finger extension is associated with the activation of the m. extensor digitorum (Williams and Warwick, 1980) which contains 0.5 1% spindles (Voss, 1959). The extensor muscles act antigravitationally as do the jaw elevator muscles, which contain numerous spindles (m. masseter 1.12%, m. temporalis 1.42%, m. pterygoideus medialis 2.03%) (Freimann, 1954). The finger flexor muscles (m. flexor digitorum superficialis) (Williams and Warwick, 1980) containing 0.37% spindles (Voss, 1959), should be compared with the jaw-opening muscles. No spindles have been found in either the m. mylohyoideus or m. digastricus in man (Voss, 1956) whereas the relative value for the m. pterygoideus lateralis is about 0.18% (Gill, 1969). The lack of receptors in depressor muscles might be related to the absence of a monosynaptic load-compensation reflex (Lamarre and Lund, 1975). Dental students’ dexterity
The observed difference in the r.m.s. of dental students and non-dental students in the freemovement flexor state only could be due to the dentist’s well-trained coordinational control between eye and hand prehension (Gauthier et al., 1988). The less accurate flexor-muscle performance of dental students in the absence of visual feedback seems to corroborate this. CONCLUSIONS
These results demonstrate the imprecision of maintaining a free-movement finger position in the absence of visual cues. In free movement, the arm acts as a multijointed limb. Such a “four degrees-of-freedom” system requires more complex pathways in response to perturbations (Lacquaniti and Soechting, 1986). This might strongly affect the subject’s performance in the absence of visual feedback. In contrast, the unique anatomy of the jaw implies a bilateral activation of the elevator muscles, which may reduce the impact of visual feedback. More important is the absence of visual guidance for
Accuracy of jaw and finger positioning natural jaw movements. This seems logical, as the jaw does not belong to the visual field. We conclude that the efficiency of jaw positioning
is not determined by visual feedback. It probably relies on the existence of short trigeminal path-ways (Cooker, Larson and Luschei, 1980) and well-developed proprioceptive inputs (Erkelens, unpublished). Visual guidance does not (or hardly) improve the precision of jaw position, which offers a clinical perspective in the case of patients who do not have proper limb control. Acknoi&dgemenrs-We are grateful to J. Geukens for his technical assistance and to M. Nys for all statistical analyses (SAS. Laboratory of Statistics and Experimental Design, Faculty of Agricultural Science, Catholic University Leuven). A. M. Cassin and R. H. Cowie are acknowledged for reviewing the manuscript. This research was sponsored by the National Fund for Scientific Research (N.F.W.O. Belgium). R. Jacobs is a research assistant of the N.F.W.O.
REFERENCES Adams J. A. (1976) Issues for a closed-loop theory of motor learning. In Motor Control: Issues and Trends (Ed. Stelmach G. E.), 1st edn, p. 95. Academic Press, New York. Christensen J. and Morimoto ‘I’.(1977) Dimension discrimination at two different degrees of mouth opening and the effect of anaesthesia applied to the periodontal ligament. J. oral Rehab. 4, 157-164.
Cooker H. S., Larson C. R. and Luschei E. S. (1980) Evidence that the human jaw stretch reflex increases the resistance of the mandible to small displacements. J. Physiol., Lond. 308, 61-78.
Freimann R. (1954) Untersuchungen iiber Anzahl. Lange und Verteilung der Muskelspindeln in den Kaumuskeln der Menschen. Anat. Anz. 100, 258-264. Gauthier G. M. and Hofferer J. M. (1976) Eye tracking of self-moved targets in the absence of vision. Expl Brain Res. 26, 121-139.
Gauthier G. M., Vercher J.-L., Ivaldi F. M. and Marchetti E. (1988) Oculo-manual tracking of visual targets: control learning, coordination control and coordination model. Expl Brain Res. 73, 127-137. Gill H. I. (1969) Muscle spindles in the lateral pterygoid muscle. J. dent. Res. 48, 1048. Hlavafka F. and Saling M. (1986) Compensation effect of visual biofeedback in upright posture control. Acfiu. Nerc. Sup. (Praha) 28, 191-196.
683
Hoffman D. S and Luschei E. S. (1980) Responses of monkey precentral cortical cells during a controlled jaw bite task. J. Neurophysiol. 44, 333-348. Lacquaniti F. and Soechting J. F. (1986) Simulation studies on the control of posture and movement in a multi-jointed limb. Biol. Cybern. 54, 367-378. Lamarre Y. and Lund J. P. (1975) Load compensation in human masseter muscles. J. Physiol. 253, 21-35. Lindauer S. J. and Gay T. (1985) Jaw position sensitivity as a function of degree of mouth opening. J. dent. Res. 62, 265.
Luschei E. and Goodwin G. M. (1975) Role of monkey precentral cortex in control of voluntary jaw movements. J. Neurophysiol. 38, 146157.
Poulton E. C. (1974) Tracking Skill and Manual Control (Ed. Poulton E. C.), 1st edn, pp. 33-37. Academic Press, New York. Sessle B. J. (1977) Identification of alpha and gamma trigeminal motoneurons and effects of stimulation of amygdala, cerebellum and cerebral cortex. Elcpl Neurol. 54, 303-322.
van Steenberghe D., Bonte B., Schols H., Jacobs R. and Schotte A. (1991) The precision of motor control in jaw and limb muscles during isometric contraction in -the oresence of visual feedback. Archs oral Biol. 36. 545-547. Tamari J. W., Naccache A., To’mey G. F. and Jabbur S. J. (1974) Auditory and visual influences on the trigeminal nuclear activity evoked by tooth pulp stimulation in the cat. Expl Neural. 45, 663-666. Van Willigen J. D. and Broekhuijsen M. L. (1983) On the self perception of jaw positions in man. Archs oral Biol. 28, 117-122.
Van Willigen J. D., Broekhuijsen M. L. and Van Der Meer W. J. (1987) The control of bite force in relation to jaw position and load in man. Archs oral Eiol. 32, 525-530. Viallet F., Trouche E.. Beaubaton D. and Legallet E. (1987) The role of visual reafferents during a pointing movement: comparative study between open-loop and closed-loop performances in monkeys before and after unilateral electrolytic lesion of the substantia nigra. E.rp/ Brain Res. 65, 399410.
Voss H. (1956) Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln, im M. frapezius und M. latissimus dorsi. Anat. An:. 103, 443-446.
Voss H. (1959) Weitere Untersuchungen iiber die absolute und relative Zahl der Muskelspindeln in verschiedenen Muskelgruppen (Hiift, Oberschenkelund Unterarmmuskeln) der Menschen. Anar. Anz. 107, 190-197. Wiener S. I. and Hartline P. H. (1987) Perioral but not visual inputs to the flank of the mouse superior colliculus. Neuroscience 21, 557-564. Williams P. L. and Warwick R. (1980) Gray’s Anatomy, 36th edn, pp. 586-593. Churchill Livingstone, Edinburgh.
A&U 0~1 Biol. Vol. 37. NO. 9, pp. 677483, 1992 Copyright 0
Printed in Great Britain. All righu reserved
1992 Pergamon Press Ltd
THE IMPORTANCE OF VISUAL FEEDBACK ON THE ACCURACY OF JAW AND FINGER POSITIONING IN MAN REI;~;HILDEJACOBS,DANIEL VAN STEENBERGHE and AN SCHOITE Department of Periodontology, Laboratory of Oral Physiology, Faculty of Medicine, Catholic University of Leuven, B-3000 Leuven. Belgium (Received
30 October
1991; accepted
I2 May 1992)
Summary-The anatomical position of the mandible means that direct visual feedback is not possible. To clarify the role of visual information, several jaw- and finger-positioning tasks were designed, both in a ‘free-movement’ and an ‘isolated’ (arm or head fixed) state, with or without a visual feedback display of the target position. The subjects had to position the mandible or the index finger of the preferred hand on to a movable metal bar and to maintain a defined position coinciding with the target level provided on an oscilloscope screen. The position signal was tape recorded and computer analysed off-line. Digital filtering differentiated between the drift and the oscillations around the target (root mean square). The results demonstrated a lack of precision in the free-movement, finger-positioning task after withdrawal of visual feedback. For jaw opening and closing muscles, position control was less impaired when a visual feedback display was abolished. It was suggested that the efficiency of jaw positioning is not primarily determined by visual feedback. Key words: proprioception,
finger tremor, jaw position, visual feedback, trigeminal system.
INTRODUCTION
MATERIALS
Subjects
The trigeminal system provides precise position control during size-discrimination tasks (Van Willigen and Broekhuijsen, 1983; Van Willigen, Broekhuijsen and Van Der Meer, 1987). Jaw separations are recognized fairly well with an imagined, a verbally specifited or a physically imposed standard (Van Willigen and Broekhuijsen, 1983). On the other hand, when subjects have to reproduce a particular reference bite force “a mechanism controlling bite-force with any degree of precision is absent in the jaw system” (Van Willigen et al., 1987). We have found that motor control of jaw muscles is less developed than that of limb muscles during isometric contraction, when the target force level was presented by means of visual feedback (van Steenberghe ef nl., 1991). As, unlike limbs, one cannot see one’s own jaw, this may explain the poor performance. Accuracy of limb movement is improved by visual feedback (Adams, 1976). For tracking performance of limb muscles, two types of visual feedback are usually available: visual feedback of the target and direct visual feedback of the moving limb itself. For the jaw, evidently only the former applies. The assumption is that jaw position control is not dependent on visual feedback. To confirm this model, we have now sought to clarify the role of visual cues in a jaw-positioning task. Abbreviarions:
The subjects were 32 healthy volunteers (21 females, 11 males; 19-29 yr of age, mean age 21). half of them dental students, without clinical evidence of occlusal abnormalities or craniomandibular dysfunction. They all gave informed consent without being aware of the purpose of the experiment. Experimental procedure
To compare equivalent muscle groups in both motor systems, the experiment involved positioning tasks with flexor or extensor muscles of the preferred index finger and jaw depressor or elevator muscles, either in an isolated or a free-movement condition (Table 1). Subjects were seated comfortably on a dental chair in a dark room in an upright position in front of the positioning device. They had to position the index finger of the preferred hand [Fig. l(A)] or the mandible [Fig. l(B)] on to a movable metal bar. Isolated versus free-movement finger position [Fig. f(A)]. In the free-movement finger-positioning
tasks, flexor or extensor muscles were activated while the upper arm was kept vertically down by the body and the forearm at 90” to the body. Thus, only the hand and the fingers could be moved. Then, the finger had to position the bar 18 mm upwards, counteracting a 0.12-O. 15 N load. In the isolated finger-positioning tasks, the forearm was fixed in a plastic cylinder and the wrist and the fingers, except for the metacarpophalangeal joint of the index finger, were immobilized by a strap. The
ANOVA, analysis of variance; LVDT, linear
variable-displacement
AND METHODS
transducer. 677
678
FSINHILDEJACOBS
er al.
Table I. Comparison of jaw and finger muscles with an equivalent function Free-movement positioning (s) Finger
Extensor
Visual feedback ;:; (b) (d)
No visual feedback
Isolated positioning (s)
Flexor O-30 60-90 30-60 90-120
k”,’ (b) (d)
Free-movement positioning (s) Jaw
Elevator
Visual feedback
O-30 i:,’ 60-90 (b) 30-60 (d) 90420
No visual feedback
Flexor O-30 60-90 3cMo 90-120
Isolated positioning (s)
Depressor No No No No
Extensor
test* test test test
Elevator i:; (b) (d)
Depressor O-30 60-90 30-60 90-120
For each muscle group, two trials were made. A trial consisted of a standard run of 30 s with visual feedback provided (a, c) followed by a 30 s-run without visual feedback (b. d). The error score during the visual feedback task was expressed as a proportion of the error score during the non-visual feedback condition. The vi/nv ratios for the r.m.s., amplitude and drift
error were computed as follows: error(a)/error(b), error(c)/error(d). *The jaw depressor muscles were not tested in the free-movement condition.
stretched index finger was held against gravity and had to align the finger signal with the horizontal baseline on the oscilloscope screen by activating either the flexor or extensor muscles. Isolated [Fig. I(B)].
versus
free-movement
jaw
position
In the free-movement, jaw-positioning task, the head rested against an occipital support while subjects had to keep the vertical head position stable. The metal bar was directed upwards by the mandible from a 30-35 mm to a 12-17 mm degree of mouth opening. The isolated jaw-positioning task consisted of activating the elevator muscles while the head was fixed to the headrest and the neck muscles were inactivated by means of a strap. Finally, to evaluate feedback on the jaw-opening muscles, the subjects lay supine with the head in hyperextension (= isolated positioning task). They were instructed to maintain a defined jaw position while the bar was resting on the lower border of the chin. The jaw opening varied between 5 and 10 mm. An LVDT contacted the opposite side of the metal bar and monitored movement in a vertical plane. The vertical displacements were monitored by means of an LVDT connected to the bar. The transducer was able to detect a displacement of 25 pm. The output of the LVDT was displayed on an oscilloscope screen set at eye level 1 m in front of the subjects. An LVDT displacement of 1 mm corresponded to 12 mm displacement on the screen. Subjects had to align the finger or jaw signal with a stationary horizontal baseline presented on the screen, which meant that the limb studied counteracted gravity and the small load of the transducer (0.12-O. 15 N). Only visual feedback of the target and the subject’s output signal were available. There was no direct visualization of the moving limb. For each muscle group, two trials were made. A trial consisted of a standard run of 30 s, with visual feedback, followed by a 30-s run without visual feedback, while subjects kept their eyes closed. Test trials were separated by a 10-s rest.
To avoid learning bias, the subjects were familiarized with the procedure before the actual experiments and for a few seconds only (Poulton, 1974). The testing sequence of all muscle groups was randomized. Calculations and statistics
Data were collected on an Ampex PR 2230 tape recorder and A/D converted at a sample frequency of 1000 Hz to transfer voltages in the -2/f 2 V range to binary values for analysis on an AT computer. The overall efficiency of performance was evaluated by means of the root mean square (r.m.s.) error calculation, which is compatible with parametric statistical tests (Poulton, 1974). It calculated the difference in position between the target level and the output of the transducer after digital high-pass filtering to get rid of the low-set signal (drift). Thus, the r.m.s. error was estimated very precisely from a central 16-s section of the record of the filtered signal, which oscillated around the target level. To exclude large positioning errors (large r.m.s. values) the preceding and following 7-s sections were discarded. Additional measures of error were the amplitude error (subtracting the minimal from the maximal amplitude of the subject’s response) and the drift (low-set signal). The drift indicated that the average response was above or below the target level. However, if the subject’s response changed direction over time, this value was not very useful. All statistical calculations were made with the statistical analysis system. A level of significance of 5% was chosen, unless otherwise stated. The ANOVA multiple comparisons method (Bonferronni correction) was applied to detect differences between the performance with and without visual feedback for each particular muscle group. Afterwards, the error score during the visual feedback task (=vi) was expressed as a proportion of the error score without visual feedback (= nv) for all variables considered (r.m.s., amplitude and drift). The ratio of
Accuracy of jaw and finger positioning
679
(4
'SJLATED CONOiTION
TED CONCiliON
UD A9 LA C K
(8) ISOLATED
C0t401T10~
CONDITION
i ~SOCATEII
CONDI’ION
AB L A C K
Fig. 1. A positioning task consisted of positioning the index finger of the preferred hand (A) or the mandible (B) on to a movable metal bar. Vertical displacements were monitored by linear variable displacement transducer LVDT connected to the bar. All signals were digitalized and high-pass filtered to get rid of the low-set signal (path I). The output of the LVDT was also displayed on an oscilloscope screen (path II). Subjects had to align their positioning signal with a stationary horizontal baseline presented on the screen. Afterwards, the visual display was abolished, while subjects closed their eyes. (A) In the free-movement finger-positioning tasks (unrestrained condition), flexor or extensor muscles were activated. Only the hand and the fingers could be moved. In the isolated finger-positioning task, the upper arm was fixed in a plastic cylinder with the wrist and fingers immobilized by a strap (isolated condition). (B) In the free-movement jaw-positioning task, the head rested against an occipital support, while the subject kept the vertical head position stable (unrestrained condition). In the isolated jaw-positioning task, the head was fixed to the headrest of a dental chair, while the neck muscles were immobilized by means of a strap (isolated condition). In the experimental set-up for the jaw depressor muscles, the subject lay supine (isolated condition). The metal bar was supported by the lower chin border.
680
REINHILDE
performances with/without visual feedback (vi/nv ratio) were compared for jaw- and finger-muscle groups with an equivalent function-jaw elevator (depressor) muscles versus limb extensor (flexor) muscles (ANOVA multiple comparisons method; Bonferronni correction). Finally, a one-way blocks ANOVA was used to evaluate the influence of the dental students’ manual dexterity. RESULTS Eflect of visual feedback
Data were first analysed by means of the ANOVA multiple comparisons method (Bonferronni correction: p < 0.001). For both free-movement finger positionings, visual feedback significantly reduced the positioning error (r.m.s., amplitude). No such differences were detected when considering the isolated positioning tasks or when evaluating jaw positioning tasks (Table 2). Several oscillations during the imposed positioning prevented any significant difference in the drift values (p > 0.05). This measure was considered as less sensitive and omitted from further statistical analysis.
Jacoas et al. which was significantly lower than the ratio for the jaw depressor muscles [ 1.2 (0. l)]. A comparison between the extensor muscles of the hand and the elevator muscles of the jaw revealed significantly higher jaw vi/nv ratios only in the free movements (p < 0.01). In these, vi/nv ratios for the finger were often smaller than I, indicating an increased error score when visual feedback was absent (Fig. 2). On the other hand, all vi/nv ratios for the jaw positioning were approximately equal to or greater than 1 (Fig. 2). Furthermore, r.m.s. vi/nv ratios were significantly higher in the isolated jaw-depressor muscle trials than in the isolated elevator muscle trials. However, both values were larger than 1, which indicated non-reliance on visual feedback in either the jaw elevator or depressor positioning task. Dental students’ dexterity By one-way blocks ANOVA for the influence of dental students’ dexterity on error scores, a similar ratio was found for both the dentist and non-dentist group (p > 0.05). Only the amplitude ratio in the flexor finger positioning of the dental student group was significantly below that of the non-dentist group (p < 0.05).
Finger versus jaw positioning
Mean vi/nv ratios of the two consecutive trials were compared for equivalent jaw and finger positionings. The r.m.s. and amplitude ratio for finger flexor muscles were significantly smaller than those for jaw depressor muscles (ANOVA multiple comparisons; Bonferronni correction, p < 0.01). In the free-movement positioning task, the mean r.m.s. ratio (SEM) for the finger flexor was 0.6 (0.01); and in the isolated condition, 0.9 (0.1). Both values were significantly lower than the ratio for the jaw depressor muscles [ 1.3 (0.2)]. Similarly, the mean amplitude ratio (SEM) for the finger flexor was 0.6 (0.01) in the free-movement condition and 0.9 (0.6) in the isolated condition,
DISCUSSION Effect of visual feedback on finger positioning
For both free-movement finger-positioning tasks, the positioning error was significantly reduced when visual feedback became available. These data confirmed that the accuracy of limb movement is improved by visual feedback (Adams, 1976; Viallet er al., 1987). The absence of significant differences in the drift variable indicated its lower discriminative power. When only a single joint was kept free while the
rest of the limb was isolated, the similarity between
Table 2. Evaluation of absolute positioning errors with or without visual feedback Mean amplitude* @EM) Finger
Visual feedback No visual feedback Jaw
Visual feedback No visual feedback Mean r.m.s.* GEM)
Isolated positioning
Free-movement positioning Flexor 9.6 (1.1) 14.5 (1.3) ____
Extensor
Flexor
4.0 (0.5) 3.6 (0.7)
4.1 (0.6) 4.6 (0.6)
Elevator
Depressor
Elevator
Depressor
7.9 (0.6) 6.6 (0.6)
-
3.9 (0.5) 2.8 (0.5)
6.2 (0.8) 5.1 (0.6)
Extensor I I.3 (0.8) -12.9 (O.S)t
Isolated positioning
Free-movement positioning
Extensor
Flexor
Visual feedback No visual feedback
2.3 (0.2)
1.9 (0.2)
1.2 (0.2)
0.9 (0. I)
-3.3 (0.2)
-3.5 (0.4)
I.0 (0.1)
1.0 (0.1)
Jaw Visual feedback No visual feedback
Eimator 1.4 (0.1) 1.6 (o.ij
Depressor -
Elevator I.3 (0.1) 0.8 (0.1)
Depressor 1.2 (0.2) I.1 (0.1)
Finger
Extensor
Flexor
-
*Both r.m.s. and amplitude variables are expressed in mm. TUnderlined values for the ‘no visual feedback’ condition indicate that the accuracy of the positioning task was significantly impaired after withdrawal of the visual feedback display.
681
Accuracy of jaw and finger positioning
Extehs6r
verws rlev$tor muscbr r.m.e. ratio (Wnv)
I
2
A)
- __-- _-.__.
__............_. ---
0
I
finger(free)
I
I
finger (boleted)
Extensor
versus
iaw (free)
elevator
I
isw (tie@
muscles
2 :B)
.o
H
2 9
_-
1
0
fingei (free)
finger (isolated)
jaw ifree)
-_.-._.
._.
jaw (is&ted)
Fig. 2. A comparison between the performance of finger extensor and jaw elevator muscles in either the free-movement or the isolated positioning task. The mean vi/nv ratio (SEM) was calculated for both the r.m.s. and amplitude error in all subjects. When the performance with or without visual feedback was similar, the ratio vi/nv was approximately equal to 1 (dashed line). (A) For either the free-movement or the isolated positioning, mean r.m.s. ratios for jaw muscles were higher than for finger muscles. (B) For either the free-movement or the isolated positioning, mean amplitude ratios for jaw muscles were higher than for finger muscles.
682
REINHILDE JACOBS et
the error scores of positioning with or without visual feedback suggested a reduced importance of visual information. The error score of the isolated positioning tasks was much smaller than in the free movements, which made any supplementary reduction of instability negligible. The finger-positioning tasks were carried out without direct visualization of the finger, in accordance with the lack of visual guidance during natural jaw movements. Tracking of an external visual target while the hand is not visible is less accurate than ocuiomotor tracking of the hand (Gauthier and Hofferer, 1976). Eflect of visual feedback on jaw positioning
Visual feedback is known to compensate for the destabilizing effect of gravity when subjects are standing upright (HlavaEka and Saling, 1986). For the head position, visual feedback acting at the level of the neck muscles may increase the positional stability. However, for the jaw, error with visual feedback was equal to or higher than with non-visual feedback, so visual cues seemed unimportant for obtaining accurate jaw positioning while the head was kept immobile. Finger versus jaw positioning
Clear-cut differences in the positioning error were found between jaw and finger muscles, especially in free movements. Comparing the vi/nv ratio for equivalent conditions of jaw and finger performance revealed significantly higher scores for the jaw, even when the positioning tasks of the isolated jawdepressor and finger-flexor muscles were compared. The small vi/ni ratio in the free-movement, fingerpositioning tasks indicated increased error after withdrawal of visual feedback. These data demonstrated the need for visual feedback in order to hold a position accurately with the finger when using either flexor or extensor muscles (Adams, 1976; Viallet et al., 1987). For the jaw-positioning tasks, vi/nv ratios were equal to or higher than 1. Thus, withdrawal of visual feedback did not affect jaw-positioning performance. When considering the isolated positioning tasks, mean vi/nv ratios for the finger were smaller than those of the jaw, although, only for the isolated flexor muscles only, the accuracy of the positioning task was impaired after withdrawal of visual feedback (vi/nv ratio < 1). Pathways
As with limb movements, control of jaw muscles could be modulated from a variety of central regions such as the amygdala, the cerebellum, the somatosensory or orbital areas of the cerebral cortex (Sessle, 1977). Connections between precentral cortex and afferent muscle feedback may be involved in voluntary jaw movements and precise control of mastication (Luschei and Goodwin, 1975; Hoffman and Luschei, 1980). Whereas oculo-manual interactions are well established in man (Gauthier and Hofferer, 1976; Gauthier et al., 1988), the existence of visuo-trigeminal pathways has been demonstrated only in the cat (Tamari
al.
et al., 1974). Tamari et al. (1974) found that photic
stimuli inhibit neurones in the pars oralis of the cat trigeminal nucleus. Nevertheless, the non-visible location of the perioral region in the mouse implies that visual inputs to the superior colliculus are absent, while perioral, somatosensory inputs to the superior colliculus are integrated in tactile-dependent behaviours (Wiener and Hartline, 1987). These findings may explain the absence of a significant impairment of jaw positioning after withdrawal of visual feedback. Accurate jaw positioning seems principally determined by muscular proprioceptive inputs. Indeed, as dentate and edentulous subjects score similarly when matching jaw positions, periodontal or temporomandibular-joint mechanoreceptors do not seem to be essential for sensing jaw position (Christensen and Morimoto, 1977; Lindauer and Gay, 1985; Van Willigen and Broekhuijsen, 1983). One could argue that as the muscle-spindle supply is rather different for jaw and limb muscles, this could explain the different outcome for antigravitational positioning tasks in the two systems. Finger extension is associated with the activation of the m. extensor digitorum (Williams and Warwick, 1980) which contains 0.5 1% spindles (Voss, 1959). The extensor muscles act antigravitationally as do the jaw elevator muscles, which contain numerous spindles (m. masseter 1.12%, m. temporalis 1.42%, m. pterygoideus medialis 2.03%) (Freimann, 1954). The finger flexor muscles (m. flexor digitorum superficialis) (Williams and Warwick, 1980) containing 0.37% spindles (Voss, 1959), should be compared with the jaw-opening muscles. No spindles have been found in either the m. mylohyoideus or m. digastricus in man (Voss, 1956) whereas the relative value for the m. pterygoideus lateralis is about 0.18% (Gill, 1969). The lack of receptors in depressor muscles might be related to the absence of a monosynaptic load-compensation reflex (Lamarre and Lund, 1975). Dental students’ dexterity
The observed difference in the r.m.s. of dental students and non-dental students in the freemovement flexor state only could be due to the dentist’s well-trained coordinational control between eye and hand prehension (Gauthier et al., 1988). The less accurate flexor-muscle performance of dental students in the absence of visual feedback seems to corroborate this. CONCLUSIONS
These results demonstrate the imprecision of maintaining a free-movement finger position in the absence of visual cues. In free movement, the arm acts as a multijointed limb. Such a “four degrees-of-freedom” system requires more complex pathways in response to perturbations (Lacquaniti and Soechting, 1986). This might strongly affect the subject’s performance in the absence of visual feedback. In contrast, the unique anatomy of the jaw implies a bilateral activation of the elevator muscles, which may reduce the impact of visual feedback. More important is the absence of visual guidance for
Accuracy of jaw and finger positioning natural jaw movements. This seems logical, as the jaw does not belong to the visual field. We conclude that the efficiency of jaw positioning
is not determined by visual feedback. It probably relies on the existence of short trigeminal path-ways (Cooker, Larson and Luschei, 1980) and well-developed proprioceptive inputs (Erkelens, unpublished). Visual guidance does not (or hardly) improve the precision of jaw position, which offers a clinical perspective in the case of patients who do not have proper limb control. Acknoi&dgemenrs-We are grateful to J. Geukens for his technical assistance and to M. Nys for all statistical analyses (SAS. Laboratory of Statistics and Experimental Design, Faculty of Agricultural Science, Catholic University Leuven). A. M. Cassin and R. H. Cowie are acknowledged for reviewing the manuscript. This research was sponsored by the National Fund for Scientific Research (N.F.W.O. Belgium). R. Jacobs is a research assistant of the N.F.W.O.
REFERENCES Adams J. A. (1976) Issues for a closed-loop theory of motor learning. In Motor Control: Issues and Trends (Ed. Stelmach G. E.), 1st edn, p. 95. Academic Press, New York. Christensen J. and Morimoto ‘I’.(1977) Dimension discrimination at two different degrees of mouth opening and the effect of anaesthesia applied to the periodontal ligament. J. oral Rehab. 4, 157-164.
Cooker H. S., Larson C. R. and Luschei E. S. (1980) Evidence that the human jaw stretch reflex increases the resistance of the mandible to small displacements. J. Physiol., Lond. 308, 61-78.
Freimann R. (1954) Untersuchungen iiber Anzahl. Lange und Verteilung der Muskelspindeln in den Kaumuskeln der Menschen. Anat. Anz. 100, 258-264. Gauthier G. M. and Hofferer J. M. (1976) Eye tracking of self-moved targets in the absence of vision. Expl Brain Res. 26, 121-139.
Gauthier G. M., Vercher J.-L., Ivaldi F. M. and Marchetti E. (1988) Oculo-manual tracking of visual targets: control learning, coordination control and coordination model. Expl Brain Res. 73, 127-137. Gill H. I. (1969) Muscle spindles in the lateral pterygoid muscle. J. dent. Res. 48, 1048. Hlavafka F. and Saling M. (1986) Compensation effect of visual biofeedback in upright posture control. Acfiu. Nerc. Sup. (Praha) 28, 191-196.
683
Hoffman D. S and Luschei E. S. (1980) Responses of monkey precentral cortical cells during a controlled jaw bite task. J. Neurophysiol. 44, 333-348. Lacquaniti F. and Soechting J. F. (1986) Simulation studies on the control of posture and movement in a multi-jointed limb. Biol. Cybern. 54, 367-378. Lamarre Y. and Lund J. P. (1975) Load compensation in human masseter muscles. J. Physiol. 253, 21-35. Lindauer S. J. and Gay T. (1985) Jaw position sensitivity as a function of degree of mouth opening. J. dent. Res. 62, 265.
Luschei E. and Goodwin G. M. (1975) Role of monkey precentral cortex in control of voluntary jaw movements. J. Neurophysiol. 38, 146157.
Poulton E. C. (1974) Tracking Skill and Manual Control (Ed. Poulton E. C.), 1st edn, pp. 33-37. Academic Press, New York. Sessle B. J. (1977) Identification of alpha and gamma trigeminal motoneurons and effects of stimulation of amygdala, cerebellum and cerebral cortex. Elcpl Neurol. 54, 303-322.
van Steenberghe D., Bonte B., Schols H., Jacobs R. and Schotte A. (1991) The precision of motor control in jaw and limb muscles during isometric contraction in -the oresence of visual feedback. Archs oral Biol. 36. 545-547. Tamari J. W., Naccache A., To’mey G. F. and Jabbur S. J. (1974) Auditory and visual influences on the trigeminal nuclear activity evoked by tooth pulp stimulation in the cat. Expl Neural. 45, 663-666. Van Willigen J. D. and Broekhuijsen M. L. (1983) On the self perception of jaw positions in man. Archs oral Biol. 28, 117-122.
Van Willigen J. D., Broekhuijsen M. L. and Van Der Meer W. J. (1987) The control of bite force in relation to jaw position and load in man. Archs oral Eiol. 32, 525-530. Viallet F., Trouche E.. Beaubaton D. and Legallet E. (1987) The role of visual reafferents during a pointing movement: comparative study between open-loop and closed-loop performances in monkeys before and after unilateral electrolytic lesion of the substantia nigra. E.rp/ Brain Res. 65, 399410.
Voss H. (1956) Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln, im M. frapezius und M. latissimus dorsi. Anat. An:. 103, 443-446.
Voss H. (1959) Weitere Untersuchungen iiber die absolute und relative Zahl der Muskelspindeln in verschiedenen Muskelgruppen (Hiift, Oberschenkelund Unterarmmuskeln) der Menschen. Anar. Anz. 107, 190-197. Wiener S. I. and Hartline P. H. (1987) Perioral but not visual inputs to the flank of the mouse superior colliculus. Neuroscience 21, 557-564. Williams P. L. and Warwick R. (1980) Gray’s Anatomy, 36th edn, pp. 586-593. Churchill Livingstone, Edinburgh.