PERI-ORAL REFLEXES IN THE CONSCIOUS

MONKEY (MACACA MULATTA)

C. R. LARSON and D. SUTTON

Department of Speech and Hearing Sciences, Virginia Mason Research Center. and Regional Primate Research Center, University of Washington.

Seattle. WA 98195, U.S.A.

Summary-Three rhesus monkeys were trained to exert simultaneous forces with their jaws and lips against force transducers. The lip transducer was coupled to a servocontrolled electro- magnet stimulator. Electromyographic (EMG) activity was recorded from orbicularis oris (00s) and medial pterygoid (MPT) muscles. Elevation or depression of the lip-force transducer with the electromagnet elicited reflexes in the lip- and jaw-closing muscles. Reflex amplitudes elicited by stretching the 00s were logarithmically related to stimulus velocity. Depression of the lip-force transducer released pre-existing stretch of the 00s muscle and elicited reflexes in the 00s and MPT. The amplitudes of the reflexes elicited by the release stimuli were slightly greater than those elicited by stretching the lip. There was no short latency suppression of the 00s EMG following the release stimulus. The perioral reflex of the macaque appears to be similar to that of man; there appear to be no normal-acting muscle spindles in the 00s muscle.

INTRODUCTION

Reflex testing is often used for investigating normal and abnormal neural functions (Ruth and Patton, 1965). A thorough understanding of reflexes in motor control necessitates knowledge of their effective stimuli. but most studies of facial reflexes have not been sufficiently specific with regard to the effective stimuli. The most extensively studied facial reflex is the blink reflex. Lindquist and Martensson (1969, 1970) found that afferent trigeminal fibres of cats re- spond to sustained contraction of a muscle and that single afferent fibres respond to stimulation of indivi- dual hairs, vibrissae, or light touch of the skin. There is no indication that muscle contraction leads to affer- ent activity from receptors located within the muscle itself (Lindquist and Martensson, 1969, 1970; Shahani and Young, 1973). Moreover, Shahani and Young (1973) showed that in anaesthetized monkeys the blink reflex is elicited by stimulation of cutaneous receptors. It has, therefore, been suggested that facial muscle contraction excites receptors located in the skin, which then relay information about the state of muscle stretch and tension (Lindquist and Mar- tensson. 1970; Shahani, 1970).

The mechanisms involved in the peri-oral reflex are not well understood, although it may play an impor- tant role in articulation, mastication and expression. To understand the human peri-oral reflex, it is necess- ary to rely on animal experimentation, as most work on receptor physiology (Dubner, Sumino and Stark- man, 1974: Kirkpatrick and Kruger, 1975) and brain stem mechanisms (Tanaka, Yu and Kitai, 1971) has been done on animals. To relate these data to man is particularly difficult in the case of the peri-oral reflex. Lindquist and Martensson (1970) obtained no response in orbicularis oris muscle to mechanical stimulation of any part of the face of anaesthetized cats. We have likewise had difficulty in mechanically

eliciting peri-oral reflexes in anaesthetized monkeys. However, we have developed a technique for eliciting and recording peri-oral reflexes in the conscious mon- key under highly-controlled conditions. The stimu- lator we use enables precise control of the physical parameters of the mechanical stimulus.

METHODS

Subjects

Three rhesus monkeys (Macacu mulatra). weighing 3.0-3.4 kg, were used.

Apparatus

All training was conducted in a sound-attenuated room. Monkeys were placed in a primate-restraining chair for daily training and testing. and their heads restrained by a V-shaped bracket at the occiput which held the muzzle between two vertical pillars (Fig. 1). A complex system for recording jaw and lip forces, delivering apple juice reinforcement and eliciting reflexes was placed in the animal’s mouth (Fig. 1). The jaw force transducer consisted of two stainless steel beams (1 x 6 x 0.25 cm) separated by 4mm. Each beam was equipped with foil type bonded strain gauges. The lip transducer was a 1 x 5 x 0.1 cm stainless steel beam equipped with strain gauges. A lo-pm deflection of the lip-force transducer corre- sponded to a force of 0.14 N. A 100~pm deflection of each beam of the jaw-force transducer corre- sponded to a force of 2.4N. The lip transducer was coupled to a servocontrolled electromagnet. providing a means for delivering controlled mechanical stimuli to the lips.

The position-sensitive servocontrolled electromag- net consisted of a speaker magnet fastened to an alu- minum base. A shaft carrying an electrical coil tra- velled on low-friction bearings through the centre of the magnet. At one end was a Hewlett-Packard linear

865

866 C. R. Larson and D. Sutton

variable differential transformer (LVDT) and at the other was the lip force transducer. The electrical coil was driven by a power amplifier regulated by elec- tronic feedback circuitry from the LDVT in conjunc- tion with amplification and shaping circuitry. The compliance of the stimulator was less than 0.1 mm/N.

Displacement of the electrical coil, shaft and lip- force transducer with ramp functions was produced by integrating square waves from a Grass S88 stimu- lator via an op amp circuit. The resulting ramp func- tions were led directly to the LVDT control appar- atus.

Training procedure

At the start of training only the jaw-force trans- ducer was used; when the monkey bit on it with a force of at least 2.4 N for 100 ms he was rewarded with apple juice. The force duration was gradually lengthened by small increments to 5OOms. Then the lip force transducer was introduced and window com- parators and logic circuitry programmed to require the animal to exert simultaneously a closing force with the jaws and a downward force with the upper lip. It was important that the animal’s head be held relatively motionless and that the lip- and jaw-force transducers be properly placed in the animal’s mouth.

The jaw-force transducer was positioned with the ends of the beams 4mm inside the inner edge of the incisors. The lip transducer was placed under the upper lip with its front edge 2mm anterior to the incisors. With the jaw- and lip-force transducers in place, the animals could exert the required forces by simultaneously biting and contracting the lip muscles. If the monkey maintained appropriate forces for a specified period, he was rewarded with apple juice delivered directly into his mouth through a stainless steel tube attached to the underside of the upper force beam. A 3-s rest followed the reward. Cue lights in front of the animal indicated the end of the rest period (white light) and gave the animal information about jaw- and lip-force levels. Jaw force of a pre- selected correct band width produced an amber light. Lip forces were signalled as too low (blue light), too high (red light) or the proper level (green light).

After 3 months training, the animals maintained jaw-bite forces of 2.4-4.8 N, and concurrently exerted lip forces of 0.140.44 N during each trial. They main- tained both forces for 2s.

Rejlex testing

At the beginning of the experimental session, bi- polar hooked wire electromyographic (EMG) elec-

TRANSDUCER

Fig. 1. (A) Orientation of the mechanical stimulator and force transducers with respect to the monkey. (B) Position of the force transducers within the animal’s mouth. Activation of the electromagnet dis-

placed the lip-force transducer and upper lip as indicated in (C).

Pert-oral reflexes m the consctous monkey (Mucuctr mularrtl) X67

Fig. 2. Averaged reflexes ehcited by various sttmuh. In each case. the sttmulus analog IS shown at the top wtth recttfied and averaged orbicularis oris (00s) and medial pterygoid (MPT) EMG traces below Veloctty of release and stretch stimuli (top) was 330 mm/s. (b-d) Show reflexes elictted by ramp veloctttes of 200, 100, 60 and 50mm/s with l.O-mm amplitude. Ttme base is IOms. (fl and

(g) illustrate mdivtdual reflexes: EMG not recttfied. Time base. 5 ms.

nodes were Inserted 0.5 cm lateral to the midline of

the upper lip. A second set was inserted into the medial pterygoid muscle (MPT) on the right side. Re- flexes were elicited by activating the electromagnet which either stretched the lip by elevating the lip- force transducer (stretch stimulus), or released stretch by lowering the transducer (stretch-release stimulus). The experimenter triggered the stimulator at random times during the period while the monkey was main- taining isometric force contractions with jaw and lips. The stimulator stretched the lip with 0.5- and l.O-mm amplitude ramp functions, attaining velocities of 30_330mm/s. Release stimuli of 0.5- and l.O-mm amplitude were also presented. Ramp plateaus were maintained for several hundred milliseconds. For each ramp duration and amplitude, 20 repetitions of the stimulus were presented.

Force, EMG signals and the stimulus analog signal were stored on magnetic tape. The 20 EMG reflexes elicited under each stimulus condition were later rec- tified, averaged with an averaging computer and printed out on an X--Y plotter. Measurements of reflex amplitudes were done manually from the plots. Latencies were measured from the onset of the ramp to the beginning of the first component of the perioral reflex. Stimulus velocities were calculated from ramp durations and amplitudes. Photographs of individual reflexes were made from a storage oscilloscope.

RESULTS

Examples of average reflexes from one monkey eli- cited by mechanical stimulation of the lip are shown in Fig. 2. While the monkey was contracting the lip and jaw muscles with the required force, a stretch stimulus of 330 mm/s velocity (1.0 mm amplitude and 3 ms duration) elicited a reflex in the lip musculature

beginning at 68 ms, peaking at 12 ms, and followed by suppression of EMG activity for 80 ms. Individual reflexes in Fig. 2g show that, occasionally. a second excitatory reflex follows the first. with a latency of 15530 ms. The lip stimulus also elicited reflexes in the MPT. The first excitatory component was quite short at a latency of 6 ms (Fig. 2g). but did not occur following every stimulus. A more consistent excitatory reflex was observed at 10-20ms latency, which was followed by EMG suppression until 30ms (Figs 2a and b). A second phase of EMG suppression followed at 4C-50ms.

A 330-mm/s velocity release stimulus to the hp eli- cited lip and jaw reflexes with latencies similar to those elicited by the stretch stimulus. Reflexes elicited by the release stimulus had slightly greater amplitudes than those elicited by the stretch stimulus.

Ramp stretch stimuli of slower velocities also eli- cited reflexes in the lip and jaw muscles (Fig. 2). The latencies of the reflexes elicited by slower velocity stimuli were the same as those elicited by the higher velocity stimuli. The amplitude of the lip reflex de- creased as the velocity of the stimulus decreased: velocities of 30mm/s elicited no reflexes. The ampli- tude of the MPT excitatory reflex was also reduced as the stimulus velocity decreased. Velocities of 30-60 mm/s often produced no detectable inhibition of the EMG.

Figure 3 shows the relationship between the lip reflex amplitude and stimulus velocity. Peri-oral reflex amplitudes for each monkey at each stimulus velocity were converted to a percentage of the reflex elicited by the 330-mm/s release stimulus. The per cent reflex values for the 3 monkeys were plotted as a function of stimulus velocity (Fig. 3, top) and log velocity (Fig. 3, bottom). Minor changes in reflex amplitude as a function of magnitude of displacement suggest that velocity has a greater effect on peri-oral reflexes than does displacement.

868 C. R. Larson and D. Sutton

DISCUSSION

Our results agree with those obtained from other experiments on animal and human peri-oral reflexes. The latencies of the peri-oral reflex are similar to those of the cat blink reflex (Lindquist and Martens- son, 1970), but slightly shorter than that elicited m man using similar techniques (Larson et LII., 1978). which is to be expected in view of the relative conduc- tion distances in the macaque monkey, cat and man. Our finding of a logarithmic relationship between peri-oral reflex amplitude and ramp velocity is con- sistent with that in the human peri-oral reflex (Larson Yt al., 1978). The velocity relationship of the peri-oral reflex indicates that the reflex mechanisms of orofacial regions in both man and macaques are similar with respect to the adequate stimuli for the perl-oral re- flexes. Thus, human and non-human primates prob- ably have similar sensory receptors and bulbar synap- tic arrangements, allowing comparisons between their oromotor mechanisms.

Because of the velocity range to which the peri-oral reflex is sensitive, inferences can be made regarding the types of naturally occurring stimuli that trigger afferent signals to the brain stem and the way such input could be used for the on-going control of lip

. 2 al u L

a IOO- a

4 75-

,’ -a E 0

s - 2 25-

l?z

I 005 01 03

Sttmulus velocity, m/s

A

‘i 0

Stimulus velocity, m/s

Fig. 3. Reflex amplitude plotted as a function of stimulus velocity (top) and log stimulus velocity (bottom). Reflex percentages were calculated from the amplitude of the reflex elicited by the 330-mm/s release stimulus. Open sym- bols refer to OS-mm amphtude stretches for each monkey. Closed symbols indicate l.O-mm amplitude stretches. The regression line in the top figure was estimated visually. Linear regression analysis was applied to the data below.

Goodness of fit was r = 0.92.

motor activity. The most rapid lip movements we observed were lip-smacking behaviour at about 6 smacks per s. This translates roughly to lip velocities of about lOOmm,‘s for lip displacements of 1 cm. The velocity of lip movement in the macaque monkey falls within the range of peri-oral lip-reflex sensittvity

(Fig. 3). Stimulus velocities less than 50mm/s do not reliably elicit reflexes, suggesting that lip movements with velocities greater than 50mm/s trigger afferent signals related to the rate of lip movement in the monkey. This suggestion is supported by the finding of Zucker and Welker (1969) that muscle contraction excites cutaneous receptors in the peri-oral region of the rat.

To understand the types of sensory receptors in the peri-oral region which may be involved in the reflexes we observed. it is necessary to draw inferences from previous work. Our data do not determine whether the peri-oral receptors themselves are respon- sive to stimulus velocity, although we know the reflex system as a whole is sensitive to stimulus velocity The system may accomplish this by responding di- rectly to velocity-sensitive receptors, by differentiating displacement-sensitive receptors, or by integrating acceleration-sensitive receptors. Earlier workers established that cutaneous receptors m the peri-oral region of cats and rats are sensitive to both displace- ment and velocity (Hahn, 1971; Rowe and Sessle, 1972: Zucker and Welker, 1969: Darian-Smith, Rowe and Sessle, 1968). Moreover, there does not appear to be much modulation of the in-coming afferent sig- nals across the first synapse to the second-order neurons m the main sensory nucleus of the trigeminal (Darian-Smith, 1966; Darian-Smith et al., 1968: Kerr et al.. 1968: Kirkpatrick and Kruger, 1975: Rowe and Sessle, 1972).

The sensory innervation of the monkey peri-oral region is similar to that of the cat and rat, with both rapidly and slowly adapting fibres present in the infra-orbital nerve of the monkey (Dubner et al., 1974: Sumino. Dubner and Starkman, 1973; Kerr et al., 1968). Therefore, it may be assumed that the mon- key peri-oral reflex system responds directly to dis- placement and velocity sensitive cutaneous receptors around the mouth.

The suggestion that the monkey peri-oral reflex is mediated by cutaneous mechanoreceptors is not sup- ported by Bratzlavsky (1973, 1976), who found that electrical stimulation of the peri-oral region does not elicit a reflex unless the stimulus is painful, and then the latency is at least 2540ms. Failure to elicit the peri-oral reflex in man by electrical stimulation of the skin led Bratzlavsky (1973) to suggest that cutaneous receptors were not involved m the reflex. He sug- gested that the reflex is elicited by stimulation of deep-lying receptors. However. KadanotT (1956) and Bowden and Mahran (1960) found few muscle spindles m the labial muscles of man and animals, and these were atypical in structure. It is. therefore, unlikely that enough muscle spindles are located in the peri-oral muscles for them to play a significant role in peri-oral reflexes.

Our findings suggest muscle spindles are not present in the peri-oral muscles. The unloading reflex has frequently been used as an indication of a mono- synaptic stretch reflex (Matthews, 1972). In our study,

Peri-oral reflexes m the conscious monkey (MU~LIC~I rnulutfu) X69

the stretch (loading) and release of stretch stimulus tile” stimulus mtenslty: mformatlon transrnlsslon by

(unloading) led to excitatory reflexes at approximately relay neurons in different trigemmal nuclei S~encc 160,

the same latency, as well as long-lasting inhibition 791-794.

in both lip and jaw musculature. There was no silent Dubner R.. Sumino R and Starkman S 1974 Responses

period m lip muscles after the release stimulus. It thus of facial cutaneous thermosensltive and mechanosennl-

appears that either loadmg or unloading stimuli of tlve afferent fibers m the monkey to noXlous heat stlmu-

the monkey lip elicit the same reflex. The absence latlon. .4dr Nrurol. 4, 61-71.

of a short latency shutdown of EMG after a release Godaux E. and Desmedt J E 1975. Exteroceptlve huppres-

stimulus suggests that either there are no spindles in sion and motor control of the masseter and temporalis muscles m normal man. Bran Res. 85, 447 -45X

the labial musculature. or if there are, they do not Goldberg L J 1971 Masseter muscle rxcltation Induced

behave as they do in the spinal system. Sakada (1971) by stimulation of periodontal and gmglval receptor\ m

found Golgi-Mazzoni corpuscles in the periosteum man. Bruin Ret 32, 369-381.

of the mandible of cats. and suggested that these are Goldberg L. J. 1972. An rxcltatory component of the jaw

more sensitive to mechanical stimulation than free openmg reflex in the temporal and masseter muscle\ of

nerve endings. According to Darian-Smith (1966). cats and monkeys Euprrwntm 28, 44-46.

Meissner corpuscles, Merkel discs and pressure recep- Hahn J. F 1971 Stimulus-response relatIonship\ in tirst-

tors are located m the peri-oral region. Mechanical order sensory fibers from cat tlbrissae J Phr\ml. L.~~~I~ 213, 115 ‘76

stimulation of these might elicit peri-oral reflexes. Kadanoff D 1956 Die senslhlen Nervenendlgungen In der The labio-mandibular reflex was of secondary inter- mmuschen Mushulatur des Menschen 2 IIII~~ LIU~II

est to us and we did not systematically collect data. Forsch. 62, I I5 Our findings indicate that the labio-mandibular reflex Kerr F. W L.. Kruger L. Schwassmann H 0 dnd Stern

m the conscious monkey is similar to that in man R. 1968 Somatotopic orgamzatlon of mechanoreceptor

(Bratzlavsky, 1976: Yu. Schmitt and Sessle. 1973). We units m the trlgemmal nuclear complex of the macaque

found latencles of the EMG excitation and suppres- J. camp Nrurol 134, 117-144

sion to be similar to those for man (Godaux and Des- KIrkpatrIck D B and Kruger L. 1975 Physloloplcal

medt. 1975). Our results also show that the lablo- properties of neurons m the principal sensory trlgemlnal

mandibular reflex was eliclted by ramps with the nucleus of the cat E.vp/ Nr,lrrol. 48. 664-690.

Larson C R. Folhlns J W, McClean M and Mullcr E same velocity that elicited the peri-oral reflex. Thus, 197X Srnsitivlty of the human penoral r&c* to par- lip-stretch stimuli with velocities of 5C300 mm& eli- ameters of mechanical stretch. Bruin RCA 146. 159- 16-l

cited the labia-mandibular reflex, but the amplitude Lmdqtnst C. and Martensson A 1969 The posslhle role

decreased with slower velocities (Fig. 2). A short of exteroceptors In the control of foal mu\cle\ -I(,ltl

latency reflex was recorded in the MPT at 6ms in physrol. \cwul suppl 330. 116.

the macaque. which IS similar to that elicited by elec- Lindqulst C. and Martensson A. 1970 Mechamrms m-

trical stimulation of the gingiva in man and macaques valved m the cat’s hllnk reflex .4c’rtr ph~‘\~o/ \(,uu~/ 80,

(Goldberg, 1971. 1972: E. S. Luschei. personal com- 149-159

munication). It is possible that the mechanical stimu- Matthews P. B C 1971. .~lutnmu/~an Mu,wlu Rrceprora uttd

therr Ctwfrtrl ~C~IIO~I\ Wdhams & Wilkms. Baltimore. lus we applied to the upper lips activated the recep- Md. tors m the ginglva, leading to the short latency reflex Rowe M. J and Sessle B. J 1972. Responses of trlgemlnal m the MPT. ganglIon and bram stem neurons in the cat to mechdm-

The technique described by us is useful for studying cal and thermal stlmulatlon of the face Brtrm Rcs 42.

oro-motor behaviour in the unanaesthetized monkey, 367-384

and does not impose undue head restraint techmques Ruth T C and Patton H. E (Eds.) 1965 P/I~\u&J~\ ~rrtd

as some methods do. With the use of controlled Bwphyvcs. 19th Edn. W B. Saunders, Phlladelphla. Penn

stimuli, it IS possible to quantify stimuli to the peri- Sakada S. 1971 Response of Go@Mazzom corpuaclea

oral region more rigorously than has hitherto been m the cat periostea to mechanical stlmuh In Orul

possible. Fuc rul Srnsorr md ,Motor Much~rtmm (Edned by Dubner R. and Kauamura Y 1 4ppleton-(‘cnturh-

AcknoM.Il,dyements~Thls study was supported by grants Crofts. New York

Shaham B 1970 The human bhnk reflex .I ‘V~,UUJI Nurrw RR00166 and NSll780 from the National lnstltutes of Health. and by a grant from the Wdham G Reed Fund

.wy P 5) c hurt 33, 791-800.

to the Vlrgmla Mason Research Center. Shaham B and Young R R. 1973. Bhnk reflexes In orblcu-

IarIs ocull. In Nr\v Del rl0pfnenf\ ~1 E/ccrr~)mi~Jyr~rphl

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