Journal of Neurology, Neurosurgery, and Psychiatry 1992;55:774-780

Gating of trigemino-facial reflex fromlow-threshold trigeminal and extratrigeminalcutaneous fibres in humans

Alessandro Rossi, Chiara Scarpini

Laboratory ofNeurophysiology,Institute ofNeurological Sciences,University of Siena,ItalyA RossiC ScarpiniCorrespondence to:Dr Rossi, Istituto di ScienzeNeurologiche, Universita' diSiena, Viale Bracci, 53100Siena, Italy.Received 30 August 1991and in revised form2 December 1991.Accepted 15 January 1992

AbstractChanges in the size ofthe test components(RI and R2) of the trigemino-facial reflexwere studied after electrical subliminalconditioning stimulation were applied tothe trigeminal, median and sural nerves.After conditioning activation of the tri-geminal nerve (below the reflex thresh-old), the early RI reflex componentshowed phasic facilitation, peaking atabout 50 ms of interstimulus delay, fol-lowed by a long-lasting inhibition recover-ing at 300-400 ms. The same conditioningstimulation resulted in a monotonicinhibition of the late R2, starting at15-20 ms, with a maximum at 100-150 msand lasting 300-400 ms. Intensity thresh-old for both the R1 and R2 changes rangedfrom 0 90 to 0 95 times the perceptionthreshold. A similar longlasting inhibitionof the R2 reflex response was also seenafter conditioning stimulation applied tolow-threshold cutaneous afferents of themedian and sural nerves. The minimumeffective conditioning-test interval was25-30 ms and 40-45 ms respectively andlasted 600-700 ms. By contrast the earlyRI reflex response exhibited a slight long-lasting facilitation with a time coursesimilar to that of the R2 inhibition. Thethreshold intensity to obtain facilitation ofthe RI and inhibition ofthe R2 test respon-ses after conditioning volley in the medianand sural nerves was similar and rangedfrom 0 9 to 1-2 times the perceptionthreshold. These results demonstrate thatlow-threshold cutaneous afferents fromtrigeminal and limb nerves exert powerfiucontrol on trigeminal reflex pathways,probably via a common neural substrate.There is evidence that, in addition to anypost-synaptic mechanism which might beoperating, presynaptic control is aprimary factor contributing to thesechanges.

(7 Neurol Neurosurg Psychiatry 1992;55:774-780)

The trigemino-facial reflex has been largelyused as a test reflex for studying the organisa-tion and integrity of brainstem reflex circuits.The reflex response of theorbicularis oculimuscles to unilateral electrical stimulation ofthe first trigeminal (TR) branch shows twomain components: an early and brief compo-nent (RI) and a later prolonged component(R2).1-3 Under appropriate experimental con-ditions a third reflex component (R3) can also

be constantly obtained.4 Many physiologicalstudies suggest that the short and long latencycomponents arise from different but parallelneural pathways.'-2

Since the original description by Kimura,"3the paired shock technique has been largelyemployed to study the recovery cycle oftheTRreflex components, both in physiological andpathological conditions.""22 In all these stud-ies conditioning stimuli were above the thresh-old for reflex responses. This caused difficultiesin interpretation of the results: a) at condition-ing-test intervals shorter than 80-100 ms thereflex response evoked by the conditioningstimulus overlaps the test reflex, obscuring theeffect of the conditioning volley on the latter;b) when the motor neurons are fired in theconditioning reflex response, a long lastingdepression of their excitability, due to post-spike after-hyperpolarisation, can be expected;c) in addition to any direct effect produced bythe conditioning stimulus, there may also bethose due to afferent reactivation during mus-cular contraction; d) finally, using high inten-sity conditioning stimuli, no conclusion can bereached on the type of afferent fibres responsi-ble for the effects observed on test responses.

In this study, graded subliminal condition-ing stimuli were applied to TR afferents andthe respective effects on the early RI and lateR2 components of the trigemino-facial reflexwere evaluated. The same TR reflex compo-nents were also studied after conditioningactivation of low threshold cutaneous afferentsarising from median (MN) and sural (SR)nerves.

MethodsThe experiments were performed on 5 adultvolunteers (30-37 years), all of whom gaveinformed consent to the experimental proce-dure which was approved by the local EthicalCommittee. In two cases the experiments wererepeated 3 and 4 times. The subjects werecomfortably seated in an armchair. Electro-myographic activity from the orbicularis oculimuscles was recorded by surface electrodes seton the lower lid.

1) Conditioning stimulationSingle pulses of 0 1-0 5 ms duration weregiven through bipolar surface electrodes, thecathode being proximal to three differentnerves: the TR, the MN and SR nerves. Sinceit was not possible to record the incomingvolley, stimulus strength was expressed inmultiples (x) of the perception (P) threshold

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(Th). In all cases conditioning strength waskept below theTh for reflex responses. Accord-ing to the ascending method of limits,23 stimuliwere increased in 0-25 mA steps and the reflexTh was the intensity value at which a responsewas evoked by approximately 50% of thestimuli. The ascending procedure was alsoused to estimate the subjective PTh, the valueofwhich was verified several times during eachexperimental session. Branch I oftheTR nervewas stimulated at the supraorbital foramen(supraorbital nerve) and branch III at themental foramen (mandibular nerve). The MNnerve was stimulated at the second and thirddigits (in one case also at wrist level). The SRnerve was stimulated at the lateral malleolus.

2) Test stimulationThe RI and R2 responses of the trigemino-facial reflex were evoked by test stimuli(0 -1-0-5 ms duration) applied by surface elec-trodes to the supraorbital nerve.

Since the aim of this study was primarily togive a description of the excitability changes ofthe trigemino-facial reflex, it was important, asa first step, to verify whether the size of the testreflex itself could affect its susceptibility to theconditioning volley. The amount of facilitationof the RI and inhibition of the R2 reflexcomponents of different size were then testedduring a constant conditioning input. Con-ditioning stimulation was applied to the MNnerve (conditioning-test interval 200 ms,intensity 1 1 x PTh) and the size of the testresponses was systematically varied by chang-

Figure I Example of theRI facilitation and R2inhibition induced by thesame conditioning stimulusto the median nerve(1-1 x PTh; 200 msconditioning-test interval)when different control sizeswere used. Note the largefacilitation on RI responsewhen the conditioningstimulus was applied on areflex test of smallamplitude (A); the sameconditioning voley failed toevoke such effect whenapplied on a test reflex thesize of which was kept nearits maximum value (B).

Figure 2 Susceptibility toa constant conditioningstimulus of the Rl (opencircles) and R2 (filledcircles) test responses ofdifferent sizes.Conditioning stimulationas in fig 1. The amount ofthe effects on theconditioned responses wasplotted against the controlreflexes size. Each symbolis the mean of tenmeasurements. Vertical barsI SD of mean.

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ing the strength of the test stimulus to thesupraorbital nerve. Figure 1 shows a repre-sentative example of the effect evoked by thesame conditioning stimulus on RI and R2responses of small (A) and large size (B). It isapparent that the facilitation of RI response ismuch more evident when the size of the testreflex is small. Figure 2 gives a detaileddescription of the susceptibility changes of RIand R2 responses in relation to their controlsize. The amount of RI facilidation and R2inhibition (expressed as a percentage of theircontrol values) is plotted against the size of thetest reflex (as a percentage of its maximumvalue) giving a two-part curve: 1) at low reflexamplitude (below 50% of their maximumvalue) the susceptibility to the conditioningvolley was high for both RI and R2 reflexes; 2)with increasing unconditioned reflex size, theamount of the R2 depression remained almostconstant, the curves exhibiting a plateau. Onthe contrary, when the size of the RI responseapproached its maximum value (above70-80%), no facilitatory event was apparent,suggesting saturation of the response. Accord-ingly the intensity of the test stimulus wasadjusted to evoke an RI response 50-70% of itsmaximum size. This allowed: a) acceptablystable responses; b) sufficient margin toobserve any phenomena of facilitation; c) anR2 response within the plateau phase of thecurve. To disclose better the time course of theRI facilitation, the size of the test response wasoccasionally adjusted to its lower value(20-30% of its maximum value). This resultedin a large scatter of the data points necessitat-ing several trials before the temporal profile offacilitation could be unambiguously recog-nized.

3) General experimental procedureThe stimulus sequences were regularly alter-nated as follows: 1) control test reflexes alone;2) test stimulus preceded by conditioningstimulation. Two groups of experiments wereperformed: 1) keeping the strength of theconditioning stimulus constant (below reflexthreshold), the conditioning-test interval wasrandomly varied from 10 to 400-900 ms; 2)keeping the conditioning-test interval con-stant, the strength of the conditioning stimuluswas randomly varied from 0-7-0-8 to 1.2-1-5x PTh. The sequence, unconditioned-con-ditioned responses, was repeated 10-15 timesfor each conditioning-test interval and for eachconditioning stimulus strength. Stimuli weregiven at intervals of 15-20 s, delivered byconstant-current stimulator. The EMG signalswere fed from the oscilloscope to a full waverectifier and further to an averager and integra-tor. The digital integral values of RI and R2conditioned reflex components were measuredand expressed as a percentage of their uncon-ditioned values.

ResultsTo obtain a valid comparison between theeffects of different cutaneous conditioningstimuli on TR reflex responses, all the data

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illustrated here are from the same subject.Although the amount of facilitation and/orinhibition caused by the various conditioningstimuli was variable from one subject toanother, qualitatively similar results wereobtained in all cases.The time course of the RI and R2 responses

when preceded by subliminal supraorbitalnerve stimulation (1 0 x PTh) is shown in fig3. The early RI response showed a facilitatoryphase between 30 and 60 ms, followed by along lasting inhibition which was maximal for aconditioning-test interval of 100-150 ms. The

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Conditioning-test interval (ms)Figure 3 Time course of the effects of a conditioning stimulus applied to the ipsilateralsupraorbital nerve (1 0 x PTh) on RI (open circles) and R2 (filed circles) test reflexresponses. The size of the conditioned RI and R2 responses is expressed as a percentage oftheir unconditioned values. Each symbol is the mean of ten responses. Vertical bars I SDof mean.

size of the conditioned response recovered tonear its control value within 300-400 ms. Thesame conditioning stimulation resulted in amonotonic long-lasting inhibition of the lateR2 response. The minimum effective con-ditioning-test interval was 15-20 ms. The testresponse was maximally depressed for aninterval of 100-150 ms and returned to itscontrol level for intervals of 300-400 ms. Acomparable time course was obtained for thecontrolateral R2 response. Very similar effectson the RI and R2 responses from the orbicu-laris oculi muscle were also obtained when theconditioning stimulus (1-0 x PTh) wasapplied to the ipsilateral mental nerve (notillustrated). In an attempt to determine theThof these changes and whether the same afferentfibres were responsible for both excitatory andinhibitory variations in the test reflexes, aconditioning stimulus of increasing strengthwas applied at 50 ms (corresponding to theincreasing phase of the RI and the decreasingphase of R2) and 100 ms (corresponding tothe inhibition of both responses) of inter-stimulus delay (fig 4). With a delay of 50 ms,increasing the strength of the TR nerve stim-ulation resulted in a progressive increase in RIand decrease in R2, both appearing at 0-9 xPTh. When the interstimulus delay was fixed at100 ms the depression of both RI and R2responses was also apparent at a conditioningstrength of 0-9 x PIh [mean (SD) 0-92(0 02); range 090-0 95 x PTh]. That theThvalues were identical suggests that these chan-ges are contingent upon the same low-thresh-old afferent fibres. Figure 5 illustrates theresults obtained when the conditioning stim-ulus was applied to the MN nerve fibres arisingfrom the fingers (1 0 x PTh). At interstimulusinterval longer than 25-30 ms, the RI compo-nent showed a first facilitatory peak followedby a subsequent long lasting facilitation whichrecovered at 500-600 ms. A similar but oppo-site time course was shown by the R2 reflexresponse. In the same subject the conditioning

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Figure 5 Time course of the effects of a conditioningstimulus applied to theMN nerve (1 0 x PTh toipsilateral HI-HII digit) on RI (open circles) and R2 (filedcircles) test reflex responses. The size of the conditioned RIand R2 responses is expressed as a percentage of theirunconditioned values. Each symbol is the mean of tenresponses. Vertical bars 1 SD of mean.

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Gating of trigemino-facial reflex from low-threshold trigeminal and extratrigeminal cutaneous fibres in humans

in all cases the threshold of the effects was verylow (0 9-1 2 x PTh), suggesting that onlylow-threshold afferent fibres were activated; b)

160. when the stimulus was applied to the medianj nerve, similar effects were observed for stim-

1.It20- I ulation at the wrist (which is supposed to4 * I 4 t ' ' activate both muscular and cutaneous affer-.1 * ents) and for selective stimulation of the,4,"4f t , cutaneous afferents from the fingers.

Activation of low-threshold TR or limb

D}1140 cutaneous afferent fibres produced a mono-. tonic long-lasting depression of the R2 reflex

component. Following activation ofTR nerve,D., O0 this inhibition was apparent at a conditioning-

test interval of 15-20 ms, reached a maximum.7 .8 .9 U0 ti 1 13 .7 *18 .91.0Itl 1.2 '

at 100 ms and lasted 300-400 ms.Intensity ofconditioning stimulus(xh) When the conditioning stimulus was applied

to the MN and SR nerve afferents, theEffect of changing the strength of conditioning stimuli applied to theMN nerve inhibition had a longer latency (25-30 ms and

d HI-HII digit) (on the left) and SR nerve (on the right) on RI (open circles) 40-45 ms respectively) and lastedtilled circles) test reflex responses. Conditioning-test interval was kept constant at 500-600 ms. The greater afferent delay due toEach symbol is the mean often responses. Vertical bars 1 SD of mean.

the distance between the site of application ofthe stimulus and the brainstem in whichinteractions between conditioning and test

stimulation was also applied to the MN nerve volleys are presumed to occur (see below), canat the wrist. The intensity was set at the motor explain the later onset of inhibition. In addi-threshold (2.5 x PTh in this case) to ensure tion, the time dispersion of the arrival of actionthat, in addition to the cutaneous volley, a large potentials in the afferent fibres from MD andfraction of muscular afferents was also activ- SR nerves must be rather large with the longated. Virtually identical results were obtained, conductance distances that are involved. Thisalthough the recovery phase ofthe R2 response time dispersion of the conditioning spikesremained incomplete (60-70% of its control could be an additional contributory factorsize) up to 900-1000 ms. Figure 6 (left panel) responsible for the longer time course of theshows the effects of increasing conditioning R2 inhibition with respect to that observedstimuli applied to the second and third digits, after TR stimulation.at 200 ms of interstimulus delay. Both the RI The almost identical temporal trajectory offacilitation and R2 inhibition became apparent the R2 inhibition originating from TR, MNat 1.0 x PTh [mean (SD) 0-96 (0-03); range and SR nerves suggests a common mechanism.0.9-1.0 x PTh). A similar time course ofboth It has been shown in animal studies thatthese reflex responses was obtained when the impulses in the TR fibres or in ascending andconditioning stimulation was applied to the SR descending pathways in relation to the TRnerve at the ankle (not illustrated). A slight complex, can depress the TR second orderlong lasting monotonic facilitation of the RI neuron response evoked by stimulation of theresponse and a deep long lasting monotonic TR afferent fibres.2129 For the ascendinginhibition of the R2 response started at inter- pathways it has been shown in animals thatvals of 40-45 ms and recovered within stimulation of the posterior columns or the700-800 ms. None of the cases showed an superficial radial and sciatic nerves is effectiveearly facilitatory peak of the RI component. in producing depression in the TRIncreasing conditioning stimulus strength nuclei.242730 Ascending influences from limb(200 ms interstimulus interval), both the afferents onTR reflex responses have also beeninhibitory effect on RI and the facilitatory observed in humans."7 Neural elements of theeffect on R2 were apparent at 1 x PTh (right medullary and upper spinal cord reticularpanel fig 6) [mean (SD) 1 04 (0 09); range formation may be a possible common final0-95-1-20 x PTh). pathway of these inhibitory interactions.273132The mean (SD) Th values for the uncon- Much evidence exists that presynaptic depolar-

ditioned RI and R2 test responses were respec- isation of the TR primary afferents largelytively 2-27 x Ph [(0 7); range 1-55-3-3] and contributes to the inhibition observed within1-46 x PTh [(0 5); range 1-2-45]; the abso- TR nuclei.2425 230 It is now generallylute mean (SD) value of PTh was 1 15 mA accepted that this depression is caused by an[(0 5), range 0-5-2 mA]. increase in conductance of the primary afferent

terminals brought about by axo-axonal TRsynapses,29 resulting in reduced transmitter

Discussion release.337 In addition to any post-synapticA single perception threshold conditioning inhibitory mechanism which might be operat-stimulus to the TR, MN and SR nerves ing, we believe that presynaptic inhibition wasmodified the excitability of neural pathways also the primary factor contributing to themediating the early RI and late R2 components inhibition of the R2 reflex component. Twoof the trigemino-facial reflex. Two main factors main arguments favour this possibility: a) thesuggest that these effects depend on the time course of this inhibition is identical to theactivation of large cutaneous afferent fibres: a) time course ofpresynaptic inhibition described

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in animals and human spinal cord;38 b) there isa surprising identity between the time courseof the R2 inhibition observed here, and that oftheTR primary afferent depolarisation seen inthe cat.24 27 29

In contrast with the monotonic inhibition ofR2, the early RI reflex component undergoesmore complex variations. When the test stim-ulus applied to the supraorbital nerve waspreceded by a conditioning stimulus to the TRfibres, (branch I or III) a facilitatory phase,having a maximum between 40 and 50 ms, wasobserved, cut off by a subsequent long-lastinginhibition which paralleled the time course ofthe R2 depression (fig 2). In the cat, afacilitatory phase, with a maximum at about30 ms, has been observed on facial motorneurons following stimulation of trigeminalafferents.39 A similar motor neuronal facilita-tion may account for the present results. Sincethe latency of this phase appears to coincidewith the time at which the R2 component isexpected, this facilitation may be produced bythe subliminal activation, brought about by theconditioning volley, of the R2 reflex pathwayinducing EPSPs on facial motor neurons.Indeed, since theTh of the R2 response is veryclose to the PTh (that is below theTh of the RIreflex), it is conceivable that the same low-threshold afferent fibres activated by the sub-liminal conditioning stimulus are alsoresponsible (when adequate spatial and/ortemporal summation takes place) for the lateR2 response. In the cat this short latencyexcitatory phase is followed by a period ofreduced responsiveness of motor neurons last-ing 30-100 ms.39 Because of the experimentalcondition used, that inhibition may be partiallydue to motor neurone after-hyperpolarisationfollowing the conditioning reflex response:when the motor neurone is fired in theconditioning volley the subsequent after-hyperpolarisation depresses its excitability andprevents it from firing again. This, however,seems unlikely to account for our case, sincethe conditioning stimulus was constantly keptbelow the motor Th, thus ruling out any post-spike after-hyperpolarisation. As shown in fig3, the temporal profile of the RI depressionparallels that of the R2 component, except fora later onset, probably masked by the preced-ing facilitation. By a process of analogy, there-fore, the most obvious possibility is that it ispresynaptic in origin.When the conditioning stimulus was applied

to the MN and SR afferents, the RI componentshowed a slight long-lasting facilitation with atime course similar to that of the R2 inhibition(fig 5). Most or all ofthe presynaptic inhibitorypathways are capable of exerting not onlytransient but also tonic inhibitory influenceson the primary afferent terminals. Temporaryremoval of tonic presynaptic depolarisationwould lead toto transitory disinhibition, whichcould be recorded as facilitation. For example,removal of tonic presynaptic inhibition on Iafibres restores the monosynaptic excitatorypost-synaptic potential to its control height.40

Electrophysiological evidence also exists infavour of a tonic presynaptic action on TR

primary afferents.29 35 41 42 In view of this andof the evidence that RI facilitation has a timecourse very similar to that ofR2 inhibition, oneof the possibilities is that this long-lastingfacilitation is due to a transient reduction intonic presynaptic control acting on the TRafferents responsible for RI reflex. However, aprerequisite for such a theory is that TRprimary afferents for the RI response aredifferent from those responsible for the R2component. The difference between RI and R2Th values observed here (see Results Section)and in previous studies23 suggests that the RIcomponent is contingent upon TR afferentssmaller (less excitable fibres) than those pro-jecting onto the R2 pathway.

Close observation of fig 5 shows that thefacilitation of RI appears to have an early peakwhich roughly coincides with the phase ofshort latency facilitation observed after TRstimulation (fig 3). Similarly, this phase offacilitation may be due to the subliminalactivation of facial motor neurons induced bythe conditioning stimulation of the MN nerve.It has been shown that MN afferents accessfacial motor neurons generating, under appro-priate condition, a reflex response in the facialmuscles.43 This interpretation is indirectly sus-tained by evidence that the same facilitatorypeak does not appear for stimulation of the SRnerve, which never evokes facial reflex respon-ses even at high stimulus intensity.Our results with limb stimulation seem

compatible with those of Bulou et al, 7 whoused the radial and SR as conditioning nerves(see fig 3). Their observations become cleareras a result of this study: first, it demonstratesthat large cutaneous afferents make a majorcontribution to these TR reflex changes; sec-ond, in view of the similarity of the reflexchanges produced, TR and limb afferentsappear to operate via a common neural sub-strate. A similar conclusion was also reachedby Rimpel et a144 who observed almost identi-cal effects of acoustic and visual stimuli onTRtest responses.

Figure 7 shows a schematic model of hypo-thetical presynaptic control of the pathwaysmediating the RI and R2 reflex components. Aconditioning volley in low threshold TR affer-ents (Ltta) subliminally activates the pathwayresponsible for the R2 component, causing anincrease in the discharge of presynaptic inter-neurones X and Z acting on the afferent fibresof both the RI (Htta) and R2 (Ltta) responses.This is translated into a parallel depression ofthese reflex responses (fig 3). Incidentally,subliminal activation of the R2 pathway couldevoke excitatory post-synaptic potentials in themotor neurons, possibly responsible for thefirst facilitatory phase observed on the RIcomponent. Low threshold afferent fibres fromlimb nerves (Ltla) converge on the interneuronZ but not on X. The increased activity of the Zinterneuron depresses the R2 pathway, conse-quently reducing the firing onto presynapticinterneuron X acting on the RI Htta. Thiscauses disinhibition of these afferents and aconsequent facilitation of the RI component(fig 5).

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Ltla

tta Ltta

Rl?IR2

iMn

Although our experiments were unable toidentify with certainty the neural substrate ofthe Rl and R2 changes, it is plausible toconclude that presynaptic action from low-threshold cutaneous afferents on TR terminalsis a major contributory factor. The possibilityof facilitating or depressing cutaneous trans-mission at presynaptic level could certainlyconstitute a powerful means of reducing andselecting peripheral information pertinent tosensory and/or motor processing. For example,"trigeminotrigeminal" and "extratrigemino-trigeminal" inhibitory influences can optimisespatial contrast, respectively within the samereceptive field and between different sensorychannels, to facilitate the localisation of thestimulus.A final comment is required on the observa-

tion that even a stimulus strength below thesubjective PTh is sometimes effective in pro-ducing changes in the trigemino-facial reflexes.One possibility is that these low-Th cutaneousafferent fibres do not access the cerebralcortex. However, the evidence in the cat thateven the activation of single fibre (from Pacin-ian corpuscles) is able to generate a corticolevoked response45 argues against this possibil-ity. Sensory perception should not be regardedas depending exclusively on the peripheralafferents activated but also on the temporaland spatial gradients of the applied stimulus.

We wish to express our gratitude to Dr B Decchi for readingand commenting upon the manuscript. This work was sup-ported by grants from the Italian CNR and Regione Toscana.

1 Kugelberg E. Facial reflexes. Brain 1952;75:385-96.2 Rushworth G. Observation on blink reflexes. J Neurol

Neurosurg Psychiatry 1962;25:93-108.3 Shahani BT, Young RR. Human orbicularis oculi reflexes.

Neurology 1972;22:149-54.4 Rossi B, Risaliti R, Rossi A. The R3 component of the blink

reflex in man: a reflex response induced by activation ofhigh threshold cutaneous afferents. Electroencephalogr ClinNeurophysiol 1989;73:334-40.

5 Lindquist Chr, Martensson A. Mechanisms involved in thecat's blink reflex. Acta Physiol Scand 1970;80: 149-59.

6 Hiraoka M, Shimamura M. Neural mechanisms of thecorneal blinking reflex in cats. Brain Res1977;125:265-75.

7 Ongerboer deVisser BW, Kuypers HGJM. Late blink reflexchanges in lateral medullary lesions: an electrophysio-logical and neuroanatomical study of Wallenberg's syn-drome. Brain 1978;101:285-94.

8 Trontelj MA, Trontelj JV. Reflex arc of the first componentof the human blink: a single motoneurone study. J NeurolNeurosurg Psychiatry 1978;41:538-47.

9 Ongerboer De Visser BW, Moffie D. Effects of brainstemand thalamic lesions on the corneal reflex. Brain1979;102:595-608.

10 Tamai Y, Iwamoto M, Tsujmoto T. Pathway of the blinkreflex in the brainstem of the cat: interneurons betweenthe trigeminal nuclei and the facial nucleus. Brain Res1986;380: 19-25.

11 Evinger C, Manning KA. A model system for motor

learning: adaptive gain control of the blink reflex. ExpBrain Res 1988;70:527-38.

12 Evinger C, Sibony PA, Manning KA, Fiero RA. A pharma-cological distinction between the long and short latencypathways of the human blink reflex revealed with tobacco.Exp Brain Res 1988;73:477-80.

13 Kimura J. Disorder of interneurons in Parkinsonism. Theorbicularis oculi reflex to paired stimuli. Brain1973;96:87-96.

14 Caraceni T, Avanzini G, Spreafico R, Negri S, Broggi G,Girotti F. Study of the excitability cycle of the blink reflexin Huntington's chorea. Eur Neurol 1976;14:465-72.

15 Kimura J, Harada 0. Recovery curves of the blink reflexduring wakefulness and sleep. J Neurol 1976;213:189-98.

16 Ferguson IT, Lenman JAR, Johnston BB. Habituation ofthe orbicularis oculi reflex in dementia and dyskineticstates. J Neurol Neurosurg Psychiatry 1978;41:824-8.

17 Boulu Ph, Willer JC, Cambier J. Analyse electrophysiolo-gique du reflexe de clignement chez l'homme: inter-actions des afferences sensitives segmentaires et

intersegmentaires, des afferences auditives et visuelles.Rev Neurol 1981;137:523-33.

18 Berardelli A, Rothwell JC, Day BL, Marsden CD. Patho-physiology of blefarospasm and oromandibular dystonia.Brain 1985;108:593-609.

19 Rossi B, Giannini C, Siciliano G, Sartucci F. The role of thetactile-pressure afferents in the habituation phenomenonof trigemino-facial reflex. Acta Neurol Scand1985;72:602-5.

20 Tolosa E, Montserrat L, Baves A. Blink reflex studies infocal dystonias: enhanced excitability of brainstem inter-neurons in cranial dystonia and spasmodic torticollis.Movemnent disorders 1988;3:61-9.

21 Valls-Sole J, Tolosa ES. Blink reflex excitability cycle inhemifacial spasm. Neurology 1989;39: 1061-6.

22 Hatanaka T, Yasuhara A, Kobayashi Y. Electrically andmechanically elicited blink reflexes in infants and childrenmaturation and recovery curves of blink reflex. Electro-encephalogr Clin Neurophysiol 1990;76:39-46.

23 Sanes JN, Foss JA, Ison JR. Conditions that affect thethresholds of the components of the eyeblink reflex inhumans. J Neurol Neurosurg Psychiatry 1982;45:543-9.

24 Darian-Smith I. Presynaptic component in the afferentinhibition observed within trigeminal brain-stem nuclei ofthe cat. J Neurophyswl 1965;28:695-709.

25 Darian-Smith I, Yokota T. Cortically evoked depolarizationof trigeminal cutaneous afferent fibers in the cat. JNeurophysiol 1966;29: 170-84.

26 Hammer B, Tarnecki R, Vyklicky L, Wiesendanger M.Corticofugal control of presynaptic inhibition in thespinal trigeminal complex of the cat. Brain Res1966;2:216-8.

27 Stewart DH, King RB. Effect of conditioning stimuli uponevoked potentials in the trigeminal complex. J Neu-rophysiol 1966;29:442-55.

28 Shende MC, King RB. Excitability changes of trigeminalprimary afferent preterminals in brainstem nuclear com-plex of squirrel monkeys (Saimiri sciureus).JNeurophysiol1967;30:949-63.

29 Stewart DH, Scibetta CJ, King RB. Presynaptic inhibitionin the trigeminal relay nuclei. J Neurophysiol1967;20:135-53.

30 Baldissera F, Broggi G, Mancia M. Depolarization oftrigeminal afferents induced by stimulation of brain-stemand peripheral nerves. Exp Brain Res 1967;4:1-17.

31 Fox JE, Wolstencroft JH. The reduced responsiveness ofneurones in nucleus reticularis gigantocellularis followingtheir excitation by peripheral nerve stimulation. j Physiol1976;258:687-704.

32 Inagaki M, Takeshita K, Nakao S, ShiraishiY, OikawaT. Anelectrophysiologically defined trigemino-reticulo-facialpathway related to the blink reflex in the cat. Neurosci Lett1989;96:64-9.

33 Wiesendanger M, Hammer B, Tarnecki R. Cortifugalcontrol of presynaptic inhibition in the spinal trigeminalnucleous of the cat. The effect of pyramidotomy andbarbiturates. Schweitz Arch Neurol Neurochir Psychiat1967;100:255-76.

34 Rowe MJ, Carmody nJ. Afferent inhibition over the responserange of secondary trigeminal neurones. Brain Res1970;18:371-4.

35 Dubner R, Sessle BJ. Presynaptic excitability changes ofprimary afferent and corticofugal fibers projecting to

trigeminal brain stem nuclei. Exp Neurol 197 1;30:223-38.

36 Eccles JC, Schmidt RF, Willis WD. The mode of operationof the synaptic mechanism producing presynaptic inhibi-tion. J Neurophysiol 1963;26:523-38.

37 Rudomin P. Presynaptic inhibition of muscle spindle and

Figure 7 A hypotheticalmodel illustratingpresynaptic control onto thepathways mediating the Rland R2 components of thetrigemino-facial reflex.Htta: High thresholdtrigeminal afferents; Ltta:Low threshold trigeminalafferents; Ltla: Lowthreshold limb afferents; Xand Z: last interneurons ofputativepathways actingpresynaptically on TRprimary afferents; Rl:reflex pathway mediatingthe Rl component; R2:reflex pathway mediatingthe R2 component.

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Rossi, Scarpini

tendon organ afferents in the mammalian spinal cord.Trends Neurosci 1990;13:499-505.

38 Hultborn H, Meunier S, Morin C, Pierrot-Deseilligny E.Assessing changes in presynaptic inhibition of Ia fibres: astudy in man and the cat. J Physiol 1987;389:729-56.

39 Lindquist Chr. Analysis of facial reflex facilitation andinhibition by microelectrode recording from the brainstem. Acta Physiol Scand 1972;85:183-92.

40 Lund S, Lundberg A,Vyklicky L. Inhibitory action from theflexor reflex afferents on trasmission to Ia afferents. ActaPhyswl Scand 1965;6:345-55.

41 Scibetta CJ, King RB. Hyperpolarizing influence of trigemi-nal nucleus caudalis on primary afferent preterminals intrigeminal nucleus oralis. J Neurophysiol 1969;32:229-38.

42 Schmidt RF. Control of the access of afferent activity tosomatosensory pathways. In: Iggo A. ed, vol II. Somao-sensory system. Handbook of sensory physiology. Berlin:Springer, 1973:151-206.

43 Dehen H, Bathien N, Cambier J. Le- reflexe palmo-mentonnier: etude electrophysiologique. Rev Neurol1974;130:39-48.

44 Rimpel J, Geyer D, Hopf HC. Changes in the blinkresponses to combined trigeminal, acoustic and visualrepetitive stimulation, studied in the human subject.Elecroencephalogr Clin Neurophysiol 1982;54:552-60.

45 McIntyre AK, Holman ME, Veale JL. Cortical responses toimpulses from single Pacinian corpuscles in the cat's hindlimb. Exp Brain Res 1967;4:243-55.

Neurological stamp

Niels Stensen (or Steno) 1648-86

Niels Stensen was still a student when he discovered in1661 the excretory duct of the parotid gland in sheep. Thiswas later identified in humans by Sylvius. Stensen was thefirst to identify the heart as a muscle and to recognise thecongenital cardiac defects later known as the tetralogy ofFallot. Stensen identified the cerebral grey and whitematter and argued that it was idle to speculate aboutcerebral function when so little was known about itsstructure. He disagreed with the views of Willis on thelocation of certain higher functions such as memory, andof Descartes who considered the pineal gland to be thelocation of the soul that existed only in humans. Stensenshowed that the pineal gland existed in other animals. Heopposed the views of Borelli who believed that increasedmuscle bulk noted on contraction was due to a fermenta-tion process generated by a discharge of liquid from thenerves.

Stensen was one ofthe founders ofgeology and he wroteimportant works on the production of strata, fossils andother geological formations. Brought up a Lutheran,Stensen converted to Catholicism in 1667 and gave up thestudy of science after he was ordained a bishop in 1677. Hewas one of the greatest intellects of his time, but died inextreme poverty.Denmark honoured him with this stamp in 1969 on the

300th anniversary of the publication of his geological workOn Solid Bodies (Stanley Gibbons 507, Scott 462).

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