Brain 2005 128(2):235-236; doi:10.1093/brain/awh394
Brain Vol. 128 No. 2 © Guarantors of Brain 2005; all rights reserved
From the Archives
Facial reflexes. By Eric Kugelberg (Department of Clinical Neurophysiology, Serafimerlasarettet, Stockholm, Sweden.) Brain 1952: 75; 385–396.
Kugelberg's paper was written to celebrate the 60th birthday of Professor Herbert Olivecrona. His starting position is that many different names had been used to describe reflex contractions of the facial musculature—depending on the area tapped, the muscles responding and the mechanisms considered to be involved. Broadly, his hypothesis is that these all described the same phenomenon; and most of the putative distinctions are artefacts arising from spurious transmission of the stimulus across bony structures in the face. Thus, winking in response to a tap around the eye had been variously confused as a skin, periosteal, perichondreal, bony or myotatic reflex. None of these descriptions was supported by evidence that the appropriate muscle spindles and afferent–efferent circuitry existed in these structures and the mimetic muscles. Nor was there agreement on which nerves contained sensory fibres and which did not. In short, a touch of clinical science applied to the facial reflexes was long overdue. Kugelberg standardized the stimuli: the tap of a light metal rod on the corner of the eye or mouth, and on the jaw; a puff of air or the flick of a knotted probe on the cornea; and calibrated pin pricks. Each was used to trigger a sweep of the oscilloscope recording muscle action potentials. Mechanical stimulations were studied in most detail. These showed a lag of 
1.5 ms by comparison with direct nerve stimulation. The same pattern was observed irrespective of whether the glabella, frontal bone, nose or zygoma was stimulated. Foster Kennedy in his introduction to Robert Wartenberg's ‘The examination of reflexes’ (1945) had earlier ridiculed ‘the open season for the hunting of the reflex.... impedimenta of variety without variance.... the shrill claims to be the Prometheus of the pyramidal tracts.... ideas precious, semiprecious or merely vulgar’. From the facial perspective, Kugelberg listed them all but disposed of the spurious nomenclature by showing that, from the physiological perspective, the responses were all rather similar. An initial well synchronized volley lasting 5–10 ms and with a latency of 12 ms was followed by a longer lasting asynchronous discharge starting after 25–30 ms and lasting at least 30 ms. With some nuances of difference in timing and threshold, gentle stimulation showed that these two components would always each be elicited. Kugelberg concluded that, despite appearing as one, this biphasic response actually represented two different reflexes. The first was unilateral, the second bilateral. As stimulus strength increased, the response spread to other muscles. Kugelberg wanted to dissect the afferent and efferent components: trigeminal rhizotomy invariably abolished both responses—unless the tap was massive, in which case the stimulus would spread to the contralateral side. Rather little could be inferred from persistence of the first component (with a raised threshold for the second) in the presence of trigeminal tractotomy since this could not be assumed to be complete. Confirmation that the afferent pathway involved the trigeminal nerve was provided by direct peroperative stimulation at 1 mA in a patient undergoing trigeminal nerve section for tic doulereaux under local anaesthetic. Stimulation with surface or needle electrodes implicated the infra-orbital nerve especially in the second response, and the motor reflex could be elicited without inducing pain. In contrast to tapping, and direct responses elicited by nerve stimulation, skin and corneal stimulation with a pin or air elicited only the second (bilateral response) unless the stimulus was applied directly over the orbicularis muscle. Then, the first component could be elicited in isolation, especially by stretch transmitted to the muscle.
Thus Kugelberg confirmed what Wartenberg had observed clinically in the context of minimal tapping—an ipsilateral blink with a weaker contralateral closure of the eyelids; and a bilateral asynchronous delayed response, elicited by pain or touch. Kugelberg added the important physiological detail that this was not one but two reflexes. Having decided on the nature of the reflex, and the pathways on which it depended, he wanted to characterize the circuitry involved. By comparing the latency of the ipsilateral orbicularis response with that of the jaw jerk, he reckoned on a missing 4.5 ms. Given nerve conduction at 45 m/s and the distance covered, most could be accounted for; but 0.6 ms was missing. This matched the interval known to arise from transmission across a single synapse, and suggested complexity by comparison with the monosynaptic masseter reflex indicating that the facial reflex is polysynaptic. What did Kugelberg add ? No longer was it sufficient to stand at the bedside and pontificate on the putative circuitry underlying reflex responses of the nervous system to mechanical or painful stimulation; rather the era of electrophysiological measurement and rigorous characterization of structure and function had arrived.
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Fig. 1 Reflex discharges evoked by tapping. (A–E) From the eyelid; and (F) from the upper lid. All records show two groups of discharges; a well-synchronized volley after a latency of  12 ms followed by an asynchronous discharge after a latency of 25–30 ms.
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Fig. 2 Records from the eyelid following trigeminal rhizotomy. (A and B) Operated side. A weak tap (A) evokes no response and a stronger tap (B) evokes only a second response. (C) Normal side. A weak tap evokes a double response.
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Fig. 3 Electrical stimulation. (A) Stimulation of the trigeminal root evokes the usual double response. (B and C) Stimulation of the infra-orbital nerve through the skin evokes (B) only the first response and (C), after shifting the position of the electrode slightly, evokes only the second response.
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Fig. 4 Reflex discharges recorded from the eyelid. Tapping with a blunt needle (A) over the orbicularis oculi muscle evokes a double response, and (B) a few centimetres away evokes only a second response. (C) A faint puff of air over the muscle evokes only a second response. (D) Corneal reflex discharge.
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Alastair Compston
Cambridge
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