The corneal reflex and the R2 component of the blink reflex

A reflex contraction of the human orbicularis oculi muscles can be evoked by stimulation of either the supraorbital region ("blink reflex") or the cornea ("corneal reflex"). We found that the latency of the corneal reflex was longer, and the duration was longer than the R2 component of the blink reflex. The absolute refractory period of the R2 component of the blink reflex was longer after supraorbital than after corneal conditioning stimulation. When the R2 component of the blink reflex was habituated by repetitive stimuli, stimulation of the cornea still evoked a reflex, but supraorbital stimulation produced only a depressed R2 response. These findings suggest that the two reflexes do not have identical neural connections.     

Further evidence for a central reorganisation of synaptic connectivity in patients with hypoglossal-facial anastomosis in man

In normal subjects, electrical stimulation of trigeminal mucosal afferents (lingual nerve - V3) can elicit a short latency (12.5+/-0. 3 ms; mean+/-S.D.) reflex response in the ipsilateral genioglossus muscle (Maisonobe et al., Reflexes elicited from cutaneous and mucosal trigeminal afferents in normal human subjects. Brain Res. 1998;810:220-228). In the present study on patients with hypoglossal-facial (XII-VII) nerve anastomoses, we were able to record similar R1-type blink reflex responses in the orbicularis oculi muscles, following stimulation of either supraorbital nerve (V1) or lingual nerve (V3) afferents. However, these responses were not present in normal control subjects. Voluntary swallowing movements produced clear-cut facilitations of the R1 blink reflex response elicited by stimulation of V1 afferents. In a conditioning-test procedure with a variable inter-stimulus interval, the R1 blink reflex response elicited by supraorbital nerve stimulation was facilitated by an ipsilateral mucosal conditioning stimulus in the V3 region. This facilitatory effect was maximal when the two stimuli (conditioning and test) were applied simultaneously. This effect was not observed on the R1 component of the blink reflex in the normal control subjects. These data strongly suggest that in patients with XII-VII anastomoses, but not in normal subjects, both cutaneous (V1) and mucosal (V3) trigeminal afferents project onto the same interneurones in the trigeminal principal sensory nucleus. This clearly supports the idea that peripheral manipulation of the VIIth and the XIIth nerves induces a plastic change within this nucleus.     

Axon reflexes or ephaptic responses simulating blink reflex R1 after XII-VII nerve anastomosis

It has been claimed that functional recovery of the blink reflex occurs after hypoglossal-facial nerve anastomosis. This has been explained through central nervous system plasticity and reorganization of neuronal connections. In 5 patients with reinnervated facial muscles after hypoglossal-facial nerve anastomosis, we observed “R1-like” responses that fulfilled criteria for facial nerve axon reflexes or ephapses. First, displacement of the stimulating electrode from the supraorbital to the zygomatic area shortened the latency of the evoked response. Second, these responses were stable (jitter mean consecutive difference < 25 μs) and they had complex potential shapes unmodified by high-frequency stimulation. Finally, collision techniques demonstrated antidromic conduction of impulses in the facial nerve from supraorbital to zygomatic points. Therefore, these “R1-like” responses are not the early component of a functionally recovered blink reflex but motor axon reflexes or ephaptic responses similar to the short latency responses observed following facial nerve regeneration or from sutured nerves in human forearms. © 1996 John Wiley & Sons, Inc.     

Intracranial stimulation of the trigeminal nerve in man. II. Reflex responses.

The reflex responses evoked by direct electrical stimulation of the intracranial portion of the trigeminal nerve have been studied in 16 subjects undergoing percutaneous retrogasserian thermocoagulation for the treatment of trigeminal neuralgia affecting the second or third division. In the obicularis oculi muscle, early and late responses similar to the R1 and R2 components of the blink reflex were recorded. The former could be evoked only by stimulation of the second division and its latency was consistent with intermediately fast afferents. A late reflex (50-70 ms) was occasionally recorded from the anterior belly of the digastric muscle. The response was sometimes followed by a later activity and showed the features of a polysynaptic reflex. No response was obtained in the jaw elevators when fully relaxed. With the subject voluntarily clenching his teeth, both an early "H-like" response and two silent periods in the background EMG were obtained. The second silent period was similar in the muscles ipsi- and contralateral to intracranial stimulation, while the first silent period was longer in the ipsilateral muscles. Possible mechanisms contributing to the inhibition following stimulation of the mixed portion of the nerve are discussed.     

Electrophysiological study of ephaptic axono-axonal responses in hemifacial spasm

One of the classic features of hemifacial spasm (HFS) is spread of the blink reflex responses to muscles other than the orbicularis oculi. The pathophysiological mechanisms underlying the generation of such abnormal responses include lateral spread of activity between neighboring fibers of the facial nerve and hyperexcitability of facial motoneurons. In this report we present evidence for another mechanism that can contribute to the generation of responses in lower facial muscles resembling the R1 response of the blink reflex. In 13 HFS patients, we studied the responses induced in orbicularis oris by electrical stimuli applied at various sites between the supraorbital and zygomatic areas. We identified responses with two different components: an early and very stable component, with an onset latency ranging from 10.5 to 14.8 ms, and a more irregular longer-latency component. Displacement of the stimulation site away from the supraorbital nerve and towards the extracranial origin of the facial nerve caused a progressive shortening of response latency. These features indicate that, in our patients, the shortest latency component of the orbicularis oris response was likely generated by antidromic conduction in facial nerve motor axons followed by axono-axonal activation of the fibers innervating the lower facial muscles. Our results suggest that motor axono-axonal responses are generated by stimulation of facial nerve terminals in HFS.     

Analysis of the corneal reflex with air puff: normal controls and patient groups.

Though there are several reports published about the corneal reflex elicited by different methods, a standardized electrophysiologic study with air puff in man has not been published. The aim of this study is to standardize the corneal reflex elicited by air puff to cornea. The authors studied the corneal reflex with air puff and direct touch by using a standardized method in patients with thalamic hemorrhage (n = 15), hemispheric infarction (n = 9), brainstem infarction (n = 9), multiple sclerosis (n = 12), and Bell's palsy (n = 12) and in normal control subjects (n = 21). The conventional blink reflex (BR) was also studied. The reflex responses were recorded from both orbicularis oculi muscles by air puff and direct touch to cornea in addition to the electrical stimulation of the supraorbital nerve. No statistical difference could be detected between the responses elicited by air puff or direct touch to cornea (P > 0.05). Corneal reflex responses were statistically different from the R2 response of the BR (P < 0.005). Because the responses elicited by direct touch and air puff to cornea are identical, air puff to cornea can be used confidently to study the corneal reflex.     

The orbicularis oculi reflexes in healthy premature and full-term newborns

Blink reflexes were evoked both by mechanical tapping and electrical current delivered to the skin of the periorbital region in 62 healthy babies distributed in 2 groups: 29 full-term newborns and 33 prematures. The electrical activity of the orbicularis oculi muscle was recorded by means of bipolar surface electrodes in all cases. Both ipsilateral R1 and R2 electrically evoked responses were obtained. Occasionally we also observed a late R3 ipsilateral response. The R2 contralateral electrically evoked response was never observed in premature babies; it was present in about 80% of the full-term newborns. The R1 recovery curves obtained by delivering two successive shocks are similar in our two groups of babies to those observed in adults. The R1 latency decreases from 18 msec (27 weeks of post-conceptional age) to 12.4 msec (37 weeks). The average value for the full-term newborns was 12.1 +/- 1.1 msec. Whatever the age mechanical stimulation evokes bilateral R1, R2 and occasionally R3 responses. The existence of central crossed connections is possible. The maturation of the blink reflex occurs essentially during the last months of pregnancy. Indeed the R1 latency measured in full-term newborns is similar to that given for adults.     

Electrophysiological evidence for crossed oligosynaptic trigemino-facial connections in normal man.

A crossed short latency component (R1) of the human blink reflex could be elicited in orbicularis oculi muscles to stimulation of the contralateral supraorbital nerve, when infraliminal conditioning stimuli were applied to various cutaneous afferents of the body (facial, upper and lower limbs). The crossed R1 responses appeared when the time interval between the conditioning and the test stimuli was of 30 to 40 ms, 50 to 65 ms and 95 to 110 ms for facial, upper and lower limbs afferents respectively. For the same time intervals, these conditioning volleys also exerted a facilitatory effect on the ipsilateral R1 responses. Furthermore, crossed R1 responses were also obtained during supraspinal facilitation induced by a voluntary contraction of the eyelids. These data show that crossed oligosynaptic trigemino-facial reflex connections exist in normal subjects, which become functional when adequate conditioning stimuli are available.     

Head extensor reflex evoked by trigeminal stimulation in humans.

OBJECTIVE: Excitatory and inhibitory responses have been recognized in human cervical muscles following trigeminal stimulation. However, no evidence has so far been published of a crossed, short-latency, excitatory response resembling the early head extensor reflex seen in the cat. We seek its existence in humans. METHODS: The study was carried out in 14 voluntary healthy subjects. Percutaneous and surface electrical stimulation of the supraorbital and infraorbital nerves was performed with single, double and repetitive stimuli. Signals were recorded from the relaxed splenius and sternomastoid muscles bilaterally. RESULTS: Percutaneous stimulation of infraorbital nerve with single stimuli evoked an early response in the contralateral splenius muscle, with onset latency ranging from 11 to 14 ms (HR1). This response was greatly facilitated by double or repetitive stimuli. Single stimuli also gave rise to two larger responses in all 4 muscles in the latency ranges 50-70 ms (HR2) and 100-160 ms (HR3). Surface stimulation of one nerve alone could not elicit any early activity. Single surface stimuli delivered simultaneously to the supraorbital and infraorbital nerves evoked HR1 in only 5 subjects. CONCLUSIONS: We detected a crossed early reflex of the head extensor muscles to trigeminal stimuli. Its timing is similar to the 8-ms response seen in cats. The evidence provided suggests that the reflex is mediated by an oligosynaptic circuit and that it needs a strong spatial summation at central synapses.     

Muscle activity during unconditioned and conditioned eye blinks in the rabbit.

EMGs were recorded from the orbicularis oculi, retractor bulbi and superior rectus muscles in rabbits to investigate the time course of muscle activation during unconditioned and conditioned eye blinks. EMGs from the three muscles showed two responses, with the responses of the orbicularis oculi and retractor bulbi showing the same latency, and the responses of the superior rectus lagging. The latency of responses to periorbital electrostimulation was about 5 ms, and to air puff stimulation about 10 ms. Results showed a tight coupling of activity between muscles, with cross-correlograms peaking at 0.65 to 0.85 and showing little time shift. Stimulus-response curves showed clear non-linearities in the response of the muscle to changes in stimulus strength. Local anesthesia of the cornea had little effect on unconditionally evoked responses. The form of unconditionally evoked responses was similar with periorbital electrostimulation and air puff stimuli but differed in latency. These results show the form of the eye blink reflex response and will be of importance in interpreting electrophysiological studies of the classically conditioned eye blink of rabbits.     

Familial congenital facial diplegia: electrophysiologic and genetic studies

A 13-year-old boy with autosomal-dominant congenital facial diplegia was evaluated by electrophysiologic and genetic investigations. Thirteen members of his family were affected over 4 generations. The electrophysiologic studies revealed blink reflex abnormalities. Both R1 and R2 responses were prolonged on the left side after ipsilateral stimulation, while R2 was also delayed by contralateral stimulation. Ipsilateral R1 and R2 were of normal latencies when the right side was stimulated. A third ipsilateral response at 63 msec of latency could be obtained when stimulating the left side. These findings suggest functional damage to the brainstem. Further support for this interpretation was provided by the prolonged time between waves I and V, bilaterally, documented by study of brainstem auditory evoked potentials.     

The relationship of eyelid movement to the blink reflex

Although the blink reflex is a standard neurophysiological investigation its relationship with eyelid movement has not been clearly established. We studied normal subjects and patients with unilateral facial paralysis to define the pattern of eyelid movement following glabellar tap, supraorbital nerve stimulation, facial nerve stimulation and direct corneal stimulation. We found that eyelid closure did not necessarily occur in a single movement. Following glabellar tap the first component of a two-stage movement was initiated by levator palpebrae relaxation while with supraorbital nerve stimulation orbicularis oculi contraction produced the first movement. The compound muscle action potential following direct facial nerve stimulation produced only minimal eyelid movement, the major closure being associated with a longer latency orbicularis oculi reflex. Corneal stimulation elicited a single component eyelid movement. Thus, the pattern of eyelid movement differed for each stimulus reflecting variations in orbicularis oculi contraction and levator palpebrae inhibition.     

Orbicularis oculi and orbicularis oris reflexes in blepharospasm and torticollis spasmodica during spasm-free intervals

To investigate possible abnormalities of the blink reflex pathways, we analyzed the latencies and amplitudes of the blink reflex responses in the orbicularis oculi (Ooculi) muscle, following supraorbital nerve stimulation, in 19 patients with blepharospasm, 16 patients with torticollis spasmodica and 22 control subjects. Furthermore, in order to examine the suprasegmental control of the responses, the reflex responses were also evoked in the orbicularis oris (Ooris) muscle after stimulation of the ipsilateral supraorbital nerve. The responses were recorded only when subjects had no contractions of the eyelid muscles, either involuntarily, voluntarily or spontaneously; this could be controlled by a sound signal. The metrics of the reflex responses in the Ooculi and Ooris muscles in patient groups were comparable to those in controls. Our data indicate that the afferent and efferent pathways of the reflex arc and the suprasegmental control of the reflex are intact in patients with blepharospasm and torticollis spasmodica, at least during spasm-free intervals. Alterations of responses may occur during spasms due to either segmental or suprasegmental changes.     

Neurophysiological evaluation of trigeminal and facial nerves in patients with chronic inflammatory demyelinating polyneuropathy

Cranial neuropathy is clinically uncommon in patients with chronic inflammatory demyelinating polyneuropathy (CIDP), but there is little information on the neurophysiological examination of cranial nerve involvement. To determine the incidence of trigeminal and facial nerve involvement in patients with CIDP, the direct response of the orbicularis oculi muscle to percutaneous electric stimulation of the facial nerve and the blink reflex (induced by stimulation of the supraorbital nerve) were examined in 20 CIDP patients. The latency of the direct response was increased in 12 patients (60%) and an abnormal blink reflex was observed in 17 patients (85%). There was no correlation between electrophysiological findings and the latencies of the direct and R1 responses and disease duration or clinical grade in CIDP patients. Nevertheless, the prevalence of subclinical trigeminal and facial neuropathy is extremely high in patients with CIDP when examined by neurophysiological tests.     

Unmasking of the trigemino-accessory reflex in accessory facial anastomosis

OBJECTIVE: To evaluate the possible blink reflex responses in facial muscles reinnervated by the accessory nerve. METHOD: Eleven patients with a complete facial palsy were submitted to a surgical repair by an accessory facial nerve anastomosis (AFA). In this pathological group, blink reflex was studied by means of percutaneous electrical stimulation of the supraorbital nerve and recording from the orbicularis oculi muscle. A control group comprised seven normal people and seven patients with a complete Bell's facial palsy; in this group, responses on the sternocleidomastoideus (SCM) muscles were studied after supraorbital nerve stimulation. RESULTS: All the patients with AFA showed a consistent degree of facial reinnervation. Ten out of the 11 patients with AFA showed reflex responses; in six, responses were configured by a double component pattern, resembling the R1 and R2 components of the blink reflex; three patients had an R1-like response and one patient showed a unique R2 component. Mean values of latencies were 15.2 (SD 4.6) ms for the R1 and 85.3 (SD 9.6) ms for the R2. In the control group, eight out of 14 people had evidence of reflex responses in the SCM muscles; these were almost exclusively configured by a bilateral late component (mean latency 63.5 (SD15.9) ms) and only one of the subjects showed an early response at 11 ms. CONCLUSION: The trigemino-accessory reflex response in the pathological group was more complex and of a significantly higher incidence than in the control group. These differences could be tentatively explained by a mechanism of synaptic plasticity induced by the impairment of the efferent portion of the reflex. This could unmask the central linking between the trigeminal and the accessory limbs of the reflex. The findings described could be a demonstration of neurobionomic function in the repairing process of the nervous system.     

Reflexes elicited from cutaneous and mucosal trigeminal afferents in normal human subjects

It has been shown that in patients in whom the central stump of the hypoglossal nerve has been anastomosed to the peripheral stump of a lesioned facial nerve, supraorbital nerve stimulation can elicit a short-latency reflex (12.5±0.6 ms; mean±S.D.) in facial muscles similar to the R1 disynaptic blink reflex response, but not followed by an R2 blink reflex component⁴⁶. Thus in addition to replacing the facial neurons at peripheral synapses, these hypoglossal nerves contribute to a trigemino-hypoglossal reflex. The aim of this work was to study the type of reflex activities which can be elicited in both facial and tongue muscles by electrical stimulation of cutaneous (supraorbital nerve) or mucosal (lingual nerve) trigeminal (V) afferents in normal subjects. The results show that although stimulation of cutaneous V1 afferents elicits the well-known double component (R1–R2) blink reflex response in the orbicularis oculi muscles, it does not produce any detectable reflex response in the genioglossus muscle, even during experimental paradigms designed to facilitate the reflex activity. Conversely, stimulation of mucosal V3 afferents can elicit a single reflex response of the R1 type in the genioglossus muscle but not in the orbicularis oculi muscles, even during experimental paradigms designed to facilitate the reflex activity. These data are discussed in terms of two similar but separate circuits for the R1 responses of cutaneous (blink reflex) and mucosal (tongue reflex) origins. They suggest that in patients with hypoglossal-facial (XII–VII) nerve anastomosis, the short-latency trigemino-‘hypoglossal-facial' reflex of the R1 blink reflex type observed in facial muscles following supraorbital nerve stimulation could be due to changes in synaptic effectiveness of the central connectivity within the principal trigeminal nucleus where both cutaneous and mucosal trigeminal afferents project.     

Blink reflex in hemiplegia

Data about the influence of hemispheric lesions on the blink reflex are conflicting. 21 hemiplegic patients and 11 control subjects were investigated. The duration, latency and electric area of electrically evoked blink reflex responses were evaluated by common electromyographic techniques. A depression of the ipsilateral and the consensual late response after stimulation of the paretic side was the most evident finding. However, also a certain increase of the early response and a depression of the late response of the paretic side independent of the side of stimulation emerged. Concerning the parameters taken into account, the evaluation of the latency period seems to be the most significant and reliable. Determination of the electric area provides additional useful data which, however, may easily lead to mistakes.     

Pain-evoked blink reflex

The electrically evoked blink reflex (BR) consists of an ipsilateral R1 component (R1) at 11 ms and two bilateral components R2 at 33 ms and R3 at 83 ms. It is still unclear whether the R2 is mediated by activation of tactile or nociceptive afferents. For testing the nociceptive hypothesis, nociceptors of the supraorbital nerve were selectively activated by infrared laser stimuli in 10 subjects. Only painful laser stimuli evoked a bilateral early polyphasic BR response (LR2) at 71 ms. Stimulation of infraorbital and mental nerve dermatomes was equally effective. A late bilateral reflex response at 130 ms was occasionally observed. Regarding the nociceptor activation time of about 40 ms, onset latencies were within the range of the electrically evoked R2 and R3, respectively. The good accordance of R2 and LR2 may be due to activation of identical nociceptive fibers or to convergence of electrically evoked tactile and laser-elicited nociceptive input onto common multireceptive neurons. © 1997 John Wiley & Sons, Inc. Muscle Nerve, 20, 265–270, 1997.     

Sensorimotor integration in patients with parkinsonian type multisystem atrophy

Sensorimotor integration is an essential feature of the central nervous system that contributes to the accurate performance of motor tasks. Some patients with multiple system atrophy with parkinsonian features (MSAp) exhibit clinical signs compatible with an abnormal central nervous system excitability to somatosen– sory inputs, such as action myoclonus or enhanced cutaneo–muscular reflexes. To investigate further the site where such dysfunction in sensorimotor integration takes place, we examined the inhibitory effects of a cutaneous afferent volley at two different levels of the motor system in 10 MSAp patients and in 10 agematched healthy volunteers. Electrical digital nerve stimuli were given as the conditioning stimulus for the motor evoked potentials (MEP) elicited by transcranial magnetic stimulation in hand muscles, and for the blink reflex responses obtained in the orbicularis oculi muscles by supraorbital nerve stimulation. Intervals for the conditioning were 20 to 50ms for the MEP and 90 to 110ms for the blink reflex. The MEP was significantly inhibited in test trials in healthy volunteers, reaching a mean of 32% of the baseline values at the ISI of 35 ms. Significant inhibition occurred also in the blink reflex, in which the R2 response was a mean of 12% of baseline values at the ISI of 100 ms. The inhibitory effects were abnormally reduced in 8 patients on the MEP, and in 7 patients on the blink reflex. There were significant group differences between patients and control subjects in the size of the conditioned MEP and blink reflex. These results suggest that sensorimotor integration is abnormal in patients with MSAp in at least two central nervous system sites: the sensorimotor cortex, and the brainstem reticular formation.     

Blink reflex in facial-hypoglossal anastomosis

Summary The blink reflex was investigated in two patients after a facial-hypoglossal anastomosis had been performed. In each case the first component of the blink reflex could be demonstrated with normal latency on the operated side after ipsilateral supraorbital stimulation. These findings give further evidence that the first component of the blink reflex is not monosynaptic in nature. The second component of the blink reflex was distinctly retarded in the first case and was not seen at all in the second case. The second component of the blink reflex is influenced strongly by alteration of the intrabulbar and efferent part of the reflex circuits; it shows some correlation with voluntary motor activity.Stipendiary of the Humboldt Foundation.