Lid restraint evokes two types of motor adaptation

Abstract

Unilateral reduction in eyelid motility produced two modes of blink adaptation in humans. The first adaptive modification affected both eyelids. Stimulation of the supraorbital branch of the trigeminal nerve (SO) ipsilateral to the upper eyelid with reduced motility evoked bilateral, hyperexcitable reflex blinks, whereas contralateral SO stimulation elicited normally excitable blinks bilaterally. The probability of blink oscillations evoked by stimulation of the ipsilateral SO also increased with a reduction in lid motility. The increased probability of blink oscillations correlated with the enhanced trigeminal reflex blink excitability. Thus, the trigeminal complex ipsilateral to the restrained eyelid coordinated an increase in excitability and blink oscillations independent of the eyelid experiencing reduced motility. The second type of modification appeared only in the eyelid experiencing reduced motility. When tested immediately after removing lid restraint, blink amplitude increased in this eyelid relative to the normal eyelid regardless of the stimulated SO. A patient with seventh nerve palsy exhibited the same two patterns of blink adaptation. These results were consistent with two forms of adaptation, presumably because unilateral lid restraint produced two error signals. The corneal irritation caused by reduced blink amplitude generated abnormal corneal inputs. The difference between proprioceptive feedback from the blink and expected blink magnitude signaled an error in blink amplitude. The corneal irritation appeared to drive an adaptive process organized through the trigeminal complex, whereas the proprioceptive error signal drove an adaptive process involving just the motoneurons controlling the restrained eyelid.

Fig. 1.

Unilateral lid restraint alters trigeminal reflex blinks. A, The relative amplitudes of a blink (Condition) evoked by a 2T SO stimulus (dotted line SO) and a blink (Test) elicited by an identical SO stimulus (dotted line SO) 500 msec later are different before (Pre) and after (Post) 165 min of upper eyelid restraint. After lid restraint, a single 2T SO stimulus evokes a reflex blink and additional blinks (Blink Oscillation) that occur at a constant time relative to the onset of the preceding blink. Each trace is a single trial from the left eyelid. B, The relative amplitudes of left lid (solid line) and right lid (dashed line) movement evoked by a left SO (LSO) or right SO (RSO) stimulus are different before (Pre) and after (Post) 2 hr of left upper eyelid restraint. Each trace is a single trial.

Fig. 2.

Unilateral lid restraint increases the excitability of blinks evoked by stimulation of the SO ipsilateral (Ipsi) to the restrained eyelid but not to stimulation of the contralateral (Contra) SO. For blinks evoked by the SO ipsilateral (●) and contralateral (○) to the restrained eyelid, the mean ± SEM excitability relative to the median prerestraint excitability for all subjects is plotted as a function of time after unilateral lid restraint for the 500 (A) and 1000 (B) msec interstimulus intervals. Lid restraint was removed at 165 min (Post, dashed line).

Fig. 3.

Blink oscillation probability increased and blink oscillation latency decreased with lid restraint. A, The mean ± SEM number of blink oscillations per trial for all subjects is plotted as a function of time after unilateral lid restraint for blink oscillations evoked by the SO ipsilateral (●) and contralateral (○) to the restrained eyelid. Lid restraint was removed at 165 min (dashed line). B, Blink density of blink oscillations produced by ipsilateral SO stimulation is plotted as a function of time after the onset of the preceding blink for blink oscillations elicited before (Pre,dashed line) and immediately after (Post,solid line) unilateral lid restraint for a single subject.

Fig. 4.

Unilateral facial palsy alters trigeminal blinks.A, The relative amplitude of blinks evoked by a 2T SO stimulus (first dashed line Stim) and an identical SO stimulus (second dashed line Stim) occurring 250 msec later are different for stimulation of the SO ipsilateral (Right SO, top trace) or contralateral (Left SO, bottom trace) to the right facial palsy. Each trace is a single trial from the unaffected, left, upper eyelid. B, A single 2T SO stimulus (dashed line Stim) ipsilateral (Right SO, top traces) and contralateral (Left SO, bottom traces) to the facial palsy evokes a reflex blink and additional blinks (Blink Oscillation) that occur at a constant time relative to the onset of the preceding blink. Each trace is a single trial from the unaffected, left, upper eyelid.

Fig. 5.

Trigeminal reflex blinks of the subject with right facial nerve palsy were hyperexcitable relative to those of age-matched control subjects. For the unaffected eyelid, the amplitude of the blink evoked by the second of two identical SO stimuli (Test) divided by the amplitude of the blink evoked by the first SO stimulus (Condition) is plotted as a function of the interstimulus interval between the SO stimuli for age-matched control subjects (Control, ♦; ±SEM) and the facial palsy subject tested 30 (●, ○) and 121 (▴, ▵) d after the onset of right facial nerve palsy. ●, ▴, Data from stimulation of the SO ipsilateral to the facial palsy (RSO). ○, ▵, Data from stimulation of the SO contralateral to the facial palsy (LSO). Each point is the mean of at least four trials. Control subject data are from those of Peshori et al. (2001).

Fig. 6.

Eyelid motility determines trigeminal reflex blink excitability. The mean excitability of the subject with right facial nerve palsy divided by the mean excitability of age-matched control subjects for the 250 msec interstimulus interval is plotted as function of the mean blink amplitude of the palsied eyelid divided by the mean blink amplitude of the unaffected eyelid for each day tested. ●, Data from stimulation of the SO ipsilateral to the right facial nerve palsy (right SO). ○, Data from stimulation of the contralateral SO (left SO).

Fig. 7.

The timing of blink oscillations is different after stimulation of the SO ipsilateral (Ipsi,solid traces) and contralateral (Contra,dashed traces) to the eyelid with facial nerve palsy. Blink density is plotted as a function of time relative to the onset of the preceding blink for blink oscillations elicited by stimulation of the ipsilateral and contralateral SO 30 (A) and 93 (B) d after the onset of facial nerve palsy.

Fig. 8.

Trigeminal reflex blink excitability correlates with blink oscillations per trial. Blink oscillations per trial are plotted as a function of trigeminal reflex blink excitability averaged over all tested intervals in the paired stimulus paradigm relative to prerestraint data (■) or relative to data from age-matched control subjects (▪; Peshori et al., 2001). Each open symbolindicates the average data from one subject with lid restraint, and each filled symbol indicates data from 1 d of testing of the seventh nerve palsy subject.