Differential Effects of Reflex Blinks on Saccade Perturbations in Humans

Studies in both humans and monkeys have indicated that blinks affect the central programming of saccades. In this study, we compared the influence of two types of reflex blinks on the trajectories and kinematics of memory-guided saccades in human subjects. We found that electrical stimulation of the supraorbital nerve shortly before or during a saccade briefly halts or decelerates the eye in midflight. After this short interruption, the eye always resumed its course and reached the target location in the absence of visual feedback. Air puff stimuli produced significant decreases in mean eye velocity too, but in addition to these changes in saccade kinematics, they produced much larger and more variable perturbations of the two-dimensional saccade trajectories. Even so, the endpoints of blink-perturbed saccades obtained under both test conditions remained as accurate and as precise as those observed in the control condition. We hypothesize that the reduction in mean eye velocity is not caused by a trigeminal reactivation of brain stem omnipause neurons but could instead arise from a trigeminal transient inhibition of saccade-related activity in the midbrain superior colliculus (SC). These findings support the theory that blink-perturbed saccades are programmed as slow, but straight, saccades onto which blink-related eye movements are superimposed. This linear superposition occurs downstream from the SC.

Conditioned Eyelid Movement Is not a Blink

Based on kinematic properties and distinct substrates, there are different classes of eyelid movement described as eyeblinks. We investigate whether the eyelid movements made in response to a conditioned stimulus (CS) are a category of eyelid movements distinct from blinks. Human subjects received 60 trials of classical eyelid conditioning with a tone as the CS and electrical stimulation of the supraorbital branch of the trigeminal nerve as the unconditioned stimulus (UCS). Before and after training, reflex blinks were elicited with the UCS. The kinematics of conditioned responses (CRs) differed significantly from those of reflex blinks. The slope of the amplitude-maximum velocity function was steeper for reflex blinks than for CRs, and reflex blink duration was significantly shorter than CR duration. Unlike reflex blinks, for which maximum velocity was independent of blink duration, the maximum velocity of CRs depended on CR duration. These quantitative and qualitative differences indicated that CRs were a unique class of eyelid movements distinct from blinks and eyelid movements with vertical saccadic gaze shifts.

Effects of Caffeine on the Trigeminal Blink Reflex

The acoustic startle and trigeminal blink reflexes share the same motor output. Since caffeine has been shown to augment the startle reflex, it was proposed that caffeine would also increase the trigeminal blink reflex. In 6 humans, the effects of caffeine (100 mg) on the trigeminal blink reflex were investigated. Reflex blinks were elicited by stimulation of the supraorbital branch of the trigeminal nerve. Following ingestion of caffeinated coffee, reflex blinks increased in amplitude and duration and occurred at a shorter latency than reflex blinks following ingestion of decaffeinated coffee. Since the blink reflex is a brainstem reflex, these results suggest that the psychomotor effects of caffeine facilitate brainstem processing.

Blink-Perturbed Saccades in Monkey. II. Superior Colliculus Activity

Trigeminal reflex blinks evoked near the onset of a saccade cause profound spatial-temporal perturbations of the saccade that are typically compensated in mid-flight. This paper investigates the influence of reflex blinks on the discharge properties of saccade-related burst neurons (SRBNs) in intermediate and deep layers of the monkey superior colliculus (SC). Twenty-nine SRBNs, recorded in three monkeys, were tested in the blink-perturbation paradigm. We report that the air puff stimuli, used to elicit blinks, resulted in a short-latency (∼10 ms) transient suppression of saccade-related SRBN activity. Shortly after this suppression (within 10–30 ms), all neurons resumed their activity, and their burst discharge then continued until the perturbed saccade ended near the extinguished target. This was found regardless whether the compensatory movement was into the cell's movement field or not. In the limited number of trials where no compensation occurred, the neurons typically stopped firing well before the end of the eye movement. Several aspects of the saccade-related activity could be further quantified for 25 SRBNs. It appeared that 1) the increase in duration of the high-frequency burst was well correlated with the (two- to threefold) increase in duration of the perturbed movement. 2) The number of spikes in the burst for control and perturbed saccades was quite similar. On average, the number of spikes increased only 14%, whereas the mean firing rate in the burst decreased by 52%. 3) An identical number of spikes were obtained between control and perturbed responses when burst and postsaccadic activity were both included in the spike count. 4) The decrease of the mean firing rate in the burst was well correlated with the decrease in the velocity of perturbed saccades. 5) Monotonic relations between instantaneous firing rate and dynamic motor error were obtained for control responses but not for perturbed responses. And 6) the high-frequency burst of SRBNs with short-lead and long-lead presaccadic activity (also referred to as burst and buildup neurons, respectively) showed very similar features. Our findings show that blinking interacts with the saccade premotor system already at the level of the SC. The data also indicate that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensation for blink-related perturbations. We propose that these interactions occur downstream from the motor SC and that the latter may encode the desired displacement vector of the eyes by sending an approximately fixed number of spikes to the brainstem saccadic burst generator.

Blink-Perturbed Saccades in Monkey. I. Behavioral Analysis

Saccadic eye movements are thought to be influenced by blinking through premotor interactions, but it is still unclear how. The present paper describes the properties of blink-associated eye movements and quantifies the effect of reflex blinks on the latencies, metrics, and kinematics of saccades in the monkey. In particular, it is examined to what extent the saccadic system accounts for blink-related perturbations of the saccade trajectory. Trigeminal reflex blinks were elicited near the onset of visually evoked saccades by means of air puffs directed on the eye. Reflex blinks were also evoked during a straight-ahead fixation task. Eye and eyelid movements were measured with the magnetic-induction technique. The data show that saccade latencies were reduced substantially when reflex blinks were evoked prior to the impending visual saccades as if these saccades were triggered by the blink. The evoked blinks also caused profound spatial-temporal perturbations of the saccades. Deflections of the saccade trajectory, usually upward, extended up to ∼15°. Saccade peak velocities were reduced, and a two- to threefold increase in saccade duration was typically observed. In general, these perturbations were largely compensated in saccade mid-flight, despite the absence of visual feedback, yielding near-normal endpoint accuracies. Further analysis revealed that blink-perturbed saccades could not be described as a linear superposition of a pure blink-associated eye movement and an unperturbed saccade. When evoked during straight-ahead fixation, blinks were accompanied by initially upward and slightly abducting eye rotations of ∼2–15°. Back and forth wiggles of the eye were frequently seen; but in many cases the return movement was incomplete. Rather than drifting back to its starting position, the eye then maintained its eccentric orbital position until a downward corrective saccade toward the fixation spot followed. Blink-associated eye movements were quite rapid, albeit slower than saccades, and the velocity-amplitude-duration characteristics of the initial excursions as well as the return movements were approximately linear. These data strongly support the idea that blinks interfere with the saccade premotor circuit, presumably upstream from the neural eye-position integrator. They also indicated that a neural mechanism, rather than passive elastic restoring forces within the oculomotor plant, underlies the compensatory behavior. The tight latency coupling between saccades and blinks is consistent with an inhibition of omnipause neurons by the blink system, suggesting that the observed changes in saccade kinematics arise elsewhere in the saccadic premotor system.

Kinetic and Frequency-Domain Properties of Reflex and Conditioned Eyelid Responses in the Rabbit

Eyelid position and the electromyographic activity of the orbicularis oculi muscle were recorded unilaterally in rabbits during reflex and conditioned blinks. Air-puff–evoked blinks consisted of a fast downward phase followed sometimes by successive downward sags. The reopening phase had a much longer duration and slower peak velocity. Onset latency, maximum amplitude, peak velocity, and rise time of reflex blinks depended on the intensity and duration of the air puff–evoking stimulus. A flashlight focused on the eye also evoked reflex blinks, but not flashes of light, or tones. Both delayed and trace classical conditioning paradigms were used. For delayed conditioning, animals were presented with a 350-ms, 90-dB, 600-Hz tone, as conditioned stimulus (CS). For trace conditioning, animals were presented with a 10-ms, 1-k/cm2 air puff, as CS. The unconditioned stimulus (US) consisted of a 100-ms, 3-k/cm2 air puff. The stimulus interval between CS and US onsets was 250 ms. Conditioned responses (CRs) to tones were composed of downward sags that increased in number through the successive conditioning sessions. The onset latency of the CR decreased across conditioning at the same time as its maximum amplitude and its peak velocity increased, but the time-to-peak of the CR remained unaltered. The topography of CRs evoked by short, weak air puffs as the CS showed three different components: the alpha response to the CS, the CR, and the reflex response to the US. Through conditioning, CRs showed a decrease in onset latency, and an increase in maximum amplitude and peak velocity. The time-to-peak of the CR remained unchanged. A power spectrum analysis of reflex and conditioned blink acceleration profiles showed a significant ≈8-Hz oscillation within a broadband of frequencies between 4 and 15 Hz. Nose and mandible movements presented power spectrum profiles different from those characterizing reflex and conditioned blinks. It is concluded that eyelid reflex responses in the rabbit present significant differences from CRs in their profiles and metric properties, suggesting different neural origins, but that a common ≈8-Hz neural oscillator underlies lid motor performance. According to available data, the frequency of this putative oscillator seems to be related to the species size.