KINEMATICS OF SPONTANEOUS, REFLEX, AND CONDITIONED EYELID MOVEMENTS IN THE ALERT CAT

1. Upper eyelid position and velocity, and the electromyographic (EMG) activity of the orbicularis oculi muscle, were recorded bilaterally i n alert cats during spontaneous, reflexively evoked, and conditioned e yelid movements. 2. Spontaneous blinks appeared randomly (0.2-0.5 per min) and consisted of a fast, large downward lid movement followed by a slower up phase. Blinks of smaller amplitude and slower velocity wer e also observed mainly accompanying behavioral movements, such as duri ng peering and grimacing. 3. Eyelid response to air puffs applied to t he cornea and tarsal lid skin consisted of a short-latency (9-16 ms), fast (up to 2,000 degrees/s) downward movement that lasted for 25-30 m s, followed by late, small downward sags that were sometimes still evi dent after stimulus offset. Blinks outlasted the duration of the stimu lus by approximate to 150 ms. Blinks elicited by flashes of light or t ones showed longer latency (47.3 +/- 6.3 and 53.7 +/- 8.0 ms, mean +/- SD, respectively), smaller amplitude, and a quicker habituation than air-puff-evoked lid responses. 4. For the down phase of the blink, the peak velocity, but not its duration, increased Linearly with blink am plitude. Because the rise time of the down phase remained constant, ch anges in blink amplitude seemed to be the result of increased blink ve locity. The down phase of a typical 10 degrees blink was 10 times fast er than the up phase of the same blink or than upward and downward lid saccades of the same amplitude. The peak velocity and duration of the up phases of reflex blinks and upward and downward lid saccades incre ased linearly with lid movement amplitude. 5. The initial down phase o f air-puff-evoked blinks decreased in latency, increased in amplitude and peak velocity, and maintained the same rise time for increasing pu ff pressure. None of these parameters was dependent on puff duration. The duration of the blink also increased linearly with air puff durati on. 6. The amplitude of air-puff-evoked blinks was inversely related t o lid position, decreasing with further lid positions in the closing d irection. In contrast, neither peak nor integrated EMG activity of the orbicularis oculi muscle was affected by lid position, being only a f unction of stimulus parameters and of the animal's level of alertness. 7. Air puffs >20 ms and >1 kg/cm(2) evoked two successive bursts (R(a p)1 and R(ap)2) in the EMG activity of the orbicularis oculi muscle. S horter and/or weaker stimuli evoked only the R(ap)1 response. Both R(a p)1 and R(ap)2 responses contributed to the generation of the initial down phase of air-puff-evoked blinks. 8. The latency and amplitude of reflex blinks were dependent on the skin receptors activated by the ai r puff. Air puffs directed to the cornea and tarsal lid skin evoked bl inks of shorter latency and larger amplitude than air puffs directed t o periorbital skin areas. Topical anesthesia of corneal receptors bloc ked the appearance of the R(ap)2 component, reducing by approximate to 1/2 the amplitude and peak velocity of the initial down phase of the blink. Air-puff-evoked blinks are thus the result of the activation of fast-conducting, low-threshold receptors, located in the lid skin, th at produce the R(ap)1 response, and of more slowly conducting, higher- threshold mechanoreceptors, located in the cornea, sclera, and tarsal skin, that produce the R(ap)2 response. 9. The late downward sags that followed the initial fast down phase of air-puff-evoked blinks were a lso dependent in their latency and amplitude on air puff pressure, How ever, these sags occurred at a dominant frequency of approximate to 25 Hz, which was independent of stimulus parameters, suggesting that thi s frequency is a property of the neural circuit controlling reflex bli nks. 10. Neither lid saccades nor slow lid movements evoked by ramp op tokinetic stimulation were accompanied by any detectable EMG activity in the orbicularis oculi muscle. The gain of upward slow lid movements during optokinetic stimulation was larger than that of downward lid m ovements, particularly at higher ramp speeds. 11. Animals were classic ally conditioned with four different paradigms. The unconditioned stim ulus (US) always consisted of a long, strong air puff applied to the l eft eyelid. Conditioned stimuli (CSs) differed in sensory modality (ai r puff or tones), intensity (weak or strong air puffs), or presentatio n side (air puffs ipsilateral or contralateral to the US). 12. For ips ilateral weak and strong air puffs, and tones used as CSs, the conditi oned response (CR) reached a 95% criterion during the second (weak and strong air puffs) or fourth (tone) conditioning sessions. Weak air pu ffs applied contralaterally as a CS never reached >40% of CRs. The lat ency of the CRs decreased slowly, whereas their peak velocity and time to peak amplitude increased to saturation at the fourth to fifth cond itioning sessions. The CR amplitude also increased until a complete cl osure of the lids was reached. 13. The latency of the CR was a functio n of the stimulus used as CS (tone or air puff) and of the side where the CS was presented (ipsilateral or contralateral to the US). For the four conditioning paradigms, the latency of the CR was always in the range of the corresponding reflex response and did not depend on CS-US interval. It is concluded that CRs are initiated in the same brain st em circuits that produce the unconditioned response, i.e., the reflex response, according to CS sensory modality, duration, strength, and pr esentation side. 14. The peak velocity of the down phase of the CR was also linearly related to CR amplitude, but with lower gains (1/5-1/10 , depending on CS sensory modality and strength) than those described for air-puff-evoked blinks. 15. The CR appeared as a downward lid move ment radiating from its onset, in a close temporal proximity to the CS , toward the US, where it reached its maximum amplitude. The CR was fo rmed by successive small downward sags similar in amplitude to the lat e components observed in reflex blinks. These sags were the result of small but conspicuous spikes present in the EMG of theorbicularis ocul i muscle. The number of these sags increased, and their duration and a mplitude decreased, with successive conditioning sessions until straig ht and dumped lid CRs were reached. At the same time and as the proxim al cause of these motor changes, the orbicularis oculi muscle changed from a phasic EMG activity to a tonic firing that was mainta