Interactions of Eye and Eyelid Movements · 325
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OUP UNCORRECTED PROOF – FIRST-PROOF, 13/04/2011, GLYPH 1 CHAPTER 17 2 Interactions of eye and 3 eyelid movements 4 Neeraj J. Gandhi and Husam A. Katnani 5 Abstract 6 Eyelid movements introduce a profound and transient modification in the positions of the eyes. 7 This chapter describes the types of eye position perturbations and highlights the neural signature 8 within the oculomotor neuraxis that may mediate them. Such results also imply that neural 9 commands considered to encode a coordinated movement of the eyes and the head may, in fact, also 10 integrate movements of the eyelid musculature as well as other skeletomotor effectors. This review 11 also considers the use of blinks as a tool to evaluate the time-course of motor preparation of saccades 12 and to probe whether a premotor signal is present during cognitive processes requiring executive 13 control. 14 Neural commands for the generation of eye movements are routinely relayed to non-extraocular 15 effectors. For example, electromyography (EMG) activity in neck muscles precedes the generation of 16 a saccadic eye movement (see also Corneil, Chapter 16, this volume), even when a head movement 17 is not required or generated. Likewise, activity observed in numerous cortical and subcortical regions 18 encodes integrated movements of the eyes and hand (e.g. Buneo and Andersen, 2006 ; Lünenburger 19 et al., 2001 ). Similarly, eyelid musculature is innervated in association with eye movements (Evinger 20 et al., 1994 ; Fuchs et al., 1992 ; Gandhi, 2007 ; Williamson et al., 2005 ). The objective of this chapter is 21 to review the integration of eyelid and eye movements. The first section of this chapter will briefly 22 characterize eyelid movements. The second will discuss the neural pathways that produce eyelid 23 movements and emphasizes the loci of overlapping control for blinks and eye movements, particu- 24 larly saccades. The third section will review the effects of blinks on characteristics of eye movements, 25 and the neural signatures that correlate with the observed behaviour will be highlighted. The final 26 section will consider the use of blinks as a tool to evaluate the time-course of motor preparation and 27 to probe whether a motor signal is present during cognitive processes requiring executive control. 28 Another important topic on disorders associated with eyelid musculature is not considered here but 29 is covered in a recent review by Helmchen and Rambold ( 2007 ). 30 Characteristics of eyelid movements 31 Two types of lid movements are prevalent. The first is a lid saccade, for which the movement of the 32 upper eyelid is yoked primarily to the vertical component of the eye movement. During upward 17-Liversedge-17.indd 323 4/12/2011 10:58:18 AM OUP UNCORRECTED PROOF – FIRST-PROOF, 13/04/2011, GLYPH 324 · Neeraj J. Gandhi and Husam A. Katnani 1 vertical movements (Fig. 17.1A ) the levator palpebrae (LP) muscle contracts and raises the upper 2 eyelid to prevent obstruction of vision. The speed of the lid movement matches that of the eye move- 3 ment, generating lid saccades with rapid eye movements or more gradual changes during smooth 4 pursuit (Becker and Fuchs, 1988 ). Downward eye movements (Fig. 17.1B ) are accompanied by 5 a depression of the eyelid, which is mediated by a reduction in LP muscle activity. During down- 6 ward saccades, in particular, LP EMG ceases and the lid ‘falls’. Such downward lid movements are 7 considered passive since they are controlled entirely by the viscoelastic properties of the ligaments 8 and connective tissue surrounding the lid (Becker and Fuchs, 1988 ; Evinger et al., 1984 ; Guitton 9 et al., 1991 ). 10 The second type of lid movement occurs when the eyelid musculature produces a blink. It can be 11 a reflexive movement, triggered by mechanical stimulation of the cornea or the periorbital skin 12 including the eyelashes. It can also be evoked by electrical stimulation of the supraorbital branch of 13 the trigeminal nerve and by exposure to strong visual and acoustic stimuli. It can be produced as a 14 conditioned response as well. Nevertheless, a blink is most prevalent as a spontaneous movement, 15 likely serving to wet and protect the cornea. In addition, it can be voluntary and accompany facial 16 movements such as winking or grimacing. It can also occur as a gaze-evoked blink that accompanies 17 a head-restrained and head-unrestrained gaze shift (Evinger et al., 1994 ; Gandhi, 2007) (Fig. 17.1C ). 18 This chapter will only consider gaze-evoked blinks and reflexive blinks triggered through trigeminal 19 activation. 20 Blinks are initiated as a rapid depression of the upper eyelid. This response is due to a cessation of 21 activity in the LP muscle plus a burst of activity in the orbicularis oculi (OO) muscle. In contrast to 22 lid saccades, however, the eyelid gradually returns to an elevated position as a result of a decrease in 23 OO discharge and an increase in LP activity (Björk and Kugelberg, 1953 ; Evinger et al., 1984 ). The 24 amplitude of a lid movement during a blink can span a large range, depending on the strength of the 25 mechanical or electrical stimulation. Regardless of the triggering mechanism, all blinks exhibit simi- 26 lar characteristics (Evinger et al., 1991 ; Gruart et al., 1995 ). The peak speeds of both downward and 27 ensuing upward phases of the blink are linearly related to blink amplitude. However, the duration of 28 the downward component is relatively constant, approximately 30 ms for reflexive blinks and 29 approximately 75 ms for spontaneous blinks; while the return or upward component is slower and 20 A B C 0 0 10 –15 –10 Vertical Vertical –30 0 Horizontal eye amp (deg) eye amp (deg) eye amp (deg) –20 TY071309 TY071309 WL101707 10 0 0 5 –5 –10 Vertical Vertical Vertical 0 blink amp (a.u.) –10 –20 blink amp (a.u.) 0 100 200 blink amp (a.u.) 0 100 200 0 100 200 Time (ms) Time (ms) Time (ms) Fig. 17.1 Coordination of eye and eyelid movements. Temporal traces of eye and corresponding eyelid movements during upward (A) and downward (B) head-restrained saccades. Each trace corresponds to one trial, and movements are aligned on saccade onset. The magnetic search coil technique was used to record the position signals. For the eyelid, a small coil was taped to the upper lid (Gandhi and Bonadonna, 2005 ). Note that these lid saccades are fast movements executed in the same direction as the vertical saccades they accompany. The lid saccade data were collected on the same day from one animal. Thus, although the blink signals are shown in arbitrary units, their calibration is identical for the two panels. C) Temporal traces of horizontal, head-restrained saccades (top) accompanied by gaze-evoked blinks (bottom). Data obtained from another animal. The initial, downward phase of the blink is rapid, while the returning upward phase has a slower time course. 17-Liversedge-17.indd 324 4/12/2011 10:58:18 AM OUP UNCORRECTED PROOF – FIRST-PROOF, 13/04/2011, GLYPH Interactions of eye and eyelid movements · 325 1 lasts 100–200 ms, with a modest increase in duration with blink amplitude. Thus, the main sequence 2 trends for blinks are different from those observed for saccades, for which duration increases linearly 3 with amplitude and peak velocity obeys a saturating function (Bahill et al., 1975 ). 4 Integration of neural pathways for eye and eyelid movements 5 The tight coordination of saccade–blink interaction can be attributed to the neural circuits which 6 integrate the generation of saccades with the musculature of the eyelid. The OO muscle resembles a 7 skeletal muscle and is controlled by motoneurons in the facial nucleus (Fig. 17.2 ). Most of the neural 8 projections are from the dorsolateral and intermediate divisions of the ipsilateral nucleus (Porter 9 et al., 1989 ). The firing rates of the motoneurons are correlated with lid velocity (Trigo et al., 1999a ). 10 With respect to oculomotor structures, evidence for contralateral tectofacial and tectoreticulofacial 11 projections exists in the rat and cat (Dauvergne et al., 2004 ; May et al., 1990 ; Morcuende et al., 2002 ; 12 Vidal et al., 1988 ), although it can be argued that these collicular signals may encode movement 13 commands for the vibrissae and pinnae (Cowie and Robinson, 1994 ; Hemelt and Keller, 2008 ; 14 Miyashita and Mori, 1995 ; Vidal et al., 1988 ). The superior colliculus also relays information to the 15 facial nucleus via the regions of sensory trigeminal nucleus complex that receives dense afferents 16 from the eyelids (Dauvergne et al., 2004 ; May and Porter, 1998 ). Even neural signals in cortical struc- 17 tures like the frontal eye fields are polysynaptically relayed to OO muscles (Gong et al., 2005 ). Thus, 18 neural commands from numerous oculomotor structures have multiple avenues to innervate the 19 OO muscle for coordinating blinks with saccadic eye movements. In addition, anatomical studies 20 have also identified trigeminotectal pathways (Huerta et al., 1981 , 1983 ; Ndiaye et al., 2002 ) through 21 which blinks can contribute to the activity in superior colliculus and other oculomotor regions. This 22 sensory information does not appear to encode lid position but is most likely limited to information 23 arising from cutaneous receptors (Trigo et al., 1999b ). 24 The LP is considered an extraocular muscle because it shares its embryogenesis with the supe- 25 rior rectus and is innervated by a branch of the superior division of the oculomotor nerve (Fig. 17.2 ). 26 The cell bodies of these motoneurons reside bilaterally within the central caudal division of the CCN MRF Levator palpebrae (LP) STC SC (5n) Orbicularis oculi (OO) Fac Nuc (7n) Fig.