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Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri
Submitted 16 September 2004; accepted in final form 23 October 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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). In lateral-eyed species, such as frogs (Dieringer and Precht 1982), lizards (Gioanni et al. 1993), rabbits (Baarsma and Collewijn 1974), chinchillas (Merwin et al. 1989), and guinea pigs (Escudero et al. 1993), eye movements in response to motion when the head is fixed have largely been shown to be undercompensatory. For example, in pigeons, we recently found that the three-dimensional (3-D) vestibuloocular (VOR) responses to both rotational and linear motion were significantly undercompensatory in gain (Dickman and Angelaki 1999; Dickman et al. 2000). The results seen in pigeons were somewhat surprising, since birds must surely stabilize their vision during demanding motions, such as those experienced during walking, running, or flight (Wallman and Letelier 1993). In fact, when a bird is enclosed in an observer's hands and the animal is rotated, a pronounced head movement is noted. In addition, whether flying or walking, birds can easily maintain quite stable head orientations despite body aspect changes (Erichsen et al. 1989; Gioanni 1988a; Outerbridge 1969; Troje and Frost 2000; Wohlschlager et al. 1993). Thus subjectively, it appears that robust compensatory head responses are contributing to gaze stabilization.
Compared with the vast knowledge regarding the oculomotor system, less is known about the various functional pathways and mechanisms underlying head movement and gaze control (Vibert et al. 1997; Wilson and Schor 1999). In humans, when the head is free to move, gaze stabilization has been shown to be completely compensatory (Crane and Demer 1997; Demer and Crane 2001). Gaze is mathematically defined as eye-in-space and is the complex sum of the eye-in-head and the head-in-space (Newlands et al. 2001; Phillips et al. 1996). During head-fixed VOR conditions using passive, whole body rotations, head-in-space movement is zero, thus gaze equals eye-in-head. Mechanistically, gaze is comprised of important contributions from the VOR, vestibulocollic (VCR), and cervicocollic (CCR) reflexes and head inertia responses (Keshner and Peterson 1995; Peng et al. 1996; Peterson et al. 1985). Recent studies have shown that one aspect of the head response, the VCR, functions as a closed-loop system (Gioanni 1988a; Peng et al. 1996), with negative feedback for low and mid-frequency stimuli. However, at high frequencies, it appears that head mechanics are dominated by inertial forces, and gaze is highly comprised of VOR output. In the turtle and the frog, Dieringer et al. (1983) have shown that a significant portion of gaze stabilization by head responses (>80%) appears "compulsory," whereas the eyes play a more limited role.
For birds, Gioanni (1988a) has asserted that eye-head coupling is stronger than in amphibians or mammals, using significant eye movements when the head is fixed, along with significant head movements if the head is unrestrained. He observed increased gaze gains above those seen in head-restrained conditions during rotations in the dark and unity gaze responses in the light when vision was present (Gioanni 1988a). At low rotational frequencies (<0.06 Hz), head gains were less than VOR gains, yet with the addition of optokinetic (OKN) stimuli at these low frequencies, near perfect gaze stabilization was achieved (Gioanni 1988a). Spatial gaze stabilization in pigeons has also been examined during natural behaviors such as flight, landing, walking, pecking, and head bobbing (Erichsen et al. 1989; Troje and Frost 2000; Wohlschlager et al. 1993).
While these works have increased our understanding of how gaze reflexes function, much remains to be learned. Many of these studies were limited to head movements in a single plane of stimulation at low frequencies and examined either directional eye movements only or neck flexion. In this study, we sought to characterize the 3-D eye, head, and gaze responses during rotational motion in multiple planes and over a large frequency bandwidth (Dickman et al. 2000; Gioanni 1988a). We were additionally curious to see if differing gaze strategies had developed for different bird species depending on behavioral adaptations to either primarily arboreal (pigeons) or terrestrial (quail) niches.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Implantation procedures
All birds were chronically implanted with a Delrin head stud attached via titanium self-tapping screws. Prior to surgery, dual eye coils for monitoring eye positions were fabricated. For pigeons, the dual eye coils were constructed using three turns of multi-stranded, Teflon-coated, 41-gauge stainless steel wire (A & M Systems) for a direction coil, along with a 100-turn watchmaker torsion coil (Sokymat Sa) covered with Aryldite (Ciba-Geigy) attached perpendicularly to the direction coil. The coils were oriented such that their sensitivity vectors were nearly orthogonal.
Chronic implantations of the head stud for all birds and the eye coil (pigeons) were performed during separate surgical procedures. Under isoflurane gas (3% in O2) via endotracheal intubation, the conjunctiva was excised circumferentially to allow visualization of the sclera. Unlike primates and other animals, the pigeon has a flat calcified sclera that is impenetrable to fine, suturing needles. Thus sutures were attached at the corneal margin of the cut conjunctiva using 8–0 prolene followed by conjunctival reapproximation using 8–0 vicryl. Nanoconnectors (Omnetics) were attached to the leads and buried in dental acrylic next to the head studs. A separate dual search coil was attached on, or next to, the head stud to monitor head movements.
For quails, two watchmaker 100-turn coils were glued together in orthogonal orientations. These coils were not surgically implanted due to the diminutive size of the eye, but were instead formed into a curved contact lens (Dickman et al. 2000). Each animal was lightly anesthetized with isoflurane via a nose cone, the eye was anesthetized with proparacaine, and the coil was attached to the cornea with cyanoacrylate adhesive. After the experiment, the coil and adhesive were removed using saline flush, followed by corneal examination using fluorescein strips. After coil removal, ophthalmic ointment and analgesic for corneal irritation were administered. The contact lens coil did not restrict the eye movement, since the nictitating membrane in quails is small, generally retracted, and with the stimuli used, the eye typically rotated <15° in the orbit (thus the coil did not contact the membrane). Eyelid and/or nictitating membrane blinks were easily recognizable in the eye movement traces, and when present, were eliminated from the responses in a manner similar to that of desaccading. As a comparison, negligible differences in results were observed in a test pigeon in which both a glued-on coil as well as an implanted coil were used.
Experimental protocols
A three-field AC magnetic coil system (CNC Engineering) was used to monitor rotational eye and head movements. The field-coils provided a 5-in homogenous cube centered about the pigeon's head and were mounted to a servo-controlled rotator/sled system (Neurokinetics). The system was controlled by a PC using a programmable interface (CED Model 1401plus, Cambridge Electronic Design) and custom written scripts for stimulus control and data acquisition (Spike2, CED). Stimulus waveforms were monitored using an accelerometer and a rate sensor mounted near the animal's head.
Following a 1-wk recovery period after surgery, each animal was placed in a padded body holder and secured in the motion stimulus device. The animal was placed beak forward, and a field-coil centered (head-fixed) reference frame (as shown in Fig. 1) for quantifying eye and head movements was adopted. Eye and head movement responses were obtained using both head-fixed (VOR) and head-free conditions. Sinusoidal rotational motions were delivered along either the earth-vertical axis (EVA; yaw, 0.01–2 Hz, 20°/s) or the earth-horizontal axis (EHA; pitch and roll, 0.02–4 Hz, 20°/s) in complete darkness.
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Procedures for analyses used in this study have been previously described in detail (Angelaki et al. 2000, 2003; Dickman and Angelaki 1999; Dickman et al. 2000). Briefly, prior to each experiment, spontaneous eye movements (head-fixed) and head movements (head-free) to orienting stimuli were recorded for 60 s. From these spontaneous movements, mean primary eye and head positions were calculated. This calibration procedure has been used successfully in the past for three-field systems to determine eye coil sensitivity and primary position in several species and serves as a good approximation as long as DC offsets are negligible (Angelaki et al. 2003; Tweed et al. 1990).
The recorded eye movement signals were first converted to rotation vectors—Ehor, Ever, and Etor for head-fixed or Ghor, Gver, and Gtor for head-free—in Cartesian coordinates (expressed relative to a head-fixed coordinate system) using the mean eye position as a reference (Dickman and Angelaki 1999; Haustein 1989; Hess et al. 1992; van Opstal 1993). Horizontal, vertical, and torsional eye and head movements were defined as rotations about the animal's z-, y-, and x-head axes, respectively. It should be noted that, for pigeons and quails, both lateral-eyed birds, the optic visual axis (Fig. 1) is located 
60–66° lateral to the beak (Fitzgerald 1969; Martinoya 1984). Head movement signals were converted to Hhor, Hver, and Htor rotation vectors, with positive direction conventions being defined as leftward (z-axis), downward (y-axis), and clockwise (x-axis) from the animal's perspective, respectively. The rotation vectors were desaccaded using scripts written in Matlab (MathWorks), which allowed semiautomatic input (Dickman and Angelaki 1999). The desaccaded rotation vectors were differentiated to produce rotation velocity vectors (eye/gaze and head). From the eye and head position and velocity vectors, angular velocity vectors with components in the horizontal, vertical, and torsional planes were calculated for eye (
Etor, Ever, Ehor) or gaze (Gtor, Gver, Ghor), along with the head (Htor, Hver, Hhor). Because each subject made occasional volitional gaze saccades, data were accepted only when the head was held within 30° of reference position during the stimulus. Several cycles were averaged and fit with a sine curve using a least-squares algorithm where the mean eye position was the sum of a DC offset position and a modulation term (Dickman and Angelaki 1999). The fitted mean sine curves were used to calculate gain and phase values in each of the three planes. Gain was expressed as the ratio of peak eye/head/gaze velocity to peak rotation velocity. Phase was expressed as the difference (°) between peak response velocity and peak stimulus velocity. The gain and phase of the eye-in-head response (Fig. 3) were computed from the complex vectorial equation E = G – H. To compute averages, the magnitude (gain) and phase values were first converted into complex format, ci = xi + yij, where j = 
. Next, an average value for each component x, y was computed, and the resulting complex number was converted into its polar form (for a detailed derivation, see Wei and Angelaki 2001)
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and 
are the variances.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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During head-fixed EVA rotation in the dark, as shown in Fig. 2A, only VOR horizontal eye movement components were observed, similar to all other species studied. The desaccaded slow phase eye velocity responses were compensatory in direction, but undercompensatory in amplitude to the imparted rotation. The corresponding head movement traces (Fig. 2A) showed that the head remained stationary with respect to the coil frame during the stimulation. Some vertical and torsional eye movement components were present; however, these secondary responses were typically an order of magnitude less than the primary component response. As previously reported for birds, saccades (and fast phases) were followed by a brief high-frequency eye oscillation (30 Hz) (Anastasio and Correia 1988; Dickman et al. 2000; Nye 1969; Wallman and Pettigrew 1985).
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5° leftward to 0° at the end of the run. Such drifts were typically due to a corresponding change in head position.
Both the gain and phase of the eye, head, and gaze responses were dependent on frequency, as shown for one animal in Fig. 3. During head-fixed motion, the VOR remained undercompensatory, reaching a maximum response gain in this bird of only 0.46 (eye velocity/head velocity; Fig. 3, 
). In contrast, during head-free yaw rotation, the gaze gain increased as stimulus frequency increased to an average value of 0.86 at 1 Hz and 0.78 at 2 Hz (Fig. 3, 
). Across all frequencies, it was the rotation of the head, rather than the eye-in-head, that contributed the most to gaze stabilization (Fig. 3, 
). For example, the head gain increased with stimulus frequency in parallel to the gaze gain to reach a maximum value of 0.77 at 1 Hz and 0.65 at 2 Hz. In contrast, the eye-in-head component of gaze in head-free conditions was small and frequency independent (0.13; Fig. 3, 
). At low frequencies, all components exhibited large phase leads (48–110°), which decreased with increasing frequency. At 0.5–2 Hz, eye, head, and gaze velocities were nearly in phase with the stimulus velocity. Mean yaw data from six pigeons are summarized in Fig. 4. Consistent with the single animal observations of Fig. 3, head rotation in head-free pigeons was the major contributor to gaze stabilization. Importantly, the eye-in-head contribution was low at all frequencies during head-free motion, although VOR gain in head-fixed animals was significantly higher (F(1,10) = 68.2, P < 0.001).
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Quail eye, head, and gaze responses
To compare if the observed gaze responses for pigeons were characteristic for other lateral-eyed bird species, we also examined responses of six Japanese quails using identical stimulus protocols. Figure 5 shows position and velocity for eye, head, and gaze responses in one adult quail. During head-fixed EVA 0.5-Hz rotational motion, the VOR (horizontal eye movements) was undercompensatory, similar to that of pigeons (Fig. 5A). When the head was free to move (Fig. 5B), horizontal gaze position and velocity modulations were of large amplitude and approached unity for the 0.5-Hz rotation stimulus. However, the observed head movement component of gaze in quails was much less than that seen in pigeons.
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These results are summarized in Fig. 7, which plots the respective head-fixed and head-free eye, head, and gaze values at 0.5 Hz for pigeons and quails. First, the eye-in-head rotations were significantly greater (F(1,22) = 28.3, P < 0.001) for the head-fixed VOR compared with head-free rotations (Fig. 7A). This difference was larger for pigeons than quails(F(1,20) = 16.3, P < 0.01). However, despite smaller eye-in-head contributions, the head-free gaze component was of significantly larger magnitude (near unity) than the head-fixed VOR (Fig. 7B) for both pigeons (F(1,20) = 45.2, P < 0.01) and quails (F(1,18) = 10.5, P < 0.01). On closer inspection, it can be seen that the quail gaze response to EVA yaw rotation was more similar to the corresponding VOR response, whereas pigeon gaze responses to EHA roll stimulation differed most from their corresponding VOR responses. Finally, when the eye component gain is plotted versus the head component gain (Fig. 7C), head-free pigeons appear to use head movements more than eye-in-head rotation for gaze stabilization. In contrast, quails used both head and eye movements for gaze stabilization. The difference in the head response gains between the species was significant (F(1,20) = 15.8, P < 0.01).
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DISCUSSION |
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; Wilson et al. 1995). Although previous studies have investigated the different components that contribute to bird gaze stabilization including eye movements (Anastasio and Correia 1988; Dickman and Angelaki 1999; Dickman et al. 2000; Nye 1969), vestibulocollic responses (Gioanni 1988a; Gioanni and Sansonetti 1999), neck muscle activation (Hayman and Donaldson 1997; Hayman et al. 1993), and behavior (Nalbach 1992; Troje and Frost 2000; Turke et al. 1996; Wohlschlager et al. 1993), in this study, we have shown for the first time differences in gaze control strategies between two different bird species. Specifically, we found that, unlike the undercompensatory head-fixed VOR for both pigeons and quails, gaze was completely compensatory during normal head motion. This compensation was achieved primarily with head movements in pigeons, but with combined head and eye-in-head contributions in quails. Aside from the differences in ocular anatomy (the pigeon has 2 foveal areas, unlike the quail), it is tempting to suggest that the disparity between the contributory components of stabilization between these two species may arise from their substantially different flight and foraging behaviors. Head-fixed VOR
The 3-D VOR responses to rotational motion observed in this study with the animal's head fixed were comparable with those reported previously for lateral-eyed birds (Anastasio and Correia 1988; Dickman et al. 2000). In complete darkness, both the pigeon and the quail VOR slow-phase eye velocity gains were severely undercompensatory for visual stabilization relative to head velocity, regardless of the plane of rotational motion. Higher VOR gains have been reported for pigeons receiving amphetamines, although those values still remained undercompensatory (Anastasio and Correia 1988; Gioanni 1988a). Like all animals, pigeons and quails exhibit a VOR response in the dark that is dependent on stimulus frequency. During EVA rotational motion, low gains and phase advances were observed, with improved responses noted as stimulus frequency increased. However, during EHA rotations, the low frequency pitch and roll gains were improved, and the phase leads were smaller compared with EVA motion. Similar to previous reports in all species, these effects have been attributed to the contribution of otolith signals that could provide an additional reference of head velocity (Angelaki and Hess 1996; Barmack 1981; Darlot et al. 1985; Dickman et al. 2000; Rude and Baker 1988). When rotational motion is experienced in the light, additional extravestibular visual cues provide optokinetic responses that enhance the VOR response to near unity gains to achieve good visual stabilization (Gioanni et al. 1981; Turke et al. 1996).
Head-free gaze responses
It is clear from this study that, when the head is free to move, gaze stabilization is accomplished through a robust combination of head and eye movements that occur synergistically in phase during rotational motion. We observed gaze responses that were of larger amplitude than the head-fixed VOR alone for all planes of motion in both pigeons and quails. In both avian species, the major component of gaze was actually the head movement response. In fact, it was striking to observe significantly lower eye movement during head-free motion compared with the head-fixed VOR.
Gaze dynamics were similar to those of the head-fixed VOR. Specifically, for all rotational planes of motion, the gaze responses were of lower amplitude during low frequency oscillations and increased as stimulus frequency increased. During EVA motion, the phase of the gaze responses at low frequencies were far advanced but declined to be in phase with head velocity for mid- and high-frequency motion. All of the motions delivered in this study were in complete darkness, thereby obviating any possible contribution from visually mediated stabilization components such as the OKN. In a previous investigation with head-free pigeons, Gioanni (1988b) observed a large amplitude vestibulocollic response during optokinetic stimulation. During EVA rotational motion in the light when visual cues were present, Gioanni (1988a) found that gaze responses were near unity and remained compensatory across the frequency spectrum. Similar to our findings, Gioanni (1988a) reported that, in the dark, gaze was composed of a large-amplitude head movement component that contributed to 80% of the stabilization response. However, there are distinct differences between Gioanni's previous observations and these findings. We observed a parallel increase of both gaze and head movement gains as stimulus frequency increased. However in Gioanni's study, gaze gains quickly plateaued near unity at 0.1 Hz, whereas the head involvement continued to increase and actually equaled the gaze gain at 1 Hz (Gioanni 1988a). At any given frequency, the phase lead of the head was always slightly greater than that of gaze (Gioanni 1988a), whereas our study did not show this to be the case. Methodological differences may account for the discrepancies between the two studies. First, in Gioanni's studies, amphetamines were administered and second, the bodies of the pigeons were not restrained but were suspended from the motion rotator so the wings and feet were free to move (Gioanni 1988a). In this study, the body and feet were wrapped together and placed in a holder, thus minimizing extravestibular inputs below the neck from proprioceptors.
Different behavioral strategies for gaze stabilization
When one compares the head and eye movement components contributing to gaze stabilization between pigeons and quails, differences in their behavioral adaptations are apparent. While both species have undercompensatory responses for VOR and near unity gains for head-free responses, contributions from the eye and head vary. Gaze in pigeons is primarily composed of head movements. In contrast, gaze stabilization in quails was composed of nearly equal eye and head components. Noting that these response differences exist, it is of interest to examine their possible underpinnings. With respect to anatomical structure, both pigeons and quails have large, flat-shaped eyes. These animals also each have a similar monocular optic axis (corresponding to the fovea centralis) oriented 66 and 60° away from the bill tip for pigeons and quails, respectively (Fig. 1) (Fitzgerald 1969; Martin 1993; Martin and Young 1983). However, the pigeon has two distinct foveal regions, the fovea centralis and area dorsalis, which are thought to be specialized for lateral and binocular viewing conditions, respectively (Martinoya et al. 1984). Pigeons are arboreal, can navigate through large territories, and nest in high lofts. In contrast, quails nest in terrestrial regions, engaging in only short distance flights. It is likely that these differences in environmental and lifestyle niches have produced different behaviors for gaze stabilization.
Work in other species, especially lower vertebrates, supports the conclusions of our study. Dieringer et al. (1983) examined eye and head contributions to gaze stability in frogs and turtles and determined that the head played a major role in stabilization (>80%), with the eyes only being used in a transient manner. In chameleons, which also happen to have a very large oculomotor range, undercompensatory gaze was observed during rotational motion, with the head once again contributing the major response component (Gioanni et al. 1993). Collewijn (1977) noted similar results in rabbits to those observed in our study, with VCR gains during head-free conditions to reach near unity in the dark, with a small eye movement component.
Unlike the majority of the nonmammalian tetrapods and avian species, mammals show a much greater reliance on the eyes for stabilization (nearly 80%), especially at higher frequencies (Meier and Dieringer 1993). It is thought that the inertial load presented by the heads of these mammals limits the dynamic range of the head-neck system, especially at higher frequencies (Peterson and Goldberg 1982). Modeling and experimental studies have shown that differences in head contributions between mammals and other vertebrates may be due to head inertia (Peterson and Goldberg 1982; Wilson and Jones 1979). For example, in unrestrained rats undergoing sinusoidal oscillations in the light, it was observed that the gaze response at 1 Hz was nearly entirely composed of an eye movement component, with little head movement response (Dieringer and Meier 1993). Other head-free rotational studies in mammals in the dark are limited. For primates, VCRs in the dark cannot be readily elicited (Fuller 1981; Wilson and Jones 1979).
For birds, the demands imposed by many complex behaviors ranging from flight to foraging involve maintaining visual constancy on targets of interest during motion, which is accomplished through vestibular-mediated gaze stabilization (Wallman and Letelier 1993; Wilson et al. 1995). These findings show that, in the dark, gaze responses during rotational motions consist of both eye and head movement components in birds, with differing contributions depending on behavioral adaptations. Due to different visual strategies in lateral-eyed animals, examination of the mechanisms contributing to gaze stabilization provides unique insight into the organization of vestibular-mediated responses.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: J. D. Dickman, Dept. of Anatomy and Neurobiology, Campus Box 8108, Washington Univ. School of Medicine, 660 S. Euclid, St. Louis, MO 63110 (E-mail: ddickman{at}wustl.edu)
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REFERENCES |
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