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Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri
Submitted 8 February 2008; accepted in final form 4 July 2008
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ABSTRACT |
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INTRODUCTION |
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). Eye responses to angular acceleration are generated by signals from the semicircular canals and help to maintain visual image stability during rotations. These are collectively referred to as the angular vestibuloocular responses (aVOR) and have been studied in several animal classes including fish (Pastor et al. 1992), amphibians (Straka and Dieringer 2004), reptiles (Gioanni et al. 1993), birds (Dickman et al. 2000), and mammals (Angelaki and Hess 1996a,b; Baarsma and Collewijn 1975; Baloh et al. 1983; Barmack 1981; Bilotto et al. 1982; Brettler et al. 2000; Harrod and Baker 2003; Rude and Baker 1988; Viirre et al. 1986). Eye responses to linear acceleration are of two types. The translational vestibuloocular reflexes (tVORs) generally consist of disconjugate eye movements that function to maintain binocular foveal image stability during linear motion. The tVOR has been studied extensively in frontal-eyed animals such as primates, where it is known to depend on target viewing distance and eccentricity (Angelaki 1998; Angelaki et al. 2003; Merfeld et al. 2005; Paige and Tomko 1991; Telford et al. 1997). A second category of linear acceleration responses are the orienting responses, which compensate for actual or apparent head tilt relative to gravity (Angelaki and Hess 1996a; Cohen et al. 2001; Maruta et al. 2001, 2005). Although primates exhibit both tVOR and orienting responses to linear acceleration, lateral-eyed species exhibit mainly orienting responses (Baarsma and Collewijn 1975; Dickman and Angelaki 1999; Hess and Dieringer 1991).
Because natural motion generally includes a combination of angular and linear accelerations, it is important to understand how canal and otolith signals interact in the generation of compensatory eye responses. For example, natural activities, like walking, typically evoke a combination of aVOR and tVOR responses (squirrel monkey: Paige and Tomko 1991; Sargent and Paige 1991; Snyder and King 1992; Telford et al. 1996, 1998; rhesus monkey: Viirre et al. 1986; human: Crane et al. 1997; Seidman et al. 2002), as well as eye and head orienting responses that serve to maintain gaze orientation relative to gravity (Oommen and Stahl 2008). Another example of canal-otolith co-stimulation occurs when the head rotates around an earth-horizontal axis (EHA). Previous studies across species have shown that the eye response compensates more effectively during EHA rotation than during earth-vertical axis (EVA) rotation. This effect is most pronounced for low-frequency motion (pigeon: Dickman et al. 2000; mouse: Harrod and Baker 2003; rat: Brettler et al. 2000; rabbit: Barmack 1981; cat: Rude and Baker 1988; nonhuman primate: Angelaki and Hess 1996b; human: Bockisch et al. 2005; Groen et al. 1999; Schmid-Priscoveanu et al. 2000). The enhanced eye response during EHA rotation has been attributed to augmentation of the canal-driven aVOR by the additional presence of a dynamic otolith signal generated by reorientation of the head relative to gravity. However, otolith afferents respond to net linear acceleration, the result of gravitational and translational acceleration (Angelaki and Dickman 2000; Fernández and Goldberg 1976). Thus the aVOR enhancement could be driven by an otolith afferent-like net linear acceleration signal or by a central representation of gravitational acceleration (Green and Angelaki 2007; Merfeld et al. 1999). Previous studies have not discriminated between these two possibilities, so the nature of the aVOR-enhancing otolith signal remains unclear. The way in which this otolith signal is integrated with the canal signal to produce eye and head responses is also unknown.
In this study, we used combinations of tilt and translation to test whether the aVOR improvement during EHA rotation correlates best with gravitational or net linear acceleration. In addition, we compared eye and head orienting responses to linear acceleration when the animals were free to move their heads. Finally, we tested whether pigeon eye and head responses could be modeled as a linear combination of canal- and otolith-driven responses. We conclude that, whereas a linear model combining canal- and otolith-driven responses can account for pigeon eye movements, the interaction seems to be more complex for head movements.
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METHODS |
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Animal preparation
Each bird was surgically implanted with a head stud and a dual eye coil. General anesthesia was achieved using isoflurane gas (3–5% in O2) via endotracheal intubation. Heart rate was monitored, and core temperature was maintained using a heating pad. First, each bird was chronically implanted with a Delrin head stud. An incision was made along the midline of the skull, and the underlying periosteum was removed from the bone. The head stud was attached to the skull via titanium self-tapping screws and secured with dental acrylic mixed with ampicillin powder (5%). The head was positioned stereotaxically such that the upright orientation of the head stud corresponded to alignment between an earth-horizontal plane and the horizontal semicircular canals. After surgery, the head wound margin was kept clean with betadine washes and antibiotic ointment.
Following a 5- to 7-day recovery period, a dual eye coil was implanted in one eye. The coil assembly consisted of a large diameter (12 mm) direction coil and a small diameter (2 mm) torsion coil. The direction coil was constructed using three turns of multi-stranded, Teflon-coated, 41-gauge stainless steel wire (A-M Systems), and the torsion coil consisted of a 100-turn copper wire watchmaker coil (Imetra) attached perpendicularly to the direction coil. The three-dimensional (3D) coil assembly was coated in a thin layer of Araldite (Huntsman). For implantation, the animal was anesthetized using isoflurane gas (3–5% in O2) via endotracheal intubation. A circumferential incision was made in the conjunctiva to allow visualization of the sclera. In pigeons, the sclera is calcified near the cornea, so the 3D coil assembly was attached to the posterior margin of the scleral globe with 8-0 prolene sutures. Coil leads were threaded through the bone of the posterior orbit and passed underneath the skin to exit near the head stud. Next, the conjuctiva was approximated and closed with 8-0 vicryl sutures. Lead wires were soldered to a nanoconnector (Omnetics), which was secured next to the head stud with dental acrylic. To monitor head movements, a separate 3D coil assembly was attached either on or next to the head stud. Following surgery, butorphanol (10 mg/kg) was administered for postoperative pain, and ophthalmic antibiotic ointment (bacytracin/neomycin) was applied to the operated eye. Pigeons were allowed to fully recover (7–10 days) before being used in experiments.
Experimental protocols
A three-field AC magnetic coil system (CNC Engineering) was used to monitor rotational eye and head movements. The coil system provided a 5-in homogeneous magnetic field cube centered about the pigeon's head. The field coils were mounted to a servo-controlled rotator/sled system (Neurokinetics) driven by a PC and programmable interface (CED Model 1401plus, Cambridge Electronic Design). Stimulus control and data acquisition were performed using custom scripts written for the interface environment (Spike2, Cambridge Electronic Design). Stimulus deliveries were monitored using a rate sensor and a three-axis linear accelerometer mounted near the animal's head. For each experiment, the pigeon was placed in a padded body holder and secured in the motion system. Eye and head movement responses were obtained under both head-fixed and head-free conditions. All experiments were performed in total darkness. All motion profiles were delivered along axes that passed through the center of the head. A right-handed field coil-fixed coordinate system was used to describe eye and head movements and stimulus orientations. With the head fixed, the x-, y-, and z-axes corresponded to the pigeon's nasooccipital, interaural, and dorsoventral axes, respectively. Positive rotations were right-ear down, nose down, and leftward. Positive translations were forward, leftward, and upward.
To determine the effect of dynamic otolith stimulation on eye and head responses during rotational motion relative to gravity, the net linear acceleration experienced during EHA tilt was manipulated. The otolith organs act as inertial sensors and therefore detect inertial acceleration or deviation from free-fall on the Earth's surface. The effect of gravity is sensed by the otolith organs as an upward 1g linear acceleration (see Hixson et al. 1966). When additional sources of linear acceleration are applied (e.g., translational motion), the otolith organs will respond to the net linear acceleration, according to the equivalence principle (Einstein 1907). For a given stimulus condition, we can represent the individual sources of linear acceleration as acceleration vectors relative to the head, and the resultant vector corresponds to the net linear acceleration detected by the otolith organs (Fig. 1). Across stimuli, the effect of gravity corresponds to a constant 1g linear acceleration along an EVA (green arrows). During steady-state sinusoidal rotation about an EHA (Fig. 1A, Tilt-only), the head rotates relative to gravity, creating a sinusoidal modulation in the head-horizontal component of gravitational acceleration (red arrows) at the fundamental rotation frequency. An additional sinusoidal variation in the head-vertical component is also present; however, this component is relatively small and modulates at the second harmonic (see Angelaki et al. 1999). Therefore future references to net linear acceleration refer only to head-horizontal linear acceleration unless otherwise specified. Steady-state sinusoidal translational motion along an EHA (Fig. 1B, Translation-only) produces a sinusoidally varying earth-horizontal linear acceleration (cyan arrows; head-horizontal component indicated by blue arrows). During combined rotational and translational motion, the net linear acceleration sensed by the otolith organs depends on the spatial and temporal relationship between the sinusoidal variations in gravitational and translational components. For example, when backward translational acceleration is paired in time with nose-upward tilt (Fig. 1C, Tilt-Translation), gravitational and translational components of head-horizontal linear acceleration are in opposite directions and work to cancel each other. Thus the magnitude of net linear acceleration is decreased relative to that experienced during the Tilt-only condition. When backward translational acceleration is paired in time with nose-downward tilt (Fig. 1D, Tilt+Translation), gravitational and translational components of head-horizontal linear acceleration are in the same direction and add with each other, increasing the magnitude of net linear acceleration.
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In addition to the primary experimental paradigm, some animals were also tested with an extended tilt/translation protocol at 0.25 Hz only, where the relative phase of rotational and translational components was varied in 45° increments (relative phase = ±45, ±90, and ±135°). As a result, the peak net linear acceleration varied from 0 to 0.06g, and the phase of the modulation in net linear acceleration relative to tilt angular velocity varied from 0 to 180° (see Fig. 6). (Note that during Tilt-only, the net linear acceleration led tilt angular velocity by 90°.) These additional motion profiles varied the relationship between angular velocity and linear acceleration, providing the opportunity to test the ability of a simple linear canal-otolith integration model to predict eye and head movement responses.
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The recorded eye and head movement signals were first converted to rotation vectors in Cartesian coordinates (expressed relative to the field coil-fixed coordinate), using the first sample from each trial as the reference position. Note that the animal's nasooccipital axis was directed collinear to the positive x-axis and that the pigeon's primary visual axis was located 
66° away from the bill tip (Martin and Young 1983). The rotation vectors were desaccaded using custom scripts written in Matlab (MathWorks). The desaccaded rotation vectors were differentiated to produce rotation velocity vectors. From the rotation vectors, angular velocity vectors with components about the x-, y-, and z axes were calculated (Haustein 1989; Hess et al. 1992; van Opstal 1993). The eye rotation velocity vectors corresponded to the net movement of the eye in space. During head-fixed trials, no head movement relative to the motion system and field coils occurred, so only eye movements were obtained in response to the motion profile [head-fixed eye (VOR)]. During head-free trials, both eye and head movements combined to produce gaze responses, or eye-in-space. The eye movement component of gaze (eye-in-head) was computed by vectorially subtracting the head coil rotation velocity vectors from the eye coil rotation velocity vectors.
For each trial, the rate sensor and accelerometer signals, as well as the eye and head movement responses, were averaged over several cycles, and fit with sine curves at the fundamental frequency using a least-squares algorithm. The fitted curves were used to calculate gain and phase values for response components about the three cardinal stimulus axes. Only desaccaded (slow-phase) angular velocity responses were analyzed in this paper. Rotational gain values were expressed as eye/head/gaze angular velocity (°/s) per stimulus angular velocity (°/s), and phase values were expressed relative to peak positive angular velocity of the motion profile. Translational gain values were initially expressed as eye/head/gaze angular velocity (°/s) per net linear acceleration (g), and phase values were expressed relative to peak positive net linear acceleration. To facilitate comparison with responses to rotational stimulus measures, translation responses were also expressed relative to apparent tilt (defined as the rotation stimulus that would produce equivalent linear accelerations). Apparent tilt gains and phases were calculated using the following formulae
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a is the response phase (re peak linear acceleration). Here, tan–1(a) is equal to the peak amplitude of head rotational displacement (deg) that would produce an equivalent head-horizontal linear acceleration of peak amplitude a (g). For sinusoidal motion, multiplication by 2
f is used to convert peak displacement to peak velocity. Therefore the denominator in this equation represents the head tilt rotational velocity (°/s) that would produce an identical modulation in head-horizontal linear acceleration to that observed during a given translational stimulus. Gain and phase values throughout are expressed as mean ± SD. Gain values represent response peak slow-phase velocity (°/s) divided by stimulus peak rotational velocity (°/s) unless otherwise specified. All statistical analyses were performed using repeated measures or one-way ANOVA (Statistica, Statsoft).
Canal-otolith combination model
A simple linear combination model was proposed to predict eye and head responses during combinations of 0.25-Hz EHA tilt and translation motion profiles. For each animal tested (n = 3), the "canal-only" response for each response component (head-fixed eye, head-free eye/head/gaze) was defined as the mean response gain (GC) and phase (C) during 0.25-Hz Tilt-Translation stimuli (where only the canal afferents were activated). The "otolith-only" response was defined as the mean response gain (GO) and phase (O) during 0.25-Hz Translation-only stimuli. These responses were used to predict responses during Tilt-only, Tilt+Translation, and the extended paradigm: stimuli that dynamically activate both canal and otolith afferents. The tilt stimulus was identical across these stimuli, whereas the net linear acceleration varied in magnitude and in its temporal relationship to tilt velocity. Predicted response gain and phase values were computed in the following way. First, the canal-only component was expressed relative to tilt velocity and converted into its polar form (C)
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C were the canal-only response gain and phase contributions expressed relative to tilt velocity. Across the stimulus set used in our model analysis, the tilt component of the stimulus remained constant. Therefore the canal-only contribution to the total observed response also remained constant. The otolith-only component was also expressed relative to tilt velocity and converted to its polar form (O). However, since net linear acceleration varied across stimuli, the specific value of otolith-only gain and phase varied with the magnitude and relative timing of net linear acceleration for a given stimulus
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O were expressed relative to net linear acceleration, and GO' and O' were the otolith-only response gain and phase contribution expressed relative to tilt velocity when a = net linear acceleration, v = tilt velocity, and 
= phase of net linear acceleration relative to tilt velocity. Canal-only and otolith-only contributions were added in the polar domain and converted to predicted gain (Gpred) and phase (pred) values for each stimulus
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To evaluate the ability of the simple linear combination model to predict actual responses, we performed linear regressions relating predicted and actual responses (separately for gain and phase). Regressions were performed for individual animals' data, as well as across animals for each response component (head-fixed eye, head-free eye and head). The linear regression procedure was modified for two dependent samples to minimize the sum square perpendicular distance between data points and the best-fit linear relation. This procedure yielded asymmetric confidence intervals on the slope and intercept values. The strength of the linear relationship between actual and predicted values was evaluated by computing the correlation coefficients (R values) and associated P values. The slope of the linear regression was used to determine whether strong linear relationships were in fact one-to-one (indicating correspondence between actual and predicted values).
In the linear regression analyses, the model used to predict responses assumed unity weights for canal-only and otolith-only contributions to the total response. The best-fit weight for canal-only and otolith-only response contributions was determined by fitting responses to all stimulus conditions simultaneously with weights on each contribution as free parameters (performed separately for head-fixed eye and head-free eye/head/gaze). The fitting procedure was done using an algorithm that minimized the sum square error with the responses expressed in polar form (simultaneous minimization of gain and phase errors). Goodness-of-fit was evaluated by computing correlation coefficients (R values) and associated P values.
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RESULTS |
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Eye and head responses to steady-state sinusoidal motion stimuli in the dark were recorded from five alert pigeons using the search coil technique. Consistent with previous studies, we found that eye and head responses to EHA rotations were compensatory for tilt direction (Dickman et al. 2000; Haque and Dickman 2005). For example, as shown in Fig. 2, head-fixed rotations (Tilt-only) about the y-axis elicited spatially appropriate (Ey) slow-phase compensatory eye movements. Orthogonal eye and head movement components directed about the other two axes were negligible and were not analyzed further. Similar compensatory eye and head responses to EHA rotations were observed under head-free conditions, for all spatial directions tested.
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; Haque and Dickman 2005). As net linear acceleration increased from 0 (Tilt-Translation) to 0.12–0.2g (Tilt+Translation), the head-fixed eye response phase decreased, approaching an ideal compensatory value (i.e., –180°) for tilt velocity. The observed effect was independent of stimulus orientation (ANOVA: P = 0.11) but interacted with stimulus frequency (F(4,416) = 22.77, P < 0.001), being largest for the lowest frequency tested (0.25 Hz). When the head was free to move, results were similar for the eye-in-head response, as shown in Fig. 4. In fact, eye-in-head response phase decreased with increasing net acceleration magnitude (F(2,134) = 33.06, P < 0.001) across all three frequencies tested (P < 0.01 for all frequencies). In contrast, head-free eye response gain was unaffected by the magnitude of net linear acceleration (ANOVA: P = 0.29).
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Canal- and otolith-driven responses: tilt-translation and translation-only responses revisited
Our initial observations showed that eye and head response phase values were brought closer to ideal compensatory phase for tilt velocity by a dynamic net linear acceleration signal. How is this effect produced? One possibility is that independent otolith- and canal-driven responses are generated and combine linearly. If so, the otolith-driven response would by necessity be spatially appropriate to augment the canal-driven response during EHA rotations. Indeed, we observed such a response during Translation-only stimulation. For example, as shown in Fig. 5 A (right), fore-aft (x-axis) translations elicited small slow-phase eye movements that would be compensatory to an apparent rotation about the y-axis. Similarly, head-fixed interaural (y-axis) translations elicited small eye movements that would be compensatory to an apparent rotation about the x-axis. These responses would be spatially appropriate to contribute to the aVOR when linear accelerations are produced by EHA tilt rather than by translation. These findings are consistent with similar apparent tilt responses reported previously for pigeons (Dickman and Angelaki 1999) and other lateral-eyed species (Baarsma and Collewijn 1975; Hess and Dieringer 1991). Eye and head responses to translation were expressed relative to apparent tilt velocity, as shown in Fig. 5B (black symbols). Both eye and head response gains were quite small (<0.1; but similar to those observed in a previous study; Dickman and Angelaki 1999) and decreased significantly with increasing frequency (head-fixed eye: F(2,146) = 180.41, P < 0.001; head-free eye: F(2,122) = 100.84, P < 0.001; head-free head: F(2,122) = 41.73, P < 0.001). The phase values observed at the different frequencies were consistent, even with low gains being present. In fact, the phase variance across trials and between individual animals were much less variable than would be expected if produced by random noise, as would occur if the response gains were zero. Instead, the observed variability in eye and head response phases during Translation-only was on the order of the variability in response phase overall. The Translation-only eye response exhibited phase lags relative to ideal (i.e., –180°) that decreased significantly between 0.25 and 1 Hz (head-fixed: F(2,146) = 8.78, P < 0.001; head-free: F(2,122) = 7.20, P < 0.001) and were smaller overall during head-free stimulation. In contrast, the head response exhibited phase leads of 180° that decreased with increasing frequency (F(2,122) = 12.57, P < 0.001).
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180°. A linear combination of canal- and otolith-driven head responses would thereby produce a response phase that was farther from ideal than the canal-driven response alone, contradicting our previous results. From these observations, we predicted that a linear combination model would be able to account for the eye response but not the head response to EHA rotations. Evaluating a simple linear combination model of canal-otolith response integration
To study the utility of a linear combination model of eye and head responses for low-frequency (0.25 Hz) stimulation, different tilt/translation combinations were used to manipulate the magnitude of net head-horizontal linear acceleration and its phase relative to tilt velocity (see METHODS). First, the predicted eye and head responses were calculated as a linear combination of the previously observed canal-driven (Tilt-Translation) and otolith-driven (Translation-only) responses, using the mean gain and phase values for each animal (n = 3). Next, linear regressions relating predicted and actual gains and phases were performed, as shown for the head-fixed eye responses in Fig. 6. There was a strong linear relationship between actual and predicted gain (R = 0.74, P < 0.001) and phase (R = 0.89, P < 0.001) values for the head-fixed eye response across animals. Regression slopes for both gain (0.91) and phase (1.3) were near unity, indicating a significant relationship between model predictions and actual response values. Results from linear regression analyses for eye and head responses across animals are summarized in Fig. 7. As shown, the actual and predicted values of eye response gain and phase were strongly linearly related across animals, under both head-fixed (R 
0.74, P < 0.01) and head-free (R 0.76, P < 0.01) conditions. Moreover, the associated best-fit linear regression slopes were generally not significantly different from unity, as indicated by 95% CIs. In contrast, there was no significant correspondence between actual and predicted head responses for two of three animals tested (P > 0.35). In the third animal, head response gain and phase were linearly related to model predictions (gain: R = 0.91, P = 0.0018; phase: R = 0.90, P = 0.0026) with slopes not significantly different from unity. However, the overall relationship between actual and predicted head responses when all animals' data points were considered was not strongly linear (gain: R = 0.50, P = 0.012; phase: R = 0.20, P = 0.36). Therefore we concluded that the linear combination model did provide a good approximation of the eye response but not the head response during combined canal-otolith stimulation.
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DISCUSSION |
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; Barmack 1981; Bockisch et al. 2005; Brettler et al. 2000; Dickman et al. 2000; Groen et al. 1999; Haque and Dickman 2005; Rude and Baker 1988; Schmid-Priscoveanu et al. 2000), response improvement was only present at low rotational frequencies (0.25 Hz in this study). We further showed that these observations can be modeled as a linear combination of canal- and otolith-driven response components in the case of the eye but not the head. Otolith-driven response: net linear acceleration or its components?
We used tilt/translation combinations to manipulate the magnitude of net linear acceleration while gravitational acceleration remained constant. We showed that increasing net linear acceleration magnitude was sufficient to improve low-frequency (0.25 Hz) eye and head response phase. Others have documented low-frequency aVOR enhancement when both the semicircular canals and otolith organs were stimulated (Angelaki and Hess 1996b; Barmack 1981; Bockisch et al. 2005; Brettler et al. 2000; Dickman et al. 2000; Groen et al. 1999; Haque and Dickman 2005; Rude and Baker 1988; Schmid-Priscoveanu et al. 2000). However, these findings represent the first direct demonstration that net linear acceleration is the stimulus component producing the enhancement.
Previous studies have provided evidence that changes in the gravitational component of linear acceleration are not necessary to generate otolith-driven tilt responses. During pure translational motion, small aVOR-like tilt responses with low-pass dynamics have been observed in both lateral-eyed (Baarsma and Collewijn 1975; Dickman and Angelaki 1999; Hess and Dieringer 1991) and frontal-eyed (Angelaki 1998; Paige and Tomko 1991) animals. In fact, otolith afferents respond to net linear acceleration (Angelaki and Dickman 2000; Fernández and Goldberg 1976), and we might expect otolith-driven responses to be generated by an afferent-like signal. However, there is considerable evidence that nonhuman primates decompose the otolith afferent signal into its gravitational (tilt) and translational components. For example, primate mid-frequency tVOR eye responses during tilt/translation stimuli depend on the translational component rather than net linear acceleration (Angelaki et al. 1999). Even when net linear acceleration equals zero, an appropriate tVOR is produced by nonzero translational acceleration. In contrast, pigeons not only lack a functional tVOR (Dickman and Angelaki 1999), but instead generate eye and head responses that do not discriminate between gravitational and translational acceleration.
Canal-otolith interaction: species differences
Pigeons also lack several key oculomotor behaviors that are observed consistently in primates and are thought to be related to the specialized canal-otolith integration required to discriminate between gravitational and translational acceleration (Green and Angelaki 2003, 2004). For example, primates exhibit velocity storage, a theoretical construct purported to lengthen the eye velocity time constant to improve low-frequency aVOR responses (Büettner and Waespe 1981; Raphan et al. 1979). In contrast, pigeons not only lack velocity storage but exhibit velocity leakage: their aVOR time constant is actually shorter than that of their canal afferents (Anastasio and Correia 1994; Dickman and Correia 1989). In addition, primates produce steady-state per-rotatory eye nystagmus during constant velocity off-vertical axis rotation, when canal afferents are no longer dynamically active (Angelaki and Hess 1996b), whereas pigeons produce no steady-state nystagmus (Dickman and Angelaki 1999).
Interestingly, canal plugging in primates results in oculomotor behavior qualitatively similar to that observed in normal pigeons. Canal plugging abolishes eye response selectivity for translational acceleration, generating a tVOR that depends on net linear acceleration (Angelaki et al. 1999). Furthermore, while the otolith-driven tilt response during pure translation is small and restricted to low frequencies in normal monkeys, this response increases over time after canal plugging, in parallel with recovery of the low-frequency aVOR to EHA rotations (Angelaki et al. 2002). In fact, both velocity storage and steady-state per-rotatory nystagmus to constant velocity rotation diminish in parallel over time after canal plugging (Angelaki et al. 2000). These observations raise the possibility that pigeons and primates share a fundamental oculomotor substrate but that primates have additionally developed specialized canal-otolith processing that dominates behavior as long as both canal and otolith organs are intact (Green and Angelaki 2003).
Canal-otolith integration: linear or nonlinear?
What distinguishes normal primate oculomotor processing from that observed in pigeons and other lateral-eyed animals? We have concluded that canal- and otolith-driven response components combine linearly to generate the pigeon aVOR. Previous studies in other lateral-eyed species have examined whether a linear model could account for the aVOR, with mixed results. However, these previous studies either used inverted EHA rotation as their primary test case (Barmack 1981; Brettler et al. 2000) or used observations from canal-plugged animals to calculate the otolith-driven response (Angelaki and Hess 1996b; Barmack and Pettorossi 1988). In this study, we constructed multiple discriminative test stimuli in normal animals and were able to determine conclusively that a linear model was sufficient to account for enhancement of the pigeon aVOR during EHA rotation.
Linear processing cannot account for observed primate eye movements, however, where responses are driven by specific linear acceleration components. To decompose net linear acceleration into gravitational and translational components, canal and otolith signals must interact in a nonlinear fashion that also generates an inertial representation of angular velocity (Green and Angelaki 2004, 2007). Moreover, these two processes are inextricably linked. Decomposition of linear acceleration into its gravitational and translational components necessarily involves decomposition of angular acceleration into earth-vertical and earth-horizontal components, and vice versa. In fact, studies of so-called tilt dumping indicate that primates represent eye movements in an inertial reference frame (Angelaki and Hess 1994), further evidence of nonlinear canal-otolith integration in these animals.
Although this study provides evidence that head responses to complex stimuli are nonlinear, we cannot conclude that the nature of this nonlinearity matches that observed in primate oculomotor behavior. It is possible that this nonlinearity arises from convergent vestibular and extravestibular cues produced during head-free motion. Most prominently, the presence of neck proprioceptive inputs from relative head-to-body rotation might influence the head response in a nonlinear fashion. However, it seems likely that pigeons, like primates, are able to discriminate between gravitational and translational sources of otolith afferent activity somewhere in their central vestibular pathways. Previous studies have shown that pigeons must be able to maintain a space-stable head orientation during flight to right themselves in the air and navigate efficiently around airborne obstacles (Warrick et al. 2002). An internal representation of inertial angular velocity or position could serve to maintain space-stable head orientation during flight. Whether such an internal representation exists in pigeons has yet to be determined and presents a fertile line of inquiry for future study.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: J. D. Dickman, Dept. of Anatomy and Neurobiology, Box 8108, 660 S. Euclid, Washington University School of Medicine, St. Louis, MO 63110 (E-mail: ddickman{at}wustl.edu)
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