Download Possible cues driving context-specific adaptation of optocollic reflex

J Neurophysiol 107: 704 –717, 2012.
First published November 2, 2011; doi:10.1152/jn.00684.2011.
Possible cues driving context-specific adaptation of optocollic reflex
in pigeons (Columba livia)
Henri Gioanni and Pierre-Paul Vidal
Centre d’étude de la Sensorimotricité (CESeM), Université Paris Descartes, Sorbonne Paris Cité, UMR-CNRS 8194,
Paris, France
Submitted 21 July 2011; accepted in final form 30 October 2011
muscular proprioception; vibratory stimuli; vestibular stimulation;
flying posture; lumbosacral apparatus
REFLEXES, once believed to be “hard-wired,” turned out to be
extremely variable during the preparation, realization, and
aftermath of a given motor behavior. This variability may
correspond in some cases to mechanisms defined as contextspecific adaptation by Shelhamer and Clendaniel (2002). To
quote these authors, reflexive responses can be maintained with
different “calibrations” (such as gain and phase) for different
situations (contexts). Context cues are associated with each
adapted state, and the context cues themselves [rather than
error feedback, as is the case, for instance, for the adaptation of
the vestibuloocular reflex (VOR)] instantaneously invoke the
proper adapted state. Different types of contextual cues could
be at play: exteroceptive cues issued from the environment,
proprioceptive information generated by a given behavior, and
internal representation of the different phases of the motor
Address for reprint requests and other correspondence: H. Gioanni, Centre
des Saints-Pères, 45 rue des Saints-Pères, CESeM, 75270 Paris Cedex 06,
France (e-mail: [email protected]).
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behavior to achieve (efferent copies of motor commands).
Which cues are crucial and how they combine to evoke
context-specific adaptation is not fully understood. Gaze stabilization in birds is a nice model with which to tackle that
question.
When flying or walking, birds stabilize their gaze (head ⫹
eye position) by combining visual (optokinetic) and vestibular
reflexes that limit retinal slip and therefore avoid visual blurring (Dickman et al. 2000; Fite 1968; Fukuda 1959; Gioanni
1988a, 1988b; Mowrer 1936; Türke et al. 1996; Wallman et al.
1982). Optokinetic responses are triggered by retinal slip and
are more efficient (higher gain) during low-frequency or constant-velocity displacements, whereas the vestibular reflexes
are optimal during high-frequency head movements. In headrestrained pigeons submitted to visual rotatory stimuli, the
ocular response is sufficient to stabilize the image of the world
on the retina for stimulation up to 20°/s (Gioanni 1988a).
However, in the head-free condition, pigeons essentially use
their head, that is, the optocollic reflex (OCR), to stabilize their
gaze (Gioanni 1988a; Haque and Dickman 2005) in response to
retinal slip.
Importantly for the study of context-specific adaptation, the
OCR is heavily modulated by the behavioral context. In bodyrestrained pigeons, the beating field is irregular and the gain of
the OCR (slow-phase head velocity/stimulation velocity) decreases for stimulation velocities higher than 40°/s (Gioanni
1988a). When the animals’ body is less restrained with the use
of a harness, so that their wings, legs, and tail are free (“resting
condition”), the beating field is still irregular but the gain
remains close to 1 for stimulation velocity up to 60°/s (Gioanni
and Sansonnetti 1999). If the pigeons are additionally blown by
a frontal airflow that provokes a flying posture (“flying condition”), the beating field becomes very stable and a substantial
response is still present for stimuli up to 200°/s (Bilo and Bilo
1978, 1983; Bilo et al. 1985; Bilo 1992; Gioanni and Sansonnetti 1999). The context-specific adaptation of the OCR is not
limited to the flying posture: When pigeons are standing still on
the ground or are walking on a treadmill, the gain of the OCR
reaches values intermediate between those obtained in the
“resting” and “flying” conditions (Maurice et al. 2006). Correlatively, the velocity of the fast phases increases in correlation with the slow-phase velocity when the animals are walking
or flying (Gioanni and Sansonnetti 1999; Maurice et al. 2006).
Similarly, McArthur and Dickman (2011) have recently shown
that vestibular eye and gaze reflexes as well as tail responses of
pigeons are also enhanced in the flying condition. These
responses are mostly improved within the low-frequency/velocity range of stimuli. In summary, the improvements in these
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Gioanni H, Vidal PP. Possible cues driving context-specific adaptation of optocollic reflex in pigeons (Columba livia). J Neurophysiol 107: 704 –717, 2012. First published November 2, 2011;
doi:10.1152/jn.00684.2011.—Context-specific adaptation (Shelhamer
M, Clendaniel R. Neurosci Lett 332: 200 –204, 2002) explains that
reflexive responses can be maintained with different “calibrations” for
different situations (contexts). Which context cues are crucial and how
they combine to evoke context-specific adaptation is not fully understood. Gaze stabilization in birds is a nice model with which to tackle
that question. Previous data showed that when pigeons (Columba
livia) were hung in a harness and subjected to a frontal airstream
provoking a flying posture (“flying condition”), the working range of
the optokinetic head response [optocollic reflex (OCR)] extended
toward higher velocities compared with the “resting condition.” The
present study was aimed at identifying which context cues are instrumental in recalibrating the OCR. We investigated that question by
using vibrating stimuli delivered during the OCR provoked by rotating the visual surroundings at different velocities. The OCR gain
increase and the boost of the fast phase velocity observed during the
“flying condition” were mimicked by body vibration. On the other
hand, the newly emerged relationship between the fast-phase and
slow-phase velocities in the “flying condition” was mimicked by head
vibration. Spinal cord lesion at the lumbosacral level decreased the
effects of body vibration, whereas lesions of the lumbosacral apparatus had no effect. Our data suggest a major role of muscular proprioception in the context-specific adaptation of the stabilizing behavior,
while the vestibular system could contribute to the context-specific
adaptation of the orienting behavior. Participation of an efferent copy
of the motor command driving the flight cannot be excluded.
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
METHODS
Forty-five adult pigeons (Columba livia) were used. The birds’
weights ranged from 300 to 500 g. All pigeons were used in accordance with the guidelines established by the CNRS and Paris Descartes for the Care and Use of Animals in Research and those
approved by the Service Vétérinaire de la Ville de Paris. The protocols
used in this work were reviewed and approved by the “Direction
Départementale de la Protection des Populations de Paris” with the
protocol number B-75-103. Animals were housed and cared for in the
certified Laboratory Animal Facilities under veterinary supervision.
Experimental Procedure
The OCR was recorded in 20 animals in three conditions: the
“resting condition,” the “flying condition,” and during body vibration.
For the “resting condition” the animal was hung up in a supple harness
so that its head, wings, legs, and tail were free. In the “flying
condition” a frontal airflow of compressed air at a constant 1.6-bar
pressure was delivered through a 15-mm-diameter tube placed 15 cm
in front of the animal. The airflow principally reached the front of the
head, the breast, and the anterior part of the wings. In these conditions
pigeons adopted a flight posture: The legs were moved to the rear, the
tail was opened, and the wings were beating or remained spread
without beating. Whether or not the pigeons beat their wings did not
influence the characteristics of the OCR. The experimental procedure
corresponding to these two conditions has been used and described in
a previous study (Gioanni and Sansonetti 1999). For body vibration,
pigeons were placed in the “resting condition” and submitted to a
vibratory stimulation over 20 –30 s once the optokinetic stimulation
had begun. In a second group of 10 animals, the OCR was additionally
recorded during head vibration and during body ⫹ head vibration. For
the combined body and head vibration, the two different vibratory
stimuli were delivered simultaneously. All these vibratory stimuli
were delivered over 20 –30 s once the optokinetic stimulation had
begun.
Before starting the OCR recording sessions, the pigeon was placed
with its head centered inside a 1-m-diameter spherical screen. During
the recording sessions, gently tapping on the spherical screen maintained the animals in a high level of alertness. The order of the
behavioral conditions varied from one animal to the other.
Stimulations
Whole-field optokinetic stimulation was delivered by a light source
within an opaque metallic sphere (11 cm in diameter). The sphere was
pierced with numerous holes and located above the pigeon’s head.
The ball projected a pattern of spots of ⬃2–3° on the spherical screen.
The optokinetic ball was rotated in the horizontal plane by a DC motor
monitored by a velocity servosystem. Optokinetic stimuli consisted of
constant velocity steps of 30, 60, 100, 150, 200, 250, and 300°/s. The
optokinetic ball was set in motion in the dark. Stimulation began when
the light was turned on and terminated when the light was turned off.
Each stimulus was given in clockwise (cw) and counterclockwise
(ccw) directions. A new stimulation was delivered only when the
postresponses were finished.
The whole body vibration was carried out, at ⬃130 Hz, with a
homemade vibrator directly in contact with the holder so that it was
mainly applied to the body of the animal. The angular amplitude of
vibrations measured with a coil attached to the back of the pigeon was
0.25° in yaw and 0.1° in roll. Because the vibrator generated noise, we
verified that the auditory stimulation alone did not generate any
particular head movements.
The vibratory stimulation of the head was delivered, at ⬃110 Hz,
with another homemade vibrator of circular shape, 15 mm in diameter
and 4 mm thick, fixed on the top of the head by adhesive tape after the
feathers had been cut. The angular amplitude of head vibrations
measured with a coil cemented to the skull was 0.15° in yaw, 0.6° in
roll, and 0.45° in pitch. Although this stimulation may activate several
receptors (see DISCUSSION), it was first intended to activate the vestibular system.
Recording of Head Movements
Head movements were recorded by the magnetic search-coil technique (Robinson 1963) with an EPM 510 apparatus (Skalar, Delft,
The Netherlands). In the “resting” and “flying” conditions as well as
during the body vibration, an 8-mm-diameter coil was fixed in a rigid
cylindrical piece of plastic. This piece of plastic was then firmly
secured to the top of the head with double-sided adhesive tape. When
animals were submitted to head vibration, in order to provide a space
to fix the vibrator a coil of 18-mm diameter was glued (light paper
glue) on the skin around one eye. Before each experiment, the coil
was calibrated by rotating it in the horizontal plane by ⫾30°, 60°, and
90°. The head position signal and the control signals of the different
stimuli (velocity of the optokinetic stimulation, airflow duration, body
and head vibration) were stored on a computer with the PowerLab
system (AD Instruments, Paris, France). As the range of horizontal
head movements can exceed the linear range of the coil system
(⫾30°), an arcsin function was applied to the head position signal to
obtain a linear signal of the head position. The head position signal
was then differentiated to obtain a head velocity signal.
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gaze-stabilizing reflexes during flight are observed within the
velocity range for which the resting response has lower gains,
i.e., improvements for low-velocity stimuli for the vestibular
reflexes and improvements for high velocity for the OCR.
Several context cues could contribute to evoke contextspecific adaptation of the OCR (Maurice et al. 2006). Sensory
feedbacks could play a major role since they differ depending
on the ongoing behavior. Proprioceptive information generated
at muscular and/or articular levels are obvious candidates since
they could vary to form patterns of activity characteristics of
each motor behavior. In the flying (Bilo and Bilo 1983; Bilo et
al. 1985) and walking conditions the skeletal muscles display
various synchronized rhythmical activities, while they should
be tonically active at rest to control posture. In addition, the
pattern of vestibular information most probably varies according to the ongoing head movements during a given behavior.
An efferent copy of the motor commands could also modulate
the optokinetic responses in a predictive way depending on the
type of behavior programmed by the pigeon. Finally, birds
possess a specific lumbosacral apparatus, extensively studied
by Necker and colleagues, that contributes to body stabilization
(Necker 1997, 2005, 2006; Necker et al. 2000). It is constituted
of bony canals and mechanoreceptors located in the accessory
lobes of the ventral spinal cord (Rosenberg and Necker 2000,
2002). These cells respond very accurately to vibrations around
75–100 Hz (Necker 2002) and could therefore encode highfrequency movements of the body, which in turn could modulate the OCR dynamics.
Therefore, this study was aimed at investigating which
context cues could contribute to evoke context-specific adaptation of the OCR and how they combine. More specifically,
we have recorded the OCR in the alert head-free pigeon while
manipulating the vestibular, proprioceptive, and lumbosacral
information during five types of behavioral conditions: a “resting condition,” a “flying condition,” and during body and/or
head vibration.
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CONTEXT-SPECIFIC ADAPTATION OF THE OCR
Surgical Lesions of the Lumbosacral Apparatus
Data Analysis
All the parameters were analyzed with PowerLab dedicated software (AD Instruments). In the “resting condition,” the slow-phase
amplitude and velocity (SPV) of the OCR for a given velocity of the
visual surround were measured once it reached a plateau. As shown in
Fig. 1, when a behavioral condition was shifted to another condition,
the transition time to reach a steady-state response was within seconds. The analysis was systematically started once the steady-state
period was reached. The slow-phase amplitude and SPV were averaged over 20 s of stimulation.
Head vibrations could not be detected at the level of the head
position and velocity traces during the body vibration. On the other
Fig. 1. Optocollic responses (OCR) recorded
in the same pigeon for the different tested
conditions. Visual stimulation was a velocity
step of 100°/s delivered clockwise (not
shown). Top: head position. Bottom: head
velocity (fast phases are truncated). Positive
values indicate a head rotation in the clockwise direction. The OCR was first provoked
in the “resting condition” and then during
body vibration (A), during head vibration
(B), in the “flying condition” (C), and during
body⫹head vibration (D). Note the irregularity of the beating field in the “resting
condition” and the differences in amplitude
and frequency of nystagmic beats obtained
in the different conditions. Except for the
“resting condition,” the gain was close to 1
in all other conditions for this pigeon.
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A surgical approach to the region was performed in 15 animals,
allowing either a mechanical lesion of bony canals or a chemical or
electrolytic lesion of the accessory lobes.
Surgery was performed under general anesthesia (40 mg/kg ketamine hydrochloride im). After a local subcutaneous injection of
lidocaine (2%), feathers were removed and a midline incision of the
skin was achieved to expose the synsacrum. The outer lamella of the
bone was removed to uncover the bony canals between L2 and S2
segments. In five pigeons, canals were mechanically removed with a
fine drill. In three pigeons, a canal was opened on one side and a small
volume of 30% neomycin saline solution was injected through the
canal aperture to allow chemical lesion of the accessory lobes bilaterally. In seven pigeons, the electrolytic lesions of the accessory lobes
were achieved after the opening of several canals (2– 6) on the two
sides. A small electrode (silver ball tip) was introduced through the
ventral hole of the canal and placed on the surface of the lobe, whereas
a reference electrode was placed on the skin. A negative DC current
of 500 ␮A was then injected for 15–20 s. This high level of intensity
was necessary to obtain correct lesions and was probably due to a
partial diffusion of the current through the cerebrospinal fluid. Lesions
involved two or three accessory lobes. The destructed bone was then
replaced by low point fusion paraffin and the skin was sutured.
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
Histological Control
Animals with lesions (canals, accessory lobes, or spinal cord)
were anesthetized with an overdose of ketamine (80 mg/kg ketamine hydrochloride im) and then perfused intracardially with
saline, which was followed by fixative (4% paraformaldehyde).
The spinal cord was removed and postfixed at 4° centigrade overnight (4% paraformaldehyde in 0.1 M phosphate buffer solution,
pH 7.4). The tissue was then stored at 4° centigrade for a day in a
solution of 30% sucrose in 0.2 M phosphate buffer solution, pH
7.4. After inclusion in tissue freezing medium, cryostat sections of
50 ␮m were made and mounted on gelatin-coated glass slides.
Sections were stained according to the cresyl violet method. The
lumbosacral column was also removed to control the section or
opening of canals.
RESULTS
The optocollic responses (OCR) recorded during the five
different behavioral conditions (“resting condition,” “flying
condition,” body vibration, head vibration, and body ⫹ head
vibration) were analyzed by measuring the amplitude and the
frequency of the slow phases and by calculating the gain of the
OCR for each visual stimulation velocity tested (30 –300°/s) in
the cw and ccw directions (n ⫽ 40). The “resting condition”
was regarded as the reference condition in all measurements.
The influence of the different behavioral conditions on the head
beating field was evaluated by calculating the mean orientation
of the head and its variability during each type of stimulation
(see METHODS). Raw data of the OCR during different types of
stimulation are illustrated in Fig. 1.
Effects of Body Vibration Compared with “Resting” and
“Flying” Conditions
Amplitude and frequency of slow phases and gain analysis of
the OCR. The amplitude of the slow phases (Fig. 2A) was
larger in the “flying condition” than in the “resting condition”
(t ⫽ 3.48, P ⬍ 0.001, n ⫽ 40) only for high-velocity stimuli
(200 –300°/s), whereas their frequency (Figs. 1C and 2B) was
augmented over the whole velocity range (t ⫽ 23, P ⬍ 0.001,
n ⫽ 40). As a result, the OCR gain was increased by the “flying
condition” for all visual velocities tested (Fig. 2C). The body
vibration produced a large increase in amplitude (t ⫽ 9.80,
P ⬍ 0.001, n ⫽ 40; Figs. 1A and 2A) and a smaller increase in
frequency (t ⫽ 14.30, P ⬍ 0.001, n ⫽ 40; Figs. 1A and 2B) of
the slow phases over the whole velocity range of the optokinetic stimuli, that difference being larger in the higher-velocity
range (150 –300°/s). As a consequence, the OCR gain increased during body vibration (Fig. 2C) for stimulation velocities ranging from 100 to 300°/s (t ⫽ 12.88, P ⬍ 0.0001, n ⫽
40), to reach values statistically similar to that obtained during
the “flying condition.”
Fast phase analysis. We measured the amplitude and PV of
the fast phases to build the main sequence. The SPV occurring
just prior and after each fast phase was also measured, since
our previous studies (Gioanni and Sansonnetti 1999; Maurice
et al. 2006) revealed a correlation between the PV of fast
phases and the SPV in the “flying condition.” The relationship
between the amplitude of fast phases, their PV, and the accompanying SPV is illustrated as tridimensional plots using a
multiple linear regression analysis in Fig. 3A (n ⫽ 700). The
equation defining each plane of correlation as well as the
results given by the statistical analyses are indicated for each
condition. The equations are under the form PV ⫽ a·amplitude ⫹
b·SPV ⫹ c, where coefficient a reflects the “main sequence”
and coefficient b the relationship between the velocity of fast
phases (PV) and the SPV of the accompanying slow phases
(Fig. 3). Constant c corresponds to a theoretical PV value of
fast phases when both their amplitude and the SPV are null,
i.e., it can be envisioned as a boost to the fast phase generator
in some behavioral conditions.
To facilitate the comparison between data obtained in the
different behavioral conditions, the planes of correlation are
plotted two by two without data points in Fig. 3, B and C. As
predicted by the classical “main sequence,” the PV of fast
phases increased linearly with their amplitude in all conditions
(Fig. 3). The slope (coefficient a) varied from 6.61 deg.s⫺1/deg
during body vibration to 10.58 deg.s⫺1/deg for the “flying
condition.” These values correspond to mean durations of fast
phases of 151.3 ms and 94.5 ms, respectively. Compared with
the “resting condition,” the mean duration of the fast phases
was increased by the body vibration and decreased in the
“flying condition” (Table 1).
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hand, head vibrations were observable when the vibrator was
applied directly to the head. In that condition, in order to analyze
the head movements, the head position and the head velocity
signals were smoothed with a triangular window (method of Bartlett) of 3 points and 41 points, respectively, to filter out the head
vibration signal. Data obtained for cw and ccw stimulations in each
behavioral condition were pooled after a statistical analysis demonstrating a lack of difference between these two sets of data. The
OCR gain values (SPV/stimulation velocity) were calculated.
The fast phases of the OCR were quantified by measuring their
peak velocity (PV) and amplitude. These measurements were made
in five animals. About 10 fast phases were quantified for each
stimulation velocity (30, 60, 100, 150, 200, 250, and 300°/s) in the
cw and ccw directions. The velocity of the slow phases preceding
and following each fast phase was also measured in order to
investigate the relationship between fast- and slow-phase velocity.
The beating field of the head was quantified in the following
way: During a given stimulation, the deviation of the head relative
to the straight-ahead position was calculated at the midexcursion of
each recorded fast phase and averaged. This averaged value was
taken as an index of the mean orientation of the beating field, and
the standard deviation (SD) was used as an index of its variability.
Statistical analyses of data relative to the slow phase of the OCR or
to the beating field consisted of two-way analysis of variance
(ANOVA) with the amplitude, the frequency, the gain, the head
position, or the SD of the beating field as the dependent variable and
the behavioral condition and the stimulation velocity as the factors of
variation. Once the normality test (Shapiro-Wilk) and the equal
variance test were passed, a global analysis was performed to determine the sources of variation. A comparison between the behavioral
conditions was then done for each stimulation velocity (Holm-Sidak
method). The parameters t and P indicated below corresponded to the
comparison between the different behavioral conditions for the stimulation velocities showing a significant difference. All comparisons
were achieved with paired tests except when comparing the effects of
head vibration or body ⫹ head vibration with the other conditions,
where unpaired tests were used.
The amplitude and the PV of fast phases along with the neighboring SPV were plotted for each condition. The fit equation corresponding to a linear correlation of the three parameters was calculated, and
the corresponding plane was drawn on the plots. Parameters R and p
of the correlation and the parameter F (analysis of variance) were
calculated and indicated together with the plots on Figs. 3 and 8.
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CONTEXT-SPECIFIC ADAPTATION OF THE OCR
In the “flying condition” (Fig. 3B) the value of c was
augmented (c ⫽ 120°/s compared with 67.4°/s in the “resting
condition”). This difference means that the velocity of all the
fast phases (PV) was enhanced by a constant value compared
with the “resting condition.” Moreover, a linear increase in PV
took place as a function of SPV with a slope (b) of 2.3.
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Fig. 2. Mean amplitude (A), frequency (B), and gain (C) of slow phases of the
OCR evoked in the different conditions in response to increasing stimuli velocity
steps. Each point represents the mean ⫾ SE (n ⫽ 40 for the “resting” and “flying”
conditions and for body vibration, n ⫽ 20 for head and body⫹head vibration) of
responses recorded in the clockwise and counterclockwise directions.
As shown in Fig. 3C, the value of c was also augmented
(c ⫽ 289°/s) during body vibration compared with the “resting
condition” (c ⫽ 67.4°/s). This increase was even higher than
that obtained during the “flying condition” (c ⫽ 120°/s).
However, the PV of fast phases was practically not influenced
by the SPV (b ⫽ 0.6) during body vibration. The fact that the
main sequence had a lower slope during body vibration than at
rest (as mentioned above) explains that the two planes of
correlation are not parallel (Fig. 3C). Consequently, the difference in PV in these two conditions decreased when the amplitude of fast phases increased.
These data suggest that proprioceptive signals contributed
to the boost of the fast-phase velocity (c) observed during
the “flying condition” and the body vibration. However, the
increase in PV and its correlation with the SPV, observed in
the “flying condition” but not during body vibration, cannot
be solely attributed to these muscular proprioceptive
signals.
Beating field analysis. The mean eccentricity of the head
was calculated (n ⫽ 40) for each behavioral condition. A
mean negative value indicated an average head deviation
toward the apparent origin of the optic flow (the direction of
the fast phase): The pigeon is looking where it would go
with a free body. This will be called the “orienting direction.” A mean positive value indicated an average head
deviation in the direction of the optic flow (the direction of
the slow phase): The pigeon is looking where it would come
from with a free body. This will be called the “stabilizing
direction.”
As a rule, the head deviation (Fig. 4A) shifted progressively
from the “resting condition” toward more positive values (i.e.,
toward the “stabilizing direction”) during the body vibration
(t ⫽ 5.15, P ⬍ 0.001, n ⫽ 40) and then in the “flying
condition” (t ⫽ 7.90, P ⬍ 0.001, n ⫽ 40). There was also a
significant difference between data obtained for the body
vibration and the “flying condition” (t ⫽ 2.81, P ⬍ 0.05, n ⫽
40). The orientation of the beating field was also influenced by
the velocity of the optokinetic stimulation. The mean orientation of the head was toward the “orienting direction” for the
low velocities of stimulation (30 – 60°/s) and was progressively
displaced toward the “stabilizing direction” when the stimulation velocity was increased (150 –300°/s). As a result of this
double influence (velocity of the visual flow and experimental
conditions), the velocity of the optokinetic stimuli for which
the orientation of the head moved from an “orienting strategy”
to a “stabilizing strategy” varied from ⬃40 to 100°/s when the
experimental condition changed from the “flying condition” to
the “resting condition.”
The regularity of the beating field during optokinetic stimulations was evaluated by the standard deviation (SD) of the
mean head position (see METHODS). As shown in Fig. 1, A and
C, and Fig. 4B, the body vibration and the “flying condition”
provoked a significant reduction of the variability of the beating field (except for the 30°/s stimulus). The lowest values of
SD were obtained in the “flying condition” for optokinetic
stimuli delivered in the 100 –300°/s range.
Effects of lesion of the lumbosacral spinal cord. The injection of neomycin (30%) in the peripheral space of the lumbosacral spinal cord was initially intended to make selective
lesions of the accessory lobes. However, the histological controls showed that the accessory lobes were either partially
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
709
touched or spared while, in most cases, the dorsal part of the
lumbosacral spinal cord was destroyed on both sides (Fig. 5A).
The ventral part of the spinal cord and in particular the
motoneurons were only slightly or not affected, and consequently the pigeons were not paralyzed. Therefore, this lesion
turned out to be interesting to assess the role of the lumbosacral
proprioceptive afferences in the context-specific adaptation of
the OCR.
The OCR gain was calculated in the “resting condition,”
during the body vibration, and in the “flying condition,” before
and 15 days after neomycin injections in five pigeons. The
OCR gain was clearly decreased by the lesions for responses
obtained with stimuli at 100 –300°/s, with a maximal effect
during the body vibration (Fig. 6, A and B; t ⫽ 5.51, P ⬍ 0.001,
n ⫽ 10), a lower effect in the “resting condition” (Fig. 6, A and
B; t ⫽ 2.97, P ⬍ 0.05, n ⫽ 10), and a minimal effect, only
significant for stimuli of 250 –300°/s, in the “flying condition”
(Fig. 6, C and D;, t ⫽ 2.30, P ⬍ 0.05, n ⫽ 10). Since a substantial
“basal decrease” in the OCR gain was provoked by the lesions in
the “resting condition,” we compared the effects of the body
vibration and the effects of the “flying condition” in the intact and
lesioned pigeons. During body vibration, the increase of the OCR
gain was suppressed at 250 and 300°/s and less pronounced at
100 –200°/s (t ⫽ 4.16, P ⬍ 0.05, n ⫽ 10) in lesioned pigeons (Fig.
6B) compared with intact pigeons (Fig. 6A).
These data strongly suggest that the lumbosacral afferences
contribute to the OCR augmentation induced by body vibration. In contrast, in the “flying condition,” the OCR gain
modulation was similar in intact and lesioned pigeons (Fig. 6,
C and D). Therefore, the lumbosacral afferences are probably
not mandatory for the OCR augmentation induced by the
“flying condition.”
Possible role for the lumbosacral apparatus. As previously
shown (Necker 2006), the unilateral or bilateral mechanical
Table 1. Values of coefficient a (main sequence) and corresponding fast phase duration obtained in the different conditions
Coefficient a
Fast phase duration, ms
Body Vibration
Body ⫹ Head Vibration
Resting Condition
Head Vibration
Flying Condition
6.61
151.3
6.92
144.5
8.66
115.5
8.76
114.1
10.58
94.5
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Fig. 3. Three-dimensional representation of the peak velocity (PV)-amplitude relation as a function of the slow-phase velocity (SPV) for the fast phases of the
OCR. A: data points and corresponding plane of correlation for the “flying condition”. B: planes of correlation obtained for the “resting” and “flying” conditions.
C: planes of correlation obtained for the “resting condition” and during body vibration. The equations of multiple linear regressions and the corresponding
statistics are indicated for each condition (n ⫽ 700 fast phases in each condition).
710
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
Effects of Head Vibration and of Body ⫹ Head Vibration
destruction of the lumbosacral canals of five pigeons provoked
a postural instability in the light and an impossibility to stand
in the dark. However, the OCR gain was not modified by these
mechanical lesions, whatever the behavioral condition. Mechanical lesions interrupted the flow of cerebrospinal fluid in
the canals, but a direct activation of the mechanoreceptors by
vibrations could not be excluded. Thus the OCR gain was then
measured before and after electrolytic lesions of the accessory
lobes. Histological control confirmed the lesions (Fig. 5B).
Data obtained before and 8 days after bilateral lesions performed in three pigeons are shown in Fig. 7. The OCR gain
was similar before and after the lesions in the three conditions.
Therefore, the lumbosacral apparatus is most probably not
involved in the context-specific adaptation of the OCR.
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Fig. 4. Influence of the conditions and of visual stimulation velocity on the
mean orientation of the head (A) and the regularity of the beating field (B).
Each point represents the mean ⫾ SE (n ⫽ 40 for the “resting” and “flying”
conditions and for body vibration, n ⫽ 20 for head and body⫹head vibration).
A: the zero head position (dashed line) represents the straight forward orientation of the head. Head position values are positive when the head is deviated
in the slow phase direction and negative when the head is deviated in the fast
phase direction. The change from an “orienting” to a “stabilizing” strategy
depends both on the condition and on the visual stimulation velocity. B: the
regularity of the beating field is evaluated by its standard deviation (SD). The
beating field is more irregular in the “resting condition” than in all other
conditions.
Gain analysis of the OCR. The head vibration (n ⫽ 20) did
not increase significantly the amplitude of the slow phases
compared with rest (Fig. 2A) but increased their frequency over
the whole velocity range (t ⫽ 9.99, P ⬍ 0.001, n ⫽ 20 for head
vibration, n ⫽ 40 for resting condition; Figs. 1B and 2B).
Consequently, the OCR gain (Fig. 2C) was only slightly
increased during optokinetic stimuli delivered at 250 –300°/s
(t ⫽ 4.14, P ⬍ 0.001, n ⫽ 20 for head vibration, n ⫽ 40 for
resting condition). The difference in gain increase provoked by
the head vibration and by the body vibration was significant
(t ⫽ 7.36, P ⬍ 0.001, n ⫽ 20 for head vibration, n ⫽ 40 for
body vibration). Thus, while the body vibration induced a
substantial increase in gain of the OCR for the 150 –300°/s
velocity range, the head vibration had little effect.
The body ⫹ head vibration (n ⫽ 20) was used to test
whether data obtained in the “flying condition” could be
experimentally replicated by the simultaneous activation of the
muscular proprioceptors and the vestibular receptors. The amplitude (Fig. 2A) and the frequency (Fig. 2B) of the slow phase
showed intermediate values between those obtained in the
“resting” and “flying” conditions. Consequently, the resulting
values of the OCR gain obtained with combined body and head
vibration turned out to be not statistically different from those
obtained during body vibration alone or in the “flying condition” (Fig. 2C). That is, head vibration does not bring much
compared with body vibration alone.
Fast phase analysis. Compared with the “resting condition,”
the mean duration of the fast phases (n ⫽ 700) was equal during
head vibration and increased by body ⫹ head vibration (Table 1).
During the head vibration (Fig. 8A), the value of c was not
increased (contrary to that observed during body vibration) but
rather decreased (c ⫽ ⫺41.9°/s) compared with the “resting
condition” (c ⫽ 67.4°/s). On the other hand, the PV values
increased with the SPV with the same slope (b ⫽ 2.3) as in the
“flying condition.” Consequently, the planes of correlation corresponding to data obtained with the head vibration and during the
“flying condition” are almost parallel (Fig. 8B).
Therefore, data obtained in the “flying condition” could be
explained by a combination of the effects produced by the body
vibration (global increase in fast-phase velocity) and by the head
vibration (correlation between the SPV and fast-phase velocity).
To test further this hypothesis we compared the planes of correlation obtained in the “flying condition” with a “simulated plane”
calculated by averaging the coefficients a and c and by summing
the coefficients b obtained for the head vibration and for the body
vibration (Fig. 8D). The simulated plane was reminiscent of the
plane of correlation corresponding to the “flying condition,”
which suggests that data obtained in the “flying condition” could
be explained by a simple combination of the effects produced by
the body and head vibrations.
The characteristics of the fast phases triggered during the
body ⫹ head vibration (b ⫽ 1.6, c ⫽ 107.7°/s) appeared to be
closer to those observed with the body vibration than to those
observed in the “flying condition” (Fig. 8C). The plane of
correlation simulated by averaging each of the three coefficients (a, b, c) obtained for the body vibration and for the head
vibration was very close to the plane of correlation corresponding to the body ⫹ head vibration (Fig. 8E).
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
711
Fig. 5. Histological control of a pharmacological
lesion of the lumbosacral spinal cord (A) and an
electrolytic lesion of the accessory lobe on one side
(B); cresyl violet staining. A: the effect of a local
injection of neomycin (30%) is shown on one side of
the spinal cord at the S1 level. The dorsal and ventral
horns are delineated with a dashed line. The somas
are completely destructed in the dorsal horn. In this
example the accessory lobes were also destructed.
B: the segmental level corresponds to S2. The hole in
the tissue of the dorsal spinal cord indicates the right
side. The accessory lobe is intact on the right side
and is completely destructed on the left side (indicated by arrow). AL, accessory lobe; TL, transverse
ligament; LL, lateral ligament; DH, dorsal horn; VH,
ventral horn; GB, glycogen body.
DISCUSSION
We have already shown that the gain of the OCR and the
velocity of the fast phases increased progressively when the
behavioral context changed from the “resting condition” to
standing and then to walking, the maximal response being
obtained in the “flying condition” (Maurice et al. 2006). Which
context cues/and or efferent copies trigger these changes and
how do they combine to evoke CSA?
What Receptors Are Triggered During the Different
Conditions?
Body vibratory stimuli. Preliminary experiments showed
that vibratory stimuli directly applied in different parts of the
body were effective to enhance the optokinetic responses.
However, the vibrator was subsequently fixated on the holder
that maintained the harness sustaining the pigeon because this
procedure allowed more reproducible stimulations.
Muscle spindles were most probably recruited with that
protocol. First, vibrations are the stimulus of choice to activate
muscle spindles (Matthews 1972) contrary to Golgi tendon
Fig. 6. Mean gain of the OCR calculated in 5 animals,
before (prelesion) and 15 days after (postlesion) the
bilateral lesion of the dorsal part of the lumbosacral
spinal cord. Responses produced in the “resting condition” and during body vibration are compared when
obtained before (A) and after (B) the lesion (n ⫽ 10).
Similarly, responses produced in the “resting” and “flying” conditions are compared when obtained before (C)
and after (D) the lesion (n ⫽ 10). The increase in gain
produced by the body vibration was reduced by the
lesion, whereas the lesion did not modify the gain increase provoked by the “flying condition.”
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Beating field analysis. Compared with the “resting condition,” the head was deviated toward the “stabilizing direction”
(Fig. 4A) during head vibration (t ⫽ 2.38, P ⬍ 0.05, n ⫽ 20 for
head vibration, n ⫽ 40 for resting condition) and during
body ⫹ head vibration (t ⫽ 4.20, P ⬍ 0.001, n ⫽ 20 for body ⫹
head vibration, n ⫽ 40 for resting condition). There was no
statistical difference between data obtained with the body
vibration, the head vibration, and the body ⫹ head vibration.
The variability of the beating field (SD) was strongly reduced
compared with the “resting condition” (Fig. 4B). The SD
values obtained during head vibration and body ⫹ head vibration were comparable to those obtained during body vibration
and in the “flying condition.”
712
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
organs (Jami 1992). Second, recordings from the domestic
duck sciatic nerve (Dorward 1970a) and from pigeon neurons
of the Clarke’s column (Necker 1990) showed that properties
of muscle and tendon proprioceptors in birds are similar to
those in mammals.
Herbst corpuscles were also likely to be activated by vibrations. These mechanoreceptors, found only in birds, have a
morphological structure similar to that of the Pacinian corpuscles in mammals (Abraham 1978; Malinovsky and Pac 1980).
They are highly phasic and especially sensitive to vibrational
stimuli, their best frequencies (low threshold) ranging from
300 Hz to ⬃1,000 Hz. They are located in different parts of the
body but have been especially studied in the beak, the legs, and
the wings (duck’s bill: Gregory 1973; goose’s beak:
Gottschaldt 1974; Gottschaldt and Lausmann 1974; duck’s leg:
Dorward and McIntyre 1971; duck’s wing: Dorward 1970b;
pigeon’s wing: Necker 1990). The body vibration we used
probably excited Herbst corpuscles located in the wings, the
legs, and the body.
Thus both muscle proprioceptors and Herbst corpuscles
were most probably excited by the body vibration and could
participate in the context-specific adaptation of the OCR.
However, several observations suggest that the effects observed during body vibration were mainly produced by activation of muscular proprioceptors. First, we observed in a previous work that the gain of the OCR was enhanced in standing
pigeons, a situation without cutaneous stimulation, compared
with the “resting condition.” In contrast, when standing pigeons were frontally blown (even strongly), a situation that
most probably produced a strong peripheral stimulation, the
OCR gain was not modified (Maurice et al. 2006).
Head vibratory stimuli. A 500-Hz head stimulation can be
used to selectively activate otolith irregular neurons (Curthoys
2010; Curthoys and Vulovic 2011). It has been shown in
guinea pigs and in humans that such a 500-Hz bone-conducted
vibration delivered at the midline of the forehead causes
simultaneous and approximately equal-amplitude linear acceleration stimulation at both mastoids, and thus at the two
labyrinths (Chiarovano et al. 2011; Curthoys et al. 2006).
Therefore, it is likely that the 110-Hz stimuli we used activated
the two labyrinths: In pigeons, the distance between the skull
and the inner ear is shorter than in humans and roughly similar
to that in the guinea pig.
Which vestibular sensors were activated in that process
remains to be determined. It is generally admitted that the skull
vibratory test (SVT) given at 100 Hz and used as a clinical test
preferentially activates the semicircular canals, mostly the
horizontal canals, at least in primates (Dumas et al. 2008;
Young et al. 1977).
Finally, we cannot exclude that neck muscle proprioceptors
and Herbst corpuscles were activated together with the vestibular sensors, and therefore participated in the changes observed
in the properties of the OCR. It remains that vibratory stimuli
did not produce the same changes in the OCR when applied to
the head or to the body. Therefore, during head vibration the
vestibular system was probably a major contributor to the OCR
adaptation.
Head vibration caused modifications of the fast phase, but
the OCR gain remained unchanged. It cannot be excluded that
the retina vibration, which would decrease the efficacy of the
OCR, canceled a putative augmentation of the gain caused by
the vibratory stimuli. This would not be the case for the fast
phases during which the visual information is suppressed (Ross
et al. 2001).
Flying condition. All the receptors mentioned so far (muscular and vestibular proprioceptors, cutaneous mechanoreceptors) were most probably activated in the “flying condition” as
during a normal flight.
A rhythmical and roughly synchronized activity of several
muscles was present during the flying posture in pigeons, even
when the wings were not flapping (Bilo and Bilo 1983; Bilo et
al. 1985). This muscular activity should activate the proprioceptors, and the present study is consistent with that hypothesis: Our data showed that the increase in the OCR gain
observed in the “flying condition” was mimicked by body
vibration.
Hörster et al. (1983) proposed that the Herbst corpuscles
located in the wings perceive oscillations on the feathers that
could be generated by air currents or disturbances. Hence,
these mechanoreceptors are good candidates to trigger the
flight posture when the birds are subjected to a frontal
airflow. The airflow could also produce vibrations at head
level and activate the vestibular system. Our data showed
that the correlation between the fast-phase velocity and the
SPV in the “flying condition” was mimicked by the head
vibration but not by the body vibration. Thus, although
several cues may combine to shift the OCR gain from values
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Fig. 7. Mean gain of the OCR calculated in 3 pigeons before (prelesion) and 8 days after (postlesion) a bilateral lesion of 2 or 3 accessory lobes. Each point is
the mean ⫾ SE (n ⫽ 6). Pigeons were tested in the “resting condition” (A), during body vibration (B), and in the “flying condition” (C). The OCR gain was not
modified by the lesions.
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
713
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Fig. 8. Planes corresponding to the multiple linear regression analysis of the fast phases are plotted for the “resting condition” and during head vibration (A),
for the “flying condition” and during head vibration (B), and during body vibration and body⫹head vibration (C). The equations of multiple linear regressions
and the corresponding statistics are indicated for each condition (n ⫽ 700 fast phases). D: comparison of the plane of correlation obtained in the “flying condition”
with a simulated plane calculated by averaging the a and c coefficients and by summing the b coefficients of the equations obtained for the head vibration and
the body vibration. The equation of the simulated plane is indicated. E: comparison of the plane of correlation obtained during body⫹head vibration with a
simulated plane calculated by averaging each of the coefficients (a, b, c) obtained for the head vibration and for the body vibration. The equation of the simulated
plane is indicated. The “experimental plane” is close to the “simulated plane” in D and E.
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714
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
appropriate for the flight, our data suggest that muscular and
vestibular proprioception are mainly involved.
In addition to sensory signals, an efferent copy of the motor
command driving the flight could also play a major or a
complementary role in the OCR augmentation observed in the
“flying condition,” and a fortiori during a normal flight. Body
vibrations alone are sufficient to increase the OCR gain to
values obtained in the “flying condition,” which tend to confer
a role of proprioception during the flight. However, it cannot be
excluded that the efferent copy could totally or partially replace
the effect of the muscular proprioceptive signals during the
flight.
Context-Specific Adaptation of Fast Phases
Possible Anatomical Pathways Involved in Modulation of
Slow and Fast Phases
The avian optokinetic pathways, which generate both the
optokinetic nystagmus and the OCR, include the nucleus of the
basal optic roots (nBOR), the pretectal nucleus lentiformis
Results Obtained by Lesions Localized at the Lumbosacral
Level
Bilateral lesions of the dorsal spinal cord at the lumbosacral
level suggest that the lumbosacral proprioceptive afferences
contribute 1) to the maintenance of the OCR gain at rest and
2) to the increase in OCR gain induced by body vibration. In
contrast, these afferences did not appear to be mandatory
during the “flying condition.” Hence, it seems that while the
lumbosacral proprioceptive afferences are important to control
the OCR during life on the ground, during flying other peripheral afferences spared by the lesion, such as the afferences
from the wings and the upper part of the body, are likely to be
more important.
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The “main sequence” of fast eye movements including
saccades and fast phases of optokinetic nystagmus (OKN) and
optokinetic afternystagmus (OKAN) is modulated by the environmental conditions and by the behavioral task (see Jansen
et al. 2009; Kaminiarz et al. 2009a, 2009b). In the present study
changes in the “main sequence” occurred principally during
body vibration and in the “flying condition.” In the “flying
condition,” the mean duration of the fast phases was decreased
compared with all other conditions, which shorten their relative
duration for each nystagmic beat. For example, during a visual
stimulation at 100°/s the mean duration of a fast phase represents 15% of the mean duration of the slow phases in the
“resting condition” and 18% in the “flying condition.” However, if the mean duration of fast phases had the same value in
the “flying condition” as in the “resting condition,” it would
represent 22% of each nystagmic beat. This could be of
interest, since during the fast phases (or during saccades) the
gaze is not stabilized, the visual information is suppressed, and
the visual perception is subjected to spatiotemporal distortions
(see Burr and Morrone 2010; Ross et al. 2001). This mechanism could be especially adapted to the flight, since the
frequency of nystagmic beats, and therefore the time occupied
by fast phases, was maximal in the “flying condition.”
Body vibration increased the velocity of all the head fast
phases by the same amount, whereas the increase in velocity
produced by the head vibration was correlated to the SPV.
Interestingly, these two effects combined in the “flying condition,” and our simulation shows that a simple arithmetic
operation can account for this combination. However, when the
head and the body vibrations were delivered simultaneously,
the resulting fast-phase velocity was lower than in the “flying
condition.” Our simulation shows that during body ⫹ head
vibration the effects of the two stimuli are weighted rather than
added. This difference could be explained by the fact that
vibrations caused by the airflow and by the rhythmic activity of
many muscles in the “flying condition” (Bilo and Bilo 1983;
Bilo et al. 1985) are most probably cyclic at the difference of
our vibratory stimuli. Also, as previously discussed, an efferent
copy of the motor command present during the flight could
participate in the changes observed in the fast-phase properties.
mesencephali (LM), and the vestibulo-cerebellum (Britto et al.
1981; Frost et al. 1990; Fu et al. 1998a, 1998b; Gioanni et al.
1983a, 1983b, 1984; Masseck and Hoffmann 2009; McKenna
and Wallman 1981, 1985; Morgan and Frost 1981; Telford and
Frost 1989; Wang et al. 2000; Winterson and Brauth 1985;
Wylie and Frost 1990a, 1990b, 1999; Wylie et al. 1998; Zhang
et al. 1999).
On the input side, two structures could integrate the muscular proprioceptive, vestibular, and visual information to end up
with a context-specific adaptation of the OCR: the cerebellum
and the vestibular nuclei. Indeed, the cerebellum in birds
receives somatotopically organized spinal projections (Necker
2001; Okado et al. 1987; Vielvoye 1977; Yamamoto et al.
2001). In particular, terminals are found in lobule IX that
belongs to the vestibulo-cerebellum. This lobule receives also
direct and polysynaptic (via the inferior olive) projections from
the nBOR and the LM (Brauth 1977; Brecha et al. 1980; Clarke
1977; Pakan and Wylie 2006; Wylie et al. 1997, 2007). The
vestibular nuclei, in addition to vestibular signals, receive information coming directly from the cerebellum and from the nBOR
(Wylie et al. 1997).
It is generally hypothesized that the mechanisms by which
the context-specific adaptation originates result from shift between different “internal models” (Imamizu and Kawato 2008;
Lee and Schweighofer 2009; Wolpert et al. 1995). The cerebellum, the basal ganglia, and some cortical areas are often
cited as candidates for the elaboration of internal models, at
least in mammals. It has been shown that in pigeons the basal
ganglia modulated the gain of the OCR but that these changes
were not specifically related to the behavioral context (Gioanni
and Sansonetti 2000). The hyperstriatum of birds is not a
functional homolog of the mammalian cerebral cortex. Therefore, we are left with the cerebellum as the main structure in
birds that could be implicated in the context-specific adaptation
of gaze.
On the output side, Yang et al. (2008a, 2008b) have shown
that the LM and nBOR are also involved in the generation of
horizontal ocular saccades. These nuclei send also premotor
commands to structures that drive neck muscles (interstitial
nucleus of Cajal, mesencephalic reticular formation, nucleus
ruber), either directly (Brecha and Karten 1979; Brecha et al.
1980) or via the tectum (Brecha 1978; Gamlin and Cohen
1988; Wylie et al. 1997). Therefore the LM and the nBOR
could play a role also in the context-specific adaptation of the
fast phases of the OCR.
CONTEXT-SPECIFIC ADAPTATION OF THE OCR
715
The lumbosacral apparatus is very sensitive to vibratory
stimuli (Necker 2002), and its sensory cells project mono- and
polysynaptically to the neurons at the origin of the spinocerebellar tracts (Necker 1997). Therefore, it was a likely candidate
to participate in the context-specific adaptation of the OCR
during body vibration and in the “flying condition.” Our data
showed that it was unlikely.
the stabilizing behavior, while the vestibular system could
contribute to the context-specific adaptation of the orienting
behavior.
Context-Specific Adaptation of the Head Beating Field
DISCLOSURES
Concluding Remarks
This study was aimed at investigating which context cues
could contribute to evoke context-specific adaptation of the
OCR and how they combine. Our data suggest a major role of
muscular proprioception in the context-specific adaptation of
We gratefully thank Isabelle Vassias and Sylvie Lecolle for the histology.
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
Author contributions: H.G. and P.-P.V. conception and design of research;
H.G. and P.-P.V. performed experiments; H.G. and P.-P.V. analyzed data;
H.G. and P.-P.V. interpreted results of experiments; H.G. and P.-P.V. prepared
figures; H.G. and P.-P.V. drafted manuscript; H.G. and P.-P.V. edited and
revised manuscript; H.G. and P.-P.V. approved final version of manuscript.
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The amplitude of the nystagmic beats remained limited and
exhibited very low variability during the “flying condition.”
Variability decreased when the velocity of the visual flow (and
therefore the velocity of flight) increased. These two characteristics make sense from a functional point of view. Large and
irregular head movements could pose a problem in terms of
aerodynamics and maintenance of the direction of flight,
whereas the numerous small slow phases of the “flying condition” would confine the portion of space monitored by the
pigeon to a restricted zone in front of the animal. Conversely,
the variability of the beating field was much higher in the
“resting condition” than in all the other conditions. The “resting condition” is not a natural situation. However, the variability of the beating field in this condition was close to that
observed in pigeons standing on the ground (see Maurice et al.
2006, Fig. 3). Thus the high variability of the beating field in
the “resting condition” could correspond to an exploratory
behavior adapted to the search of food, whereas such a strategy
would probably be counterproductive during flight.
In the “flying condition” and during body vibration the OCR
gain was similar. However, in the “flying condition,” the slow
phases had smaller amplitude and higher frequency than during
body vibration. Thus it could be that the burst driving neurons
of the head, which trigger the fast phases (and remain to be
identified), behave differently in the two behavioral conditions
and therefore participate in the context-specific adaptation of
the OCR.
The orientation of the head in space was also modified when
the velocity of the visual flow increased or when the behavioral
condition was changed from “resting” to “flying”: The pigeon
shifted from an “orienting strategy” to a “stabilizing strategy.”
If we assume that the “resting condition” and low velocity
range of the visual flow correspond to life on the ground, the
“orienting strategy” is indeed adapted to the search for food.
On the contrary, during flight (high velocity range of visual
flow) stabilization of the head could be the main if the only
necessity, as suggested by the enhancement of visual and
vestibular gaze reflexes (Gioanni and Sansonetti 1999; McArthur and Dickman 2011) and by biomechanical studies of
bird flight (see Warrick et al. 2002). In the intermediate
situation encountered for velocities of the visual flow around
40 – 60°/s, the head remained roughly oriented straight forward. This situation could correspond to a flight performed at
low velocity, for example, when the animal is landing with a
curved trajectory.
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