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transferencia ocular avesTRANSCRIPT
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Avian visual perception:
Interocular and intraocular transfer
and
head-bobbing behaviour in birds
A Dissertation submitted for
the Degree of Philosphiae doctoris (PhD) in Neuroscience
at the
International Graduate School of Neuroscience (IGSN)
of the
RUHR-UNIVERSITY BOCHUM
by
Laura Jimnez Ortega
October 2005
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Printed with permission of the International Graduate School of Neuroscience of the RUHR-UNIVERSITY BOCHUM First Referee: Prof. Dr. Nikolaus F. Troje Second Referee: Prof. Dr. Onur Gntrkn Third Referee: Prof. Dr. L. Huber (Wien) Date of the oral examination: 30-11-2005
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Table of contents
1. GENERAL INTRODUCTION....................................................................................1
1.2 Intraocular and interocular transfer in pigeons ............................................................................................... 2 1.2.1 Intraocular transfer of information ......................................................................................................... 3 1.2.2 Interocular transfer of information.......................................................................................................... 5 1.2.3 Interim summary ....................................................................................................................................... 9
1.3 Visual asymmetries in birds.............................................................................................................................. 10 1.3.1 Right eye/left hemisphere dominances ................................................................................................... 11 1.3.2 Left eye/right hemisphere dominances .................................................................................................. 12 1.3.3 Asymmetric interhemispheric transfer .................................................................................................. 14 1.3.4 Interim summary ..................................................................................................................................... 16
1.4 Head-bobbing in birds ...................................................................................................................................... 16 1.4.1 Biomechanical function ........................................................................................................................... 17 1.4.2 Image stabilization ................................................................................................................................... 18 1.4.3 Motion parallax........................................................................................................................................ 19 1.4.4 Head-bobbing birds ................................................................................................................................. 20 1.4.5 Interim summary ..................................................................................................................................... 22
1.5 Anatomical substrate ........................................................................................................................................ 22 1.5.1 The avian eye............................................................................................................................................ 22 1.5.2 Visual pathways in the avian brain ........................................................................................................ 26 1.5.3 Interim summary ..................................................................................................................................... 30
1.6 Goals of this work ............................................................................................................................................. 31
2. GENERAL METHODS ...........................................................................................32
2.1 Experimental arena .......................................................................................................................................... 32
2.2 Motion capture system ...................................................................................................................................... 33
2.3 Subjects ............................................................................................................................................................. 34
2.4 Training Procedure .......................................................................................................................................... 34
3. EXPERIMENT 1, 2 AND 3: INTRAOCULAR AND INTEROCULAR TRANSFER IN PIGEONS. ..................................................................................................................38
3.1 Experiment 1: Limits of intraocular transfer in pigeons I: frontal to lateral direction. ................................ 38 3.1.1 Methods .................................................................................................................................................... 39 3.1.2 Results....................................................................................................................................................... 41 3.1.3 Discussion ................................................................................................................................................. 46
3.2 Are pigeons capable of interocular transfer between the two yellow fields? .................................................. 49 3.2.1 Methods .................................................................................................................................................... 50
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3.2.2 Results....................................................................................................................................................... 51 3.2.3 Discussion ................................................................................................................................................. 53
3.3 Limits of intraocular transfer in pigeons II: lateral to frontal direction. ....................................................... 56 3.3.1 Methods .................................................................................................................................................... 56 3.3.2 Results....................................................................................................................................................... 57 3.3.3 Discussion ................................................................................................................................................. 59
3.4 Interim summary............................................................................................................................................. 62
4. EXPERIMENT 4: PATTERN RECOGNITION DURING HEAD-BOBBING: ARE PIGEONS CAPABLE OF PATTERN RECOGNITION DURING THE THRUST PHASE? .....................................................................................................................63
4.1 Methods............................................................................................................................................................. 63
4.2 Results ............................................................................................................................................................... 67 4.2.1 Percentage of correct responses.............................................................................................................. 67 4.2.2 Head-bobbing motion .............................................................................................................................. 69 4.3.3 Interim summary ..................................................................................................................................... 81
5. EXPERIMENT 5: WHY DO BIRDS BOB THEIR HEADS? ....................................82
5.1 Methods............................................................................................................................................................. 83 5.1.1 List of head-bobbing and non head-bobbing birds ............................................................................... 83 5.1.2 Taxonomic tree of head-bobbing and non head-bobbing birds ........................................................... 85 5.1.3 Analysis of behavioural and ecological factors under head-bobbing .................................................. 87
5.2 Results ............................................................................................................................................................... 89 5.2.1 Head-bobbing and non head-bobbing birds list .................................................................................... 89
5.3 Discussion ....................................................................................................................................................... 100 5.3.1 List of head-bobbing and non-bobbing birds: exceptions within a family........................................ 101 5.3.2 Rare or occasional head-bobbing behaviour ....................................................................................... 103 5.3.3 Are body-bobbing birds head-bobbing birds? .................................................................................... 106 5.3.4 Are other-head-movements functions similar to head-bobbing functions? ...................................... 106 5.3.5 Head-bobbing evolution ........................................................................................................................ 107 5.3.6 Ecological and behavioural factors under head-bobbing, body-bobbing and non-bobbing ........... 114 5.3.7 Interim Summary .................................................................................................................................. 115
6. GENERAL DISCUSSION .....................................................................................117
6.1 Intraocular and interocular transfer of information.................................................................................... 117 6.1.1 Intraocular transfer of information ..................................................................................................... 118 6.1.2 Interocular transfer of information...................................................................................................... 120
6.2 Pattern recognition during head-bobbing...................................................................................................... 122
6.3 Why do birds bob their heads? ....................................................................................................................... 124
6.4 Summary ......................................................................................................................................................... 126
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APPENDIX................................................................................................................128
A. Intraocular and interocular transfer ............................................................................................................ 128
B. Pattern recognition during head-bobbing ................................................................................................... 132
C. Why birds bob their heads?........................................................................................................................... 134
REFERENCES .........................................................................................................157
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ABSTRACT
Two aspects of the avian visual perception were investigated: inter- and intraocular transfer of
information in walking pigeons as well as head-bobbing behaviour in birds. The retina of the
pigeon has two areas of enhanced vision: the red field pointing into the frontal binocular field
and the yellow field projecting into the lateral monocular field. The entire retina projects to the
tectofugal pathway, whereas the monocular area projects to the thalamofugal pathway. The
first part of this study examines how information received in different retinal areas is
generalised in the pigeon brain. The pigeons task was to discriminate between two shapes by
pecking on one of the two keys located at one end of an experimental alley, while walking
between two feeders. In the first study intraocular transfer between the red and the yellow field
was tested, by moving the stimulus presentation from the frontal to the lateral visual field in
consecutive steps. When the stimuli were located at 45 in the experimental arena, we observed
a drastic decrease of performance that may be due to a switch between the tectofugal and the
thalamofugal pathway. Intraocular transfer of information was also tested from lateral to
frontal direction. The transfer of information was poor or inexistent. Interocular transfer of
information between the yellow fields of the eyes was also tested. A lack of interocular transfer
was found in eight out of nine birds. Pigeons showed more difficulties to learn the task in the
monocular right visual field than in the monocular left visual field.
It is widely accepted that head-bobbing (HB) may act as an optokinetic behaviour, stabilizing
the retinal image and allowing pattern recognition during the hold phase. Pattern discrimination
during HB was tested by presenting two shapes during the hold phase, the thrust phase, or
randomly. The pigeons discriminated the shapes during the entire HB cycle: no differences
between the phases were observed. Finally, a list of 322 species of head-bobbing and non-
bobbing birds is offered. The development of HB in evolution and its behavioural and
ecological characteristics were also investigated. Half of the birds of the world may be head-
bobbing birds; the rest may be equally divided between body-bobbing (hopping) and non-
bobbing birds. HB may have appeared for the first time in a common ancestor of all living
birds. However, evidence for suppressions and several independent evolutions of HB were
observed. Head-bobbing may be a mechanism developed early in evolution to solve visual
demands, like pattern recognition and to monitor predators, in birds with lateralised eyes.
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General Introduction
1
1. GENERAL INTRODUCTION
Birds are the most visually dependent class of vertebrates (Gntrkn, 2002), as they are
highly specialised in visual perception. They live in a wide variety of habitats from desert to
rain forest and feed on a wide range of food: seeds, insects, small mammals, carcass, etc. Some
birds suffer a strong predator pressure, while others are predators themselves. Birds may need
to afford different visual demands that lead to different visual specialisations. The flying ability
is probably one of the greatest challenges for the avian visual system. For these reasons avian
models have often been used to investigate different aspects of the visual system.
The optic nerves in birds are almost completely decussated (Weidner, Reperant, Miceli, Haby,
& Rio, 1985), furthermore the birds brain has a limited amount of interhemispheric
commissures (Bischof & Watanabe, 1997; Ehrlich & Saleh, 1982; Saleh & Ehrlich, 1984) and
a lack of corpus callosum. Due to these unique characteristics, cerebral asymmetries, using the
avian visual model, have been broadly investigated. These asymmetries represent an important
neural principle in many vertebrates brains, including humans (Rogers & Andrew, 2002).
There is much evidence indicating that interhemispheric interactions may be an important
component for understanding visual asymmetries (Gntrkn & Bohringer, 1987; Keysers,
Diekamp, & Gntrkn, 2000; Parsons & Rogers, 1993). In this context, the study of
interocular transfer and intraocular transfer of information in the avian brain may also
contribute to a better understanding of visual asymmetries in vertebrates.
Many studies about asymmetries have been done in chickens and pigeons (Gntrkn, 1997a).
As a result, we have a better understanding of the visual system of those animals (Zeigler &
Bischof, 1993), although there are still many unresolved questions. One open question is the
role of head-bobbing in visual perception. Pigeons and chickens are head-bobbing birds, that
is, they move the head backward and forward while walking and landing (Dagg, 1977b;
Dunlap & Mowrer, 1930).
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General Introduction
2
Head-bobbing is present in at least 40% of the birds, furthermore it has been demonstrated that
head-bobbing is controlled visually (Friedman, 1975b).The head-bobbing function is not yet
well understood, however the contribution of head-bobbing in visual perception is widely
accepted (Davies & Green, 1988; Friedman, 1975; Green, Davies, & Thorpe, 1992; Green,
Davies, & Thorpe, 1994; Troje & Frost, 1999, 2000).
Very often in inter- and intraocular transfer studies, the possible role of optic flow and head-
bobbing in visual perception was not considered. In most cases, the experimental conditions of
the studies prevent the birds to show head-bobbing (examples can be found in: Mallin &
Delius, 1983 ; Nye, 1973; Remy & Emmerton, 1991b; Roberts, Phelps, Macuda, Brodbeck, &
Russ, 1996). In addition, there are few experiments investigating interocular transfer between
the yellow visual fields. This is probably due to the difficulties in training pigeons to solve
visual tasks in the lateral visual field (Remy & Watanabe, 1993).
The main aim of this work is to combine these two aspects of the visuals system in birds: on
the one hand to contribute to a better understanding of information transfer and its
asymmetries, and on the other hand to investigate the functional significance of head-bobbing
in birds.
1.2 Intraocular and interocular transfer in pigeons
Pigeons and many other birds have lateralised eyes. The Pigeons eye is specialised to acute
near binocular vision at short distances during pecking and to panoramic vision at long
distances (Bloch & Martinoya, 1982a; Goodale, 1983). These two different visual functions are
mediated by two separate visual fields that project into two retinal areas: a binocular dorso-
temporal red field and a monocular yellow field. The red field is pointing into the lower visual
field, while the yellow field is pointing into the upper frontal and lateral visual fields.
In a natural situation a bird might perceive stimuli with both eyes, and also with different areas
of the retina. The main goal of inter- and intraocular transfer experiments is to clarify the way
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General Introduction
3
in which information retrieved from both eyes and different retinal areas is integrated in birds
brains (Remy & Watanabe, 1993).
1.2.1 Intraocular transfer of information
Intraocular transfer experiments in birds are infrequent and difficult to interpret (Remy &
Watanabe, 1993). Two main limiting factors are responsible for that: first it is difficult to
establish the retinal area in which the stimuli are presented in freely moving subjects; second
training birds in the lateral visual field has been proved to be an arduous task.
The first attempt to train birds in the lateral visual field was done by Nye (1973). He trained six
pigeons in 4 different tasks: rectangular bar detection task, rotating disk of bars detection
task, colour (red and green) and brightness (high and low) discrimination tasks. Birds learned
the task successfully when the stimuli were presented behind the pecking keys in the frontal
visual field. In contrast, when the stimuli were presented laterally in screens located 90 to each
side of the axis of the beak, the response of the birds dropped to chance level. Further attempts
to train the birds with stimuli presented in the lateral screens did not succeed. The pigeons
performed at chance level after weeks of training in the bar and rotating disk detection
tasks. For colour and brightness discrimination the author trained the pigeons initially in the
frontal visual field and moved the screens in 18 azimuth steps to the lateral sides. A
progressive drop of percentage of correct responses to chance level occurred when approaching
90. Nye concluded that pigeons do not possess the neural capability required to learn to use
information contained in laterally located stimuli to directly control pecking behaviour.
In a previous experiment, Levine (1952) found a drop in the discrimination performance when
the stimuli were shifted from a subrostral to an anterorostral position. He interpreted these data
as a lack of intraocular transfer in pigeons between two separate functionally independent
retinal areas.
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General Introduction
4
Mallin and Delius (1983) conducted an intraocular transfer experiment in head fixed pigeons.
The birds were trained to discriminate two coloured lights using jaw movements
(mandibulando) as an operant response. They found a weak transfer of light colour
discrimination from one locus to another within the visual field of the same eye. Interestingly,
they also found a poor intraocular discrimination transfer of coloured lights when the stimuli
were shifted from frontal to lateral position and vice versa. However, the transfer from lateral
to frontal position was slightly better (around 10%) than the reverse performance. These
observations were confirmed by Remy and Emmerton (1991b) in head-fixed pigeons, who
described the existence of information transfer from the lateral to frontal visual field and
observed a lack of information transfer from the frontal to the lateral visual field in a light
discrimination task.
Most recently, Roberts et al. (1996) trained eight unrestrained pigeons in an experimental
chamber to perform a symbolic delayed matching to sample task. The results confirm previous
findings obtained in head-fixed pigeons (Mallin & Delius, 1983; Remy & Emmerton, 1991b),
that is, there is intraocular transfer of information from the lateral to the frontal visual field, but
not vice versa. They also demonstrated that pigeons are capable of discriminating stimuli in the
lateral visual field, in contradiction to Nyes hypothesis (1973).
Two main suggestions have been proposed to explain intraocular transfer asymmetries. First,
Nye (1973) argued that pigeons were incapable of learning a discrimination task that requires a
pecking response when the stimuli are presented in the lateral visual field. However, it has
been demonstrated that pigeons are capable of stimulus discrimination in the lateral visual field
(Bloch & Martinoya, 1982b; Goodale & Graves, 1982; Mallin & Delius, 1983; Remy &
Emmerton, 1991b; Roberts et al., 1996). Second, it has been proposed that intraocular transfer
of information from the lateral to the frontal visual field may be an ecological advance. On the
one hand, birds should be able to switch from lateral to frontal vision when perceiving food
and approaching to peck (Friedman, 1975; Remy & Emmerton, 1991b; Roberts et al., 1996). In
addition, intraocular transfer from lateral to frontal visual field may be required to monitor the
environment for approaching predators while the frontal vision is occupied in feeding (Remy &
Emmerton, 1991b; Roberts et al., 1996). On the other hand, there is no need for information
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General Introduction
5
transfer from the frontal to the lateral field. Usually objects processed by the lateral visual field
are not seen in the frontal field first (Roberts et al., 1996). Field observations suggest that if an
object is processed by the lateral visual field, it is often shifted to the frontal visual field but
rarely vive versa.
1.2.2 Interocular transfer of information
Interocular transfer has been traditionally studied by covering one eye during the process of
learning a visual task. Once the bird reaches a certain criterion of performance, the naive eye
is tested in the same task (Goodale & Graves, 1982).
According to Levine (1945a), the earliest interocular transfer experiment was done in 1917 by
Khler. He observed that chickens showed interocular transfer in discriminating two sheets of
grey paper differing in brightness, which were located horizontally at ground level. In contrast
to Khlers findings, a lack of interocular transfer was found in pigeons trained monocularly in
a go/no-go colour discrimination task. In this experiment the stimuli were displayed on a
vertical screen above ground level (Beritov & Chichinadse, 1935).
Levine conducted a set of experiments using a jumping stand in which birds were placed in a
rotating perch that forced them to jump onto one of two platform according to different stimuli
(colours and shapes discrimination) (Levine, 1945a, 1945b, 1952). If the bird chose the
incorrect platform according to the presented stimuli, it collapsed and the animals dropped into
a net. If the correct platform was chosen, the birds were allowed to stay there for 15 seconds.
He observed that information transfer between the two eyes in pigeons depends on the location
of the stimuli in the visual field with reference to the position of the birds head. If the stimuli
were presented horizontally in a plane below the pigeons head (subrostral), interocular transfer
was present. In contrast, if the stimuli were presented vertically in front of the pigeons head
(anterostral) there was an absence of transfer (Levine, 1945a, 1945b, 1952). Two hypotheses
were proposed to explain these results: the sensorimotor integration hypothesis ( Watanabe,
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General Introduction
6
1986) and the retinal locus hypothesis (Goodale & Graves, 1982; Levine, 1945b; Mallin &
Delius, 1983).
The sensorimotor integration hypothesis proposes that pigeons may transfer information
depending on whether the response (manipulandum) and the stimuli (stimulandum) have
the same or different spatial locations. When manipulandum and stimulandum share the same
spatial locations, for example the stimulus is presented on the surface of the pecking key,
interocular transfer of information is expected. If they are located in different spatial location a
lack of interocular transfer is predicted (Remy & Watanabe, 1993).
To test the sensorimotor integration hypothesis, pigeons were trained in three conditional
spatial tasks employing two pecking keys arranged either vertically or horizontally (Watanabe,
1986). No matter whether the keys were arranged horizontally or vertically, if manipulandum
(response of the pigeon) and stimulandum were located in the same pecking key, there was a
perfect interocular transfer of information. However, if manipulandum and stimulandum were
located in different keys (for example: the stimulus was presented in the lower key and the
pigeons had to peck in the upper key) the pigeons were incapable of interocular transfer.
The retinal locus hypothesis proposes that interocular transfer occurs when the stimuli are
presented in the dorso-temporal part of the retina (red field), but not when the stimuli are
presented in the other parts of the retina (yellow field) (Goodale & Graves, 1982). The first
author supporting this hypothesis was Levine (1952). He proposed that in the pigeons eyes
there are at least two independent visual areas: a retinal locus corresponding to the subrostral
position in the visual field (below the head) and a retinal locus pointing into the anterostral
position (in front of the head) of the visual field. He argued that only the subrostral retinal
locus has the required neural connections which mediate interhemispheric transfer of
information. Furthermore, anterostral-subrostral transfer did not occur within a single eye.
Catania (1965) challenged this hypothesis by training pigeons to peck on a key located in front
of the pigeon head, in brightness, colour and pattern discrimination tasks. The stimuli were
projected either on the frontal key or on one of two lateral screens. Pigeons showed interocular
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General Introduction
7
transfer of information in both conditions. Catania offered two explanations for the lack of
interocular transfer in Levines experiments. Pigeons are laterally far-sighted and anteriorly
near sighted. In the jumping stand, the pigeons have to cock their head to one side in order to
observe the stimuli with the lateral visual field. The direction in which the head has to be
cocked depends on the covered-eye, and therefore this change of posture may affect interocular
transfer of information. Moreover, the amount of training may influence interocular transfer: In
Catanias studies the pigeons might have been over-trained in comparison to the pigeons in
Levines experiments (Catania, 1965).
A set of experiments replicating Levines jumping stand were designed to investigate Catanias
postural hypothesis (Goodale & Graves, 1982). Furthermore, the authors conducted several
key-pecking (FR1) discrimination tasks to test training amount and task difficulty as possible
factors in interocular transfer. They claimed that the lack of interocular transfer was a genuine
phenomenon which did not depend on postural habit, amount of training and task complexity.
Furthermore, birds trained binocularly in the jumping stand often showed evidence of learning
with only one eye when tested monocularly. They concluded that: the lack of interocular
transfer found in situations such as the jumping stand is a consequence of the discriminative
stimuli falling within the monocular field. Therefore, Goodale and Graves (1982) proposed
that interocular transfer occurs when the stimuli were projected into the red field, but not when
they were presented to the yellow field
Mallim and Delius (1983) conducted an experiment with head fixed pigeons using jaw
movements (mandibulando) as an operant in a colour discrimination task. They presented two
coloured lights in different locations of the retina. The advantage of this experimental design is
that the spatial localization of the stimuli is separated from the response and the presentation of
the stimuli in a certain retinal locus is controlled. Birds showed interocular transfer of
information when the discrimination task was monocularly presented inside the red field and a
lack of interocular transfer when the stimulus was presented within the yellow field. These
results support the retinal locus hypothesis, although Remy and Watanabe (1993) pointed out
that, in this task, pigeons did not need to direct their response spatially. Furthermore, the
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General Introduction
8
pigeons beak was oriented towards the position of the stimuli in the frontal position, whereas
during the lateral stimulation the beak is oriented in a different direction.
The retinal locus and sensorimotor integration hypotheses may not be contradictory.
Retinal locus may be crucial when a task does not require sensorimotor integration. However,
if a task requires sensorimotor integration, interocular transfer will not occur even when the
stimuli falls into the binocular field (Remy & Watanabe, 1993).
In addition, some experimental findings suggest that other characteristics of a task, such as
biological relevance, may influence interocular transfer. A lack of interocular transfer was
found in avoidance of the visual cliff (Zeier, 1970). Transfer of information was absent in heat
reinforcement but it was present in a similar task using food reinforcement (Gaston, 1984).
Interocular transfer was also observed in taste aversion in chicks (Bell & Gibbs, 1979; Gaston,
1984), as well as in cardiac conditioning in pigeons (Mihara & Watanabe, 1982) and in
conditioned withdrawal in pigeons, chickens and gulls (Stevens & Klopfer, 1977).
Furthermore, interocular transfer in pigeons colour discrimination but not in motor response
training has been found (Stevens & Kirsch, 1980). Pigeons eyes were occluded during initial
acquisition of the pecking response and subsequently during learning colour discrimination.
When the animals were tested with the occluded eye they were unable to respond. Once the
pigeons were trained to peck a blank response key, transfer of the colour discrimination task
was observed. This is an interesting result, because most of the pigeons discrimination
experiments involve training of the motor response under binocular condition prior to
monocular training on the experimental task. Additional studies of interocular transfer of the
motor response would be useful to explain this phenomenon (Remy & Watanabe, 1993).
In a recent publication, interhemispheric transfer of memories was tested in pigeons
(Nottelmann, Wohlschlager, & Gntrkn, 2002). Pigeons task was to peck on one of two
vertical keys according to a pattern displayed on both keys. Six pairs of patterns were used, for
half of these pairs the animals had to peck the upper pattern, for the other half the lower one.
Transfer of information from the left eye/right hemisphere to the right eye/left hemisphere, but
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General Introduction
9
not vice versa was observed. In this experiment, stimuli are presented within the red field and
sensorimotor integration occurs, however a lack of interocular transfer is found when the
stimuli are presented in the right hemisphere. Therefore, asymmetries in bird brain should be
considered as an important factor for interocular transfer. Most probably, asymmetries and
interocular transfer of information are interrelated phenomena in birds. In fact, Skiba et al
(2000) found asymmetries in interocular transfer of information. A faster shift of learned
colour cues from the dominant right to the left eye than vice versa was reported.
Finally, it should be noted that none of the hypotheses is capable of explaining all experimental
results in interocular transfer. The retinal locus hypothesis together with the current
knowledge of the anatomic aspects and asymmetries will lead to a better understanding of the
interocular transfer phenomenon.
1.2.3 Interim summary
The main goal of inter- and intraocular transfer experiments is to clarify the way in which
information retrieved from both eyes and different retinal areas is integrated in birds brains.
Interocular transfer experiments test the transfer of information between the two eyes (i.e.,
between the two hemispheres), whereas intraocular transfer experiments test the transfer of
information between different retinal areas of the same eye.
Birds have two distinctive retinal areas: a lateral monocular yellow field and a frontal binocular
field, often called the red field. Intraocular transfer has been investigated training the animals
to solve a visual task presented in one of these two visual fields and testing in the other.
Investigations in non walking pigeons have demonstrated that there is information transfer
from the lateral to the frontal visual field. However, a lack of transfer was found from the
frontal to the lateral visual field.
In birds, interocular transfer has been traditionally studied by covering one eye during the
process of learning a visual task. Once the animal reaches a certain criterion of performance,
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General Introduction
10
the naive eye is tested in the same task. Interocular transfer depends on the experimental
conditions and the task. Two main hypotheses have been proposed to explain the presence or
absence of interocular transfer: the sensorimotor integration hypothesis and the retinal
locus hypothesis.
The sensorimotor integration hypothesis proposes that pigeons may transfer information if
the response and the stimuli share the same spatial locations. In contrast, if they do not share
the same spatial location, a lack of interocular transfer will be observed. The retinal locus
hypothesis proposes that interocular transfer occurs when the stimuli are presented within the
red field, but not when the stimuli are presented in the yellow field.
1.3 Visual asymmetries in birds
Birds are highly visual animals, their visual capabilities are the most specialised among
vertebrates (Gntrkn, 2003). The optic nerves in birds are almost completely decussated
(Weidner et al., 1985). In addition, the amount of thalamic and mesencephalic commissures in
birds is very limited (Bischof & Watanabe, 1997; Ehrlich & Saleh, 1982; Saleh & Ehrlich,
1984). Consequently, hemispheric asymmetries can be easily investigated by directing the
visual information to one hemisphere by the simple mechanism of temporarily covering one
eye.
These characteristics make the avian visual system a very valuable model for the study of
visual asymmetries. Many studies in visual asymmetries have been done by using a variety of
birds species, like marsh tits (Clayton & Krebs, 1994a), domestic chicks (Andrew, 1988;
Andrew & Dharmaretnam, 1993; McKenzie, Andrew, & Jones, 1998; Rogers & Andrew,
2002, Parsons, 1993 #3354), zebra finches (Alonso, 1998; Voss & Bischof, 2003), European
starlings (Hart, Partridge, & Cuthill, 2000), quails (Valenti, Sovrano, Zucca, & Vallortigara,
2003) and pigeons (Gntrkn & Bohringer, 1987; Gntrkn et al., 2000; Gntrkn &
Hahmann, 1994; Prior & Gntrkn, 2001; Prior et al., 2004; Skiba et al., 2000).
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General Introduction
11
1.3.1 Right eye/left hemisphere dominances
Monocular occlusion studies revealed a right eye/left hemisphere dominance in discriminating
two-dimensional artificial patterns in pigeons (Gntrkn, 1985) and three dimensional natural
objects by means of a grain-grit task in pigeons (Gntrkn & Kesch, 1987), zebra finches
(Alonso, 1998) and chickens in a pebble-floor task (Mench & Andrew, 1986). Right eye
system dominance is also found in pattern discrimination (Gntrkn, 1997a). A higher degree
of illusion is observed for the right eye, when the birds were stimulated with geometrical optic
illusions (Gntrkn, 2003).
Some complex studies in pigeons have shown that memories of visual engrams and pattern
information are stored unilaterally in the left hemisphere (Gntrkn, 1997a; Nottelmann et al.,
2002; von Fersen & Gntrkn, 1990). This asymmetry, in memorizing visual stimuli, most
probably results in a right eye/left hemisphere advantage in homing (Ulrich et al., 1999),
although when pigeons are tested in circumstances in which they cannot rely on visual cues,
like landmarks, the left hemisphere advantage vanishes (Prior, Lingenauber, Nitschke, &
Gntrkn, 2002). A right eye dominance is also found in large-scale homing as a consequence
of a strong lateralisation of the avian magnetic compass and optic flow processing in favour of
the left hemisphere (Prior et al., 2004).
There is evidence for left hemisphere asymmetries in cognitive processes such as learning-to-
learn. In a colour discrimination reversal learning task birds learned faster with their right
eye/left hemisphere than with the left eye/right hemisphere (Diekamp, Prior, & Gntrkn,
1999)
Although, it has been demonstrated that the European starling shows an asymmetric
distribution of photoreceptors in the retina, the majority of the asymmetries described are
attributed to genuine central processes. They are not due to peripheral factors such as visual
acuity (Gntrkn & Hahmann, 1994), wavelength discrimination (Remy & Emmerton,
1991a), or depth resolution (Martinoya, Rivaud, & Bloch, 1983).
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General Introduction
12
Due to the amount of evidences in favour of the left hemisphere superiority, accumulated early
in the literature, it has been postulated as the dominant hemisphere. At the moment, it is
believed that none of the avian hemispheres dominates completely the visual analysis
(Gntrkn, 2003). In fact, there is also evidence for right hemisphere superiority in a variety
of tasks.
1.3.2 Left eye/right hemisphere dominances
Left eye/right hemisphere dominance has been observed in geometric or spatial information in
marsh tits (Clayton & Krebs, 1994b) and chicks (Tommasi & Vallortigara, 2001; Vallortigara,
2000). A right hemisphere dominance is also found for social recognition, like aggressive and
sexual responding, in chicks (Rogers & Andrew, 2002; Vallortigara, 1992). Wild living
Kookaburras (Dacelo gigas) search for food on the ground using preferably their left eye
(Rogers, 2002). In pigeons, a left eye/right hemisphere advance was found in choice reaction
times to a patter discrimination task (Di Stefano, Kusmic, & Musumeci, 1987). Most recently,
left eye/right hemisphere dominances was observed in the spatial distribution of attention
related to food detection for pigeons and chickens (Diekamp, Regolin, Gntrkn, &
Vallortigara, 2005).
The opposite left-right specialisation hypothesis for the lateral and frontal visual fields propose
that the left eye/right hemisphere may be dominant in the lateral visual field which is mainly
focused at long distances, whereas the right eye/left hemisphere may be dominant in binocular
vision which is specialised on short distance visual processes (Evans & Evans, 1999; Evans,
Evans, & Marier, 1993; Rogers, 2000; Vallortigara, Cozzutti, Tommasi, & Rogers, 2001).
In fact, in the majority of the experiments in visual asymmetries, the stimuli were shown in the
frontal binocular visual field, which is mainly analysed by the tectofugal pathway (Gntrkn
& Hahmann, 1999; Skiba et al., 2000). However, some evidences of lateral visual field
processing have arisen recently. Chickens fixated approaching predators by turning the head
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General Introduction
13
abruptly to one side preferably using the left eye (Evans et al., 1993) and showed shorter
reaction times using the left eye to detect a novel moving stimuli (a model raptor) (Rogers,
2000). In contrast, hens responded to a food call by fixating downward with the frontal visual
field. This pattern was not observed when alarm calls and contact calls were presented (Evans
& Evans, 1999). Furthermore, Social recognition experiments showed that chickens use either
the lateral field of its left eye, or the frontal field of the right eye, before pecking at a stranger,
but not at cagemates (Vallortigara et al., 2001).
Having a lateralised brain may allow dual attention to short distance tasks like feeding (using
the right eye/left hemisphere system) and long distance tasks like vigilance for predators (left
eye/right hemisphere system) (Rogers, 2000).
A recent study with pigeons found a left hemisphere dominance of the thalamofugal visual
pathway in a pattern discrimination task in an open arena (Budzynski & Bingman, 2004). The
thalamofugal pathway receives information from the lateral visual field, and therefore it is
assumed that it may be specialised in far field information processing. Therefore, the left
hemisphere dominance in the open arena may contradict the opposite left-right specialisation
hypothesis for the lateral and frontal visual fields in chicks. Moreover, the main asymmetry
was observed in the visual wulst, a structure that belongs to the thalamofugal pathway but also
contributes to the tectofugal pathway (Bagnoli, Grassi, & Magni, 1980; Engelage & Bischof,
1994; Folta, Diekamp, & Gntrkn, 2004; Miceli, Reperant, Villalobos, & Dionne, 1987).
However, it should be taken into consideration that the retinal projection of the stimuli was not
controlled.
Two more alternatives for explaining hemispheric specialisation have been discussed in the
literature. The right eye/ left hemisphere in chicks may be involved in the analysis of novelty
and in the spatial configuration of the environment (R.J. Andrew & Dharmaretnam, 1993).
This proposal is not in contradiction with the opposite left-right specialisation hypothesis for
the lateral and frontal visual fields, indeed a novel stimulus may be perceived first with the
lateral visual field.
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General Introduction
14
In addition, asymmetries in the birds visual system may increase the computational speed of
certain processes by concentrating them into one hemisphere. A good example is that visual
lateralisation improves grain-grit discrimination success in pigeons (Gntrkn et al., 2000).
Furthermore in a double task, like finding food and being vigilant for predators, not-lateralised
chicks perform worse than lateralised ones (Rogers, Zucca, & Vallortigara, 2004).
Consequently to the ecological advantages of being capable to attend to both predators and
feeding source, the computational advantages of processing information in one hemisphere
should be added. Most probably the asymmetric avian brain is a consequence of the interaction
between the ecological and computational advantages mediated by the anatomical substrate.
1.3.3 Asymmetric interhemispheric transfer
Various studies have investigated asymmetries of transfer between the two hemispheres. Such
investigations can give valuable cues to understand interhemispheric transfer, visual
asymmetries, and their interactions.
In chickens, a poorer interocular transfer of information from the left eye system to the right
eye system than in the opposite direction was described. A passive avoidance task was used, in
which birds learned to avoid a bead covered with a bitter substance. Binocular and right lesions
in the intermediate hyperstriatum ventrale (IMHV) resulted in amnesia (in monocularly trained
birds) when the chicks were tested with the left eye open. On the other hand, left IMHV lesions
did not impair performance regardless of the eye used (Sandi, Patterson, & Rose, 1993).
Furthermore, lesions in the left IMHV right after training induced amnesia in binocularly
trained birds, whereas bilateral ablations of IMHV lesions made one and six hours post-
training did not result in amnesia (Patterson, Gilbert, & Rose, 1990). Sandi et al (1993)
explained those results as a consequence of a relationship between lateralisation of IMHV
function and the visual asymmetries which occur at the behavioural and structural level. They
proposed a model in which the memory trace is not fixed into the left IMHV, but it is
transferred within one hour to the right IMHV.
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General Introduction
15
Another IMHV asymmetry has been found in chicks imprinted with an artificial object. Lesion
studies showed that within the first hours after imprinting there is information transfer from left
IMHV to the right IMHV which may be responsible for storing the visual characteristics of the
imprinted object (Horn, 1991; Nicol, Brown, & Horn, 1995).
An asymmetrical transfer of information has been found in marsh tits for memory storage.
Monocular occlusion was used to investigate lateralisation and memory transfer in a food
storing and in a one-trial associative learning task. In both cases it was found that both eyes are
involved in short-term storage, whereas only the right eye system is responsible for long-term
storage. The results indicated that memories are transferred from the right to the left eye
system between 3 and 24h after the memory formation. Seven hours after the memory
formation, the engram is no longer accessible to the left eye system but has not yet reached the
right eye system (Clayton, 1992; Clayton & Krebs, 1994).
In pigeons, it has been demonstrated that each hemisphere shifts colour information to the
contralateral side, but the efficiency of the transfer is time and side dependent. There is a faster
shift of learned colour cues from the right to the left eye than vice versa within the first 50
minutes after acquisition. For intervals longer than 3 hours, no differences have been found
(Skiba et al., 2000). The authors of this experiment concluded that inter-ocular transfer from
the right to the left eye should be facilitated due to a higher bilateral representation of the left-
sided tectofugal pathway.
The interhemispheric asymmetries in food storing, colour discrimination and passive avoidance
are not in the same directions. Those differences may arise by the diverse types of cognitive
processes required for each task (Skiba et al., 2000). For example, a storing food task demands
the utilization of spatial cues which are mainly processed in the right hemisphere, whereas
visual cues needed for a pattern discrimination task are processed mainly in the left
hemisphere. For giving a coherent explanation of interhemispheric asymmetry patterns, three
factors should be considered, functional asymmetries, time course, and physiological
characteristics.
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General Introduction
16
1.3.4 Interim summary
In birds, right eye/left hemisphere dominance is observed in pattern discrimination, stimulus
categorization and memory of visual stimuli. In contrast, left eye/right hemisphere superiority
has been found in processing geometric information, social recognition like aggressive and
sexual responding. It has been recently proposed that the right eye/left hemisphere may be
dominant for short distance tasks like feeding, whereas the left eye/right hemisphere may be
specialised in long distance tasks like vigilance. In addition having an asymmetric brain may
increase computational speed and allow dual attention to short and long distances.
Asymmetries in the information transfer between the two hemispheres have also been
described. In a passive avoidance task a poorer interocular transfer of information from the left
eye system to the right eye system than in the opposite direction was found. In Marsh tits,
memories are transferred from the right to the left eye system between 3 and 24h after the
memory formation. In pigeons, it has been demonstrated that there is a faster shift of learned
colour cues from the right to the left eye than vice versa, within the first 50 minutes after
acquisition.
1.4 Head-bobbing in birds
Pigeons, chickens, moorhens, partridges, storks, crows, ibises, and many other birds show a
characteristic head movement while walking (Dagg, 1977b; Davies & Green, 1988; Dunlap &
Mowrer, 1930; Friedman, 1975; Friedman, 1975; Frost, 1978). In pigeons, the head moves
backward and forward with respect to the body with a frequency that ranges from about 2 to 10
Hz (Troje & Frost, 2000). Head-bobbing is characterized by a hold phase and a thrust phase
(Fig. 2). During the hold phase the head of the bird remains stable in space (Frost, 1978; Troje
& Frost, 2000), whereas during the thrust phase the head is moved forward (Fig. 1 and Fig. 2).
In pigeons, heead-bobbing movement has been observed during walking, landing flight
(Davies & Green, 1991), prior to pecking (Goodale, 1983), and in other behaviours. Even a
stationary bird actively observing its environment, shows head-bobbing behaviour.
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General Introduction
17
Head-bobbing was first described in 1930 by Dunlap and Mowrer. Since then, three main
functions have been proposed, a biomechanical function and two visual functions: image
stabilization and depth perception through motion parallax.
Head movement of a walking moorhen
200
400
600
800
1000
1200
1400
0 0.2 0.4 0.6 0.8 1 1.2
Time (s)
Hor
izon
tal d
ispl
acem
ent (
pixe
ls)
1.4
Figure 1: Head position of a walking moorhen (Gallinula chloropus) in freedom. The head position in space was obtained by frame by frame analysis of walking moorhen video recordings. The horizontal coordinate of the head position, given by pixels, was plotted against the time.
1.4.1 Biomechanical function
In walking birds, head-bobbing is synchronized with the motion of the feet (Dagg, 1977a;
Dunlap & Mowrer, 1930). For this reason, the first attributed function to head-bobbing was a
biomechanical function (Dagg, 1977b). However, later it was shown that head-bobbing is
controlled visually and can be elicited independently of active locomotion (Friedman, 1975;
Friedman, 1975; Frost, 1978). Although this finding points clearly to a visual function, head-
bobbing may also have a biomechanical correlation. Body movements are synchronized with
head movements in various behaviours and the stride length of a walking bird is correlated
with the relative magnitude of head-bobbing (Fujita, 2004). Troje and Frost (1999) proposed a
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General Introduction
18
central pattern generator involved in coordinating complex motion patterns. Eye stabilization
may play a role in enhancing equilibrium during walking (Fujita, 2002).
1.4.2 Image stabilization
Some remarkable evidences supporting the visual function of head-bobbing were found in
Ring Doves (Friedman, 1975). A single bird was trained to walk inside a cylindrical cage; at
least two of the six experimental conditions demonstrated an unequivocal dissociation between
walking and head-bobbing. In one condition, the bird walked on a mobile false floor while the
cage and the visual surrounding were static. Head-bobbing was not observed in this case. In
another experimental condition, the bird remained static on the floor but the cage was moved
smoothly in a rostral-to-caudal direction, provoking optic flow. A clear head-bobbing
behaviour was observed in this situation. These findings were corroborated in pigeons: head-
bobbing was abolished when the animals walking on a treadmill matched the belt velocity,
confirming that head-bobbing is visually elicited (Frost, 1978).
Taking in account those results, it was suggested that the hold phase could be similar to other
optokinetic behaviours stabilizing the retinal image (Frost, 1978). During the hold phase the
head is not completely stabilized, but it slips slightly providing the necessary error signal that
drives the compensation mechanism to stabilize the head (Frost, 1978; Troje & Frost, 2000).
Stabilizing the retinal image allows object recognition and allows the visual system to
distinguish between self motion and outside world motion (Davies & Green, 1988; Frost, 1978;
Troje & Frost, 1999). Whooping cranes, during foraging, walk at speeds that permit them to
keep their heads immobilized with respect to the visual surroundings while covering large
search areas (Cronin, Kinloch, & Olsen, 2005). In spite of the fact that image stabilization is
widely accepted as a head-bobbing function, it has been found that in running and landing
pigeons the hold phase is replaced with a flexion phase which maintains alternation between
two different head velocities. However, in these cases the retraction of the head does not
compensate the fast forward movement of the body and the head is not stabilized (Green, 1998;
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General Introduction
19
Green et al., 1994). These observations suggest that head-bobbing may have several functions
depending on the situations and environmental demands.
1.4.3 Motion parallax
During the thrust phase, pigeons and other birds may use motion parallax computation to
derive distances. Pigeons and many other birds like ibises, storks, partridges, chickens,
woodcocks etc. have laterally placed eyes with very small binocular fields. Stereo vision as a
cue for depth perception can play a role only in a very restricted area. It is therefore assumed
that birds use motion parallax to monocularly derive depth information (Green et al., 1994).
Figure 2: Stroboscopic image from a walking pigeon that illustrates the typical head-bobbing which consists of a period in which the head remains fixed in space (hold phase) and a period in which it is quickly moved forward (thrust phase). From: (Frost, 1978).
S
W
K
&
t
d
f
M
d
everal animal species discriminate depth through motion parallax: locust (Collett, 1978;
allace, 1959), praying mantis (Kral, 1998, 2003; Poteser & Kral, 1995; Poteser, Pabst, &
ral, 1998), barn owl (van der Willigen, Frost, & Wagner, 2002) and gerbils (Goodale, Ellard,
Booth, 1990). Those animals perform head movements called peering in order to generate
he necessary optic flow for motion parallax computation. Bees are also capable of calculating
epth through motion parallax taking advantage of the ambient optic flow generated during
lying (Lehrer, Srinivasan, Zhang, & Horridge, 1988).
otion parallax computation is based on the fact that a translation of the eye induces a
isplacement of the retinal image of an object. The translation of the eye xh and the
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General Introduction
20
displacement of the retinal image of an object xr are related by the ratio of the focal length f of the eye and the distance d of the object (Fig. 3).
d fxhxr---------=
Figure 3: Motion parallax computation where d is the distance to the object, f is the focal length, xh is the translation of the eye, and xr is translation of the retinal image.
The displacement of the eye xh and the corresponding shift of the retinal image xr can well
be replaced by the respective velocities vh and vr:
d fvhvr-----=
Whereas f is an anatomical constant and vr can be derived directly from the visual input, the
velocity of the eye with respect to the visual surroundings vh has to be determined independently. In a walking bird this may be achieved by propioceptive and vestibular
information. In praying mantis the propioceptive cervical hair plate sensilla are involved in the
measurement of the distance to a jump target with the aid of motion parallax actively produced
by translatory head motion (Poteser et al., 1998).
1.4.4 Head-bobbing birds
Although head-bobbing behaviour has been very often discussed in the literature, there exists
no comprehensive list about which birds do and which ones do not. Frost (1978) reported that
irds, such as pigeons, doves, hens, head-bobbing occurs in at least 8 of the 27 orders of bstarlings, pheasants, coots, moorhens, rails, sand-pipers, phalaropes, parrots, magpies, and
quails. Dagg (1977) listed 28 head-bobbing and 21 non head-bobbing species during
locomotion. These lists are rather incomplete and some birds could be misclassified, but they
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General Introduction
21
suggest that at least 1/3 of the birds could show head-bobbing. Furthermore, the ecological
behavioural and phylogenetic information have been rarely considered in the study of head-
bobbing.
To our knowledge, apart from these reports there is a lack of information in the literature about
head-bobbing birds. Most of the articles focus on pigeons head-bobbing behaviour without
retrieving data about other species that could help to clarify its functional significance.
An unanswered question is why some birds bob their heads, whereas other birds walk without
bobbing their heads. Furthermore, it is not a clear answer why some species of birds walk with
or without displaying head-bobbing. Some birds like magpies can walk with head-bobbing, run
or hop. Head-bobbing during walking is used for low velocities, whereas running and out-of-
phase hopping are alternative gaits for higher speed in magpies. Furthermore, it is not known
why some birds use running and hopping as alternative gaits and why they prefer hopping over
running at high speeds (Verstappen, Aerts, & Van Damme, 2000).
Dagg (1977) reported that Mynah birds and starlings alternated between walking with head-
bobbing and hopping, depending on the speed of the motion. Birds that walk and bob their
heads tend to be of intermediate size. Small birds like most of the Passeriformes, living in
bushes and trees, with short legs tend to hop rather than walk (Friedman, 1975).
Hopping behaviour in birds may be comparable to head-bobbing and may play a similar role
(Davies & Green, 1988; Friedman, 1975). A frame by frame analysis of hopping sparrows
(Passer domesticus) while foraging reveals that birds head is thrust forward before the legs
start to push the body into the air. Likewise, the head stops and is stabilized in the visual space
before the body finished landing from the hop. This behaviour is also observed in alert
sparrows but not in somnolent ones (Friedman, 1975).
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General Introduction
22
1.4.5 Interim summary
Many birds show a characteristic forward and backward head movement while walking,
running, and during landing flight called head-bobbing. It is characterized by a hold phase and
a thrust phase. Typically, during the hold phase the head of the bird remains stable in space
while during the thrust phase the head is moved forward. Three main functions for head-
bobbing have been proposed: biomechanical function, image stabilization, and depth
perception through motion parallax. Although head-bobbing behaviour has been very often
discussed in the literature, most of the birds that bob their heads are not listed. Dagg (1977) and
Frost (1978) reported that head-bobbing occurs in at least 8 of the 27 orders of birds and in 28
species such as pigeons, doves, hens, starlings, pheasants, etc. It has been proposed that
hopping in birds could be comparable to head-bobbing. It is not known why head-bobbing
occurs in some species of birds but not in others. Further investigations are required to
investigate the functional and ecological significance of head-bobbing behaviour.
1.5 Anatomical substrate
The avian visual system is composed of two parallel visual pathways that process retinal
information from different parts of the retina: the thalamofugal and the tectofugal pathway. In
addition the accessory optic system is dedicated to the analysis of optic flow. A comprehensive
understanding of the three pathways is important for any attempt to understand the mechanisms
underlying visual asymmetries, inter- and intraocular transfer of information, and head
bobbing.
1.5.1 The avian eye
Birds have large eyes relative to their body size, suggesting that vision is an important sensory
modality in the class aves (Garamszegi, Moller, & Erritzoe, 2002; Martin, 1993). The small
tawny owl (450g) has eyes with a greater axial length than humans. The diameter of the ostrich
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General Introduction
23
eye is considered to be amongst the largest of all terrestrial vertebrates, with an axial length
close to 40 mm (Martin, 1993; Martin, Ashash, & Katzir, 2001). The resolution power of the
eye does not depend entirely on its size, other important factors like the structure and
concentration of rods and cones on the retina should be considered. Diverse evolutionary
demands, as diurnal or nocturnal activity, result into different kind of eyes that vary in the
absolute size, position, and amplitude of movement (Martin 1993).
Th avian retina like the mammals retina consist on by five layers: the outer nuclear and
pl
lay
an
sy
co
Th
bl
ox
lik
ce
ob
m
(6
an
eexiform layers, the inner nuclear and plexiform layers, and the ganglion cell layer. These
ers contain five kinds of cells: photoreceptors, bipolar cells, horizontal cells, amacrine cells
d ganglion cells (Fig. 4). The photoreceptors, bipolar cells, and horizontal cells make
naptic contact in the outer retinal layer. The bipolar, amacrine, and ganglion cells make
ntact in the inner retinal layer (Husband & Shimizu, 2001).
e avian retina shows some interesting differences compared to mammals. It contains no
ood vessels; the pecten, a highly vascular structure, is responsible for providing nutrients and
ygen to the cells. Furthermore, it contains double cones, more richer intraretinal connections
e horizontal and amacrine cells (Hayes, 1982; Mariani, 1982, 1987), and complex ganglion
ll response properties (Pearlman & Hughes, 1976). Four different types of cones have been
served in the avian retina, whereas only three types of cones have been described in the
ammalian retina. The spectral sensitivity ranges from ultraviolet (320nm) to the far red
50nm) (Remy & Emmerton, 1991a). The presence of oil-droplets covering the cones add
other layer of complexity to the spectral composition of the photoreceptors in the retina.
Figure 4: Avian retina. The photoreceptors, bipolar cells, and horizontal cells make synaptic contact in the outer retinal layer. The bipolar, amacrine, and ganglion cells make contact in the inner retinal layer. Figure from Husband and Shimizu (2001).
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General Introduction
24
The distribution of eye droplets in the retina defines two retinal areas (Fig. 5). The red field is
characterized by a high concentration of red and orange oil droplets and the yellow field with a
bigger concentration of yellow droplets.
P
RF
YFF
Figure 5: Schematic representation of the pigeons retina (modified from Galifret, 1968), where RF is the red field, YF is the yellow field, P is the pecten and F is the fovea centralis.
The red field located under the beak in the dorso-temporal retinal quadrant points into the
frontal visual field (Bloch & Martinoya, 1982b; Martin & Young, 1983; Martinoya, Rey, &
Bloch, 1981). Within the red field most birds also have an area of enhanced vision, the area
dorsalis which increases the acuity of the frontal binocular visual field (Martin & Katzir,
1999). This area is implicated in close sighting, feeding behaviour and the control of pecking
(Goodale, 1983).
The eyes of most birds are aligned laterally (Martin, 1993), which permits birds to receive and
process information of the lateral visual field through the yellow field. The lateral field also
contains an area of high ganglion cell density called the fovea centralis. This lateral visual
field serves far sighting, monitoring predators and conspecifics, as well as to detect food at
some distance (Fernndez-Juricic, Erichsen, & Kacelnik, 2004; Green et al., 1994). Hens tend
to view distant objects laterally while the preferentially observe objects less than 20-30 cm
away frontally (Dawkins, 2002).
Pigeons and some ground-foraging birds have a localized myopia in the temporal region. It can
be explained as an adaptation that permits pigeons to keep the ground in focus while foraging.
This localized myopia does not appear in the lateral visual field. In consequence, birds are
capable of maintaining in focus panoramic views and therefore monitor relevant information
like predators in the lateral visual field while foraging (Hodos & Erichsen, 1990).
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General Introduction
25
The cyclopean area is the coverage of the total visual field of an animal around the head, that
is, the summation of the frontal and lateral visual fields (Martin & Katzir, 1999). Species with
large eyes have developed sunshade structures (e.g. eyebrows or eye lash-type feathering) and
larger blind areas to minimize sunlight glare (Martin & Katzir, 2000). Large blind areas
correspond to smaller cyclopean field, which might be reasonable in large species with low
predatory risk. However, species with small eyes generally have smaller blind areas and larger
cyclopean fields, because they may need a wider visual field for predators detection and are
not so strongly affected by sunlight (Fernndez-Juricic et al., 2004).
Martin and colleagues classified avian visual fields into 3 basic types and an additional
category (combination of two basic classes) (Martin et al., 2001; Martin & Coetzee, 2004;
Martin & Katzir, 1993, 1994, 1995, 1999, 2000).
Type 1. Visual guidance to food items taken in the bill: the visual projection of the bill tip
falls in the centre of the binocular region. The visual field is defined by an extensive cyclopean
field, with a long vertical but narrow binocular field. For example, rock pigeon, starling and
cattle egret.
Type 2. Non-visual guidance to food items taken with the bill: the projection of the bill falls
in the periphery of the visual field. A big cyclopean field is also expected with a narrow
binocular field, for example, Eurasian woodcock, mallard and teal.
Type 3. Non-visual guidance to food items taken with the feet: the projection of the bill fall
outside of the visual field. The blind area is relatively large and the binocular field is wide but
vertically small, for example tawny owl.
Combination of Types 1 and 3: similar to Type 1 in which individuals visually follow and take
mobile prey; but prey is taken with the feet, for example short-toed eagle.
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General Introduction
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1.5.2 Visual pathways in the avian brain
Two main visual pathways process visual information in birds: The thalamofugal pathway and
the tectofugal pathway (Fig. 6). The thalamofugal pathway corresponds to the geniculocortical
pathway in mammals, whereas the tectofugal pathway corresponds to the extrageniculocortical
pathway in mammals. These visual pathways are structurally and functionally independent,
although several connections and modulations between them have been described. The
accessory optic system in birds is a third independent visual pathway dedicated to optic flow,
self motion signals, and optokinetic stimulation processing.
Figure 6: Schematic overview of the thalamofugal (green) and tectofugal pathways (red). Abbreviations: E, entopallium; GLd, nucleus geniculatus lateralis, pars dorsalis; OT, optic tectum; Rt, nucleus rotundus.
P
RF
YFF
P
RF
YF
F
TO
E
left right
TO
Rt
E
left right
Gld
Wulst
CT+CP
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General Introduction
27
1.5.2.1 Thalamofugal pathway
In pigeons, but not in chickens, the thalamofugal pathway receives visual input from the
yellow visual field (Gntrkn, Miceli, & Watanabe, 1993; Remy & Gntrkn, 1991), which
is transmitted to the contralateral thalamic nucleus geniculatus lateralis, pars dorsalis (GLd).
The GLd projects bilaterally to the visual wulst, a structure located in the telencephalon,
comparable to the striate cortex in mammals (Gntrkn, 2003; Jarvis et al., 2005).
In pigeons, the thalamofugal pathway mainly processes visual input from the lateral monocular
fields of the laterally placed eyes (Gntrkn & Hahmann, 1999; Remy & Gntrkn, 1991;
Vallortigara et al., 2001). However, in chicks, thalamofugal lesions affect frontal viewing in
chicks, suggesting that the thalamofugal system processes frontal visual field information in
chicks, but not in pigeons (Deng & Rogers, 2002).
In chicks, the thalamofugal system is asymmetrically structured by means of more contralateral
visual projections of the left nucleus geniculatus lateralis, pars dorsalis (GLd), to the right
hyperstriatum than vice versa (Deng & Rogers, 2002).
1.5.2.2 Tectofugal pathway
The tectofugal pathway processes visual information proceeding from the entire retina. The
visual input ascends from the retina to the contralateral optic tectum (OT), which projects
bilaterally to the entopallium (E) via the thalamic nucleus rotundus (Rt). The tectofugal
pathway is equivalent to the extrageniculocortical pathway in mammals: the optic tectum
corresponds to the superior colliculus, the nucleus rotundus to the lateral posterior-pulvinar,
and the entopallium to the extrastriate visual areas of the mammalian brain (Gntrkn, 2003;
Jarvis et al., 2005)
Morphological asymmetries have been found in the tectofugal system of the pigeon. In the
tectum and the Rt of pigeons, the soma size of visual cells is larger in the left hemisphere
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General Introduction
28
(Gntrkn, 1997b; Manns & Gntrkn, 1999). The bilateral projections from the tectal
lamina 13 to the Rt lead to representations of both the ipsi- and the contralateral eye in the
tectofugal system of each hemisphere (Gntrkn, 2003). These ipsi- to contralareral
tectorotundal projections are asymmetric (Fig. 6). On the one hand, the quantity of ipsilateral
tectorotundal projections is similar. On the other hand, the number of neurons projecting
contralaterally from the right tectum to the left Rt are approximately twice in number than vice
versa. Therefore, the Rt on the left side receives a massive ipsilateral tectal input and also a
large number of afferents from the contralateral tectum (Gntrkn, Hellmann, Melsbach, &
Prior, 1998). Thus, the pigeons tectofugal system displays significant morphological
asymmetries which might be related to the behavioural lateralisation of the animals. In fact, the
left Rt is involved in acuity discrimination with the right and the left eye, whereas the right Rt
has minor relevance in participating in binocular acuity (Gntrkn & Hahmann, 1999).
Furthermore, there is evidence of asymmetries in the tectal and posterior commissures
connecting the tecta of both hemispheres. Field evoked potential (in response to a stroboscope
flash to the contralateral eye) recorded in the left and right tectum showed that the left-to-right
tectotectal modulation was more pronounced than vice versa (Keysers et al., 2000).
1.5.2.3 Tectofugal-thalamofugal projections
The tectofugal and thalamofugal pathways are not isolated systems, but they are interconnected
by projections from the thalamofugal system onto the tectofugal system and vice versa (Fig. 6
and Fig. 7). The visual wulst sends ipsilateral descending projections directly to the optic
tectum (Bagnoli et al., 1980; Karten, Hodos, Nauta, & Revzin, 1973; Miceli et al., 1987). This
projection is probably very important for the understanding of the functioning of the avian
visual system (Gntrkn et al., 1993). Recently, by recording from single units of the left and
right Rt of the tectofugal pathway, a modulation of the left visual wulst on both right and left
tectofugal systems has been described, whereas the right visual wulst showed only an
ipsilateral influence (Folta et al., 2004, Folta et al. in preparation).
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General Introduction
29
P
RF
YFF
Tectum opticum
Lateral geniculate nucleus
Nucleus rotundus Entopallium
V. wulst
Figure 7: Schematic representation of the connections (in black) between the tectofugal (in red) and thalamofugal systems (in green).
Tectofugal-thalamofugal projections have been also described, radial neurons located in the
optic tectum project to the dorsolateral thalamus (Gamlin & Cohen, 1986; Wild, 1989).
Furthermore, the information processes by both ascending visual pathways converge into the
entopallium, thanks to projections from the visual wulst to the entopallium (Husband &
Shimizu, 1999; Karten & Hodos, 1970; Shimizu, Cox, & Karten, 1995; Watanabe, Ito, &
Ikushima, 1985). In zebra finches, the visual wulst has a significant facilitatory influence on
the processing of the contralateral visual information of the entopallium (Engelage & Bischof,
1994).
1.5.2.4 The accessory optic system
In addition to these two ascending visual pathways, the accessory optic system (AOS) is a
distinct visual pathway dedicated to the analysis of optic flow fields and various visual signals
generated by self-motion or optokinetic stimuli (Simpson, 1984). Given that head-bobbing is
triggered by optic flow (Friedman, 1975; Friedman, 1975b), it is widely accepted that the AOS
is involved in head-bobbing. Furthermore, AOS is considered to play a role in the stabilization
of the retinal image (Simpson, 1984; Westheimer & Blair, 1974), a function attributed to the
hold phase of head-bobbing.
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General Introduction
30
Numerous electrophysiological studies have shown that neurons in the AOS exhibit direction
selectivity in response to large visual stimuli moving in the contralateral visual field (Frost,
Wylie, & Wang, 1990). Some neurons have binocular receptive fields that encode optic flow
fields induced by self-translation or self-rotation (Frost et al., 1990; Wylie & Frost, 1990;
Wylie, Glover, & Aitchison, 1999; Wylie, Glover, & Lau, 1998). In birds, the AOS consists of
the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (nLM).
The nBOR receives input from the retinal displaced ganglion cells, the visual forebrain, the
contralateral nBOR and the ipsilateral nucleus lentiformis mesencephali (nLM), and projects to
diverse regions including the contralateral nBOR, the ipsilateral nLM, the vestibulocerebellum
and the oculomotor complex (Frost & Wylie, 2000; Wang, Gu, & Wang, 2000).
Neurons of the nBOR directly project onto the Rt of the same hemisphere (Diekamp,
Hellmann, Troje, Wang, & Gntrkn, 2001). Furthermore, projections from the nBOR onto
the GLd have been described (Wylie, Bischof, & Frost, 1998; Wylie, Linkenhoker, & Lau,
1997). The data suggest that the AOS is able to modulate both thalamofugal and tectofugal
ascending visual pathways. It is plausible that these projections are necessary to distinguish
self- and object-motion processed by the AOS and the ascending pathways, respectively
(Diekamp et al., 2001).
1.5.3 Interim summary
The retina of the pigeon has two areas of enhanced vision: the red field in the dorsotemporal
retina pointing into the frontal binocular field and the yellow field projecting into the lateral
monocular field. The entire retina projects to the contralateral optic tectum and continues via
the diencephalic nucleus rotundus to the entopallium (tectofugal pathway). The monocular area
also projects to the contralateral geniculate thalamic nucleus and continues to the wulst
(thalamofugal pathway). These two different visual systems possibly operate independently in
the pigeons eye, however they are not isolated. Both pathways converge into the entopallium,
the visual wulst sends ipsilateral descending projections directly to the optic tectum, and finally
radial neurons located in the optic tectum project to the dorsolateral thalamus.
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General Introduction
31
In addition to these two ascending visual pathways, the accessory optic system, consisting of
the nucleus of the basal optic root and the nucleus lentiformis mesencephali, is a distinct visual
pathway dedicated to the analysis of optic flow fields and various visual signals generated by
self-motion or optokinetic stimuli.
1.6 Goals of this work
The main aim of this work is to combine two aspects of the visual system in birds: on the one
hand to contribute to a better understanding of information transfer and its asymmetries, and on
the other hand to investigate the functional significance of head-bobbing in birds together with
its evolutionary basis.
The first part of this work investigates how information perceived in different parts of the
pigeons retinas, which is processes by two independent visual systems in each hemisphere, is
generalised in the pigeons brain. To achieve this aim, several experiments were designed. In
the first experiment and the third experiment, we tested intraocular transfer of information
between the red and the yellow fields in walking pigeons. In the second experiment, interocular
transfer of information between the yellow fields of both eyes was investigated.
It is believed that head-bobbing acts as an optokinetic behaviour allowing pattern recognition
during the hold phase. The aim of the fourth experiment was to clarify the role of the head-
bobbing hold and thrust phases in pattern recognition. Therefore, we conducted an
experimental task in which the pigeons needed to discriminate between two stimuli presented
either in the thrust phase, the hold phase, or randomly. To our knowledge, although head-
bobbing behaviour has been often discussed in the literature, few head-bobbing birds have
been listed until now. In the fifth experiment, a comprehensive list of head-bobbing and non
head-bobbing birds is offered. Furthermore, field observations, video recordings and
phylogenetic information, together with an analysis of behavioural and ecological characters,
were combined to clarify the adaptive value of head-bobbing and its evolutionary foundations.
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General Methods 32
2. GENERAL METHODS
Many experiments reported until now