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Many studies of cerebral asymmetries in different species lead, on the one hand, to a better understanding of the functions of each cerebral hemisphere and, on the other hand, to develop an evolutionary history of hemispheric laterality. Our animal model is particularly interesting because of its original evolutionary path, i.e. return to aquatic life after a terrestrial phase. The rare reports concerning visual laterality of marine mammals investigated mainly discrimination processes. As dolphins are migrant species they are confronted to a changing environment. Being able to categorize new versus familiar objects would allow dolphins a rapid adaptation to novel environments. Visual laterality could be a prerequisite to this adaptability. To date, no study, to our knowledge, has analyzed the environmental factors that could influence their visual laterality. We investigated visual laterality expressed spontaneously at the water surface by a group of five common bottlenose dolphins (Tursiops truncatus) in response to various stimuli. The stimuli presented ranged from very familiar objects (known and manipulated previously) to familiar objects (known but never manipulated) to unfamiliar objects (unknown, never seen previously). At the group level, dolphins used their left eye to observe very familiar objects and their right eye to observe unfamiliar objects. However, eyes are used indifferently to observe familiar objects with intermediate valence. Our results suggest different visual cerebral processes based either on the global shape of well-known objects or on local details of unknown objects. Moreover, the manipulation of an object appears necessary for these dolphins to construct a global representation of an object enabling its immediate categorization for subsequent use. Our experimental results pointed out some cognitive capacities of dolphins which might be crucial for their wild life given their fission-fusion social system and migratory behaviour.
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RESEARCH ARTICLE Open Access
Visual laterality in dolphins: importance of the
familiarity of stimuli
Catherine Blois-Heulin
1*
, Mélodie Crével
1
, Martin Böye
2
and Alban Lemasson
1
Abstract
Background: Many studies of cerebral asymmetries in different species lead, on the one hand, to a better
understanding of the functions of each cerebral hemisphere and, on the other hand, to develop an evolutionary
history of hemispheric laterality. Our animal model is particularly interesting because of its original evolutionary
path, i.e. return to aquatic life after a terrestrial phase. The rare reports concerning visual laterality of marine
mammals investigated mainly discrimination processes. As dolphins are migrant species they are confronted to a
changing environment. Being able to categorize new versus familiar objects would allow dolphins a rapid
adaptation to novel environments. Visual laterality could be a prerequisite to this adaptability. To date, no study, to
our knowledge, has analyzed the environmental factors that could influence their visual laterality.
Results: We investigated visual laterality expressed spontaneously at the water surface by a group of five common
bottlenose dolphins (Tursiops truncatus) in response to various stimuli. The stimuli presented ranged from very
familiar objects (known and manipulated previously) to familiar objects (known but never manipulated) to
unfamiliar objects (unknown, never seen previously). At the group level, dolphins used their left eye to observe
very familiar objects and their right eye to observe unfamiliar objects. However, eyes are used indifferently to
observe familiar objects with intermediate valence.
Conclusion: Our results suggest different visual cerebral processes based either on the global shape of well-known
objects or on local details of unknown objects. Moreover, the manipulation of an object appears necessary for
these dolphins to construct a global representation of an object enabling its immediate categorization for
subsequent use. Our experimental results pointed out some cognitive capacities of dolphins which might be
crucial for their wild life given their fission-fusion social system and migratory behaviour.
Background
Laterality, previously considered to be exclusively a
human characteristic, has been show in many verte-
brates as well as invertebrate species (for example:
[1-6]). Thus, the asymmetry of cerebral functions seems
to be the rule rather than the exception in the animal
kingdom [7]. Analyses of lateralized motor, perceptual
or behavioral responses broaden our understanding of
cerebral organization and of treatment of information
by each cerebral hemisphere.
Characteristics of perceived stimuli can be linked to the
treatment of the information received by one of the cere-
bral hemispheres and to the implication of a given
hemisphere. This link is modulated by subjectsinternal
state such as levels of hunger, vigilance or stress [8], as
well as their age [9] or social environment [10]. Moreover,
stimulus characteristics like emotional value [11,12] and
novelty [13,14] are known to influence perceptual
laterality.
The anatomical characteristics of the visual nervous sys-
tem make visual laterality a good candidate to study per-
ceptual laterality, and most particularly in dolphins. It is
well known that the two cerebral hemispheres do not
receive sensory information from a single stimulus in the
same proportions. For instance in many mammals, the
contralateral hemisphere receives monocular visual infor-
mation faster (crossed fibers) than that received by the
ipsilateral hemisphere (uncrossed fibers) [8,15]. So the
involvement of each cerebral hemisphere depends on the
organization, the quantity and the transmission speed of
* Correspondence: catherine.blois-heulin@univ-rennes1.fr
1
UMR 6552 University of Rennes 1 - CNRS, Station Biologique, 35380
Paimpont, France
Full list of author information is available at the end of the article
Blois-Heulin et al.BMC Neuroscience 2012, 13:9
http://www.biomedcentral.com/1471-2202/13/9
© 2012 Blois-Heulin et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attri bution License (http://creativecommons.org /licenses/by/2.0), which permits unrestricte d use, distribution, and
reproductio n in any medium, provided the original work is properly cited.
nervous impulses [15]. Dolphins are particularly interest-
ing model for hemispheric laterality investigations for at
least four reasons. First, their eyes are situated laterally
and all their optic fibers cross [16,17] allowing a reliable
interpretation of the underlying cerebral asymmetry. The
left hemisphere receives visual information exclusively
from the right eye, and the right hemisphere from the left
eye. Moreover, stronger isolation of brain hemispheres is
due to relatively less developed corpus callosum [18]. Pre-
ferential use of a given eye (also called eye use bias) at the
group level indicates the treatment of visual information
by the contralateral hemisphere [11,19]. Second, several
reports evidence the existence of lateralized behavior in
marine mammals (whales: [20,21]; dolphins: [16,22-25]).
For example, the general tendency of dolphins to swim
counter-clockwise [16,24,25] might indicate the presence
of laterality in this species. Third, previous reports indi-
cated that dolphins generally use monocular vision (due to
a narrow binocular visual field), and that they visually
solve visio-spatial tasks better using their right eye and
therefore their left brain hemisphere [17,24,26-29]. How-
ever, a recent study has shown that even if dolphins were
clearly able to visually discriminate between familiar and
unfamiliar human beings, they preferentially used their left
eye to look at those two categories of people [30]. Forth,
dolphins possess a high brain/body ratio [31], and several
of the brains morphological traits differ from those of ter-
restrial mammals [31-34]: their brains present anatomical
structures similar to those of highly evolved brains, but at
the same time, the organization of their rudimentary neo-
cortex recalls more that of the hypothetical ancestor of
mammals [35]. Analysis of their perceptual laterality
should help understand the implication of each hemi-
sphere in the treatment of various types of information,
compared to other species.
One of the most frequently studied characteristics of
stimuli influencing perceptual laterality is novelty). A cer-
tain consensus appears concerning the processing of the
novelty of a stimulus (Novelty hypotheses). Generally,
the left eye is privileged to look at novel stimuli (chicks:
[36-38], fish: [39,40]) and/or to be better at processing or
storing visual information which allows recognition of
individual conspecific [41,42]. But exceptions can be
found. De Boyer Des Roches et al [43] have shown that
mares used preferentially their right eye to explore novel
objects. According to Navon [44,45], characteristics of
objects can be visually analyzed either globally or in detail
(local traits). Local characteristics are mainly analyzed by
the posterior superior temporal-parietal regions of the
left hemisphere while global characteristics are analyzed
by the posterior superior temporal-parietal regions of the
right hemisphere (Information treatment modality
hypotheses) [46-51]. Thus, a link between the type of
information treatment and the stimulus characteristics
can be surmised: global analysis should be favored when
observing a familiar object, whereas local analysis should
occur in presence of a novel object to gather detailed
information.
Our aim was to understand how these marine mam-
mals perceive, analyze and treat visual stimuli with dif-
ferent levels of familiarity (i.e. unfamiliar, familiar non-
manipulated, very familiar manipulated). In this study
the following questions were investigated experimentally:
(1) Is there a behavioral laterality in dolphins, as it was
found in others marine animals? (2) How does stimulus
novelty affect the visual preference in dolphins? Three
contradictory predictions can be done. First, based on
the novelty hypotheses, dolphins should preferentially
use their left eye to look at novel objects (unfamiliar)
and should not display any preference for non-novel
objects (familiar and very familiar). Second, according to
the Information treatment modality hypothesis[44,45],
dolphins should use their left eye to look at very familiar
objects, because a global visual inspection is sufficient to
recognize and categorize the stimulus, but use their
right eye to look at unfamiliar objects for which a more
detailed visual inspection is required. The third predic-
tion was based on Thieltges et al [30] results. These
authors have demonstrated that dolphins used their left
eye to look at human whatever their degree of novelty.
So we wondered whether dolphins would generalize this
left eye preference to look at all kinds of objects, regard-
less of their degree of novelty. 3) Is there a link between
visual and swimming laterality? As swimming laterality
seems strong in captive dolphins, we also analyzed the
swimming preferences of our animals in order to con-
trol that the visual laterality observed was not a direct
consequence of swimming preferences.
Results
Reactivity
Stimulus category neither influenced the number of trials
when dolphins approached and observed the set-up spon-
taneously (Friedman test, df = 2, c
2
= 6.35, p = 0.096), nor
the total number of gazes at objects of each category sig-
nificantly (Friedman test, df = 2, c
2
= 5.08, p = 0.166).
Dolphins preferred monocular to binocular vision to
look at object of all categories (Wilcoxon tests, z = 2.02,
p = 0.043).
Laterality
First reaction (Table 1)
Three dolphins (Cecil, Peos and Thea) used their left
eye to observe very familiar previously manipulated
objects, whereas two dolphins (Cecil and Mininos) used
their left eye to observe familiar never-manipulated
objects. None of the dolphins was lateralized when view-
ing unfamiliar objects (Table 1).
Blois-Heulin et al.BMC Neuroscience 2012, 13:9
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At the group level, a significant left bias was evident
when watching at very familiar previously manipulated
objects(ttest,t=-4.80,df = 4, p = 0.009) (Figure 1A).
Conversely, a significant right bias was evidenced for
watching at unfamiliar objects (ttest, t = 7.50, df =4,
p = 0.002). When watching at familiar never manipu-
lated, objects the dolphins did not use one eye prefer-
ably (ttest, t = -1.95, df = 4, p = 0.123) (Figure 1A).
Strength of laterality did not vary significantly with
experimental situation (Friedman test, ABS(VLI), c
2
=
1.20, df = 2, p = 0.55).
Reactions following the first reaction
Peos, Mininos and Thea used more their left eye to look
at very familiar, previously manipulated, objects. Two
dolphins (Cecil and Peos) used their left eye significantly
more frequently to look at familiar never manipulated
objects. Conversely, Amtanusedmoreherrighteyeto
observe unfamiliar objects (Table 2).
At the group level, as for the first reaction, a significant
left bias was evidenced for watching at very familiar pre-
viously manipulated objects (ttest, t = -3.41, df =4,p=
0.027), but no significant bias was found for watching at
familiar never manipulated objects (ttest, df =4,t=
-1.91, p = 0.129). The following reactions to unfamiliar
objects differed significantly from the first reaction to
these objects as no bias towards the usage of the left or
right eye was found (ttest, df = 4, t = 0.23, p = 0.832)
(Figure 1B).
Strength of laterality did not vary significantly between
the three experimental situations (Friedman test, c
2
=
0.89, df = 3, p = 0.85).
Comparisons of bias and strength of laterality between the
first and the following reactions
Laterality indices and strength of laterality did not differ
significantly between the first and the following reac-
tions irrespective of the experimental situation (Wil-
coxon test, n = 5, FM situation: VLI z = 0.13 p = 0.893,
Abs (VLI) z = 0.13 p = 0.893; FNM situations: VLI z =
0.40 p = 0.686, Abs (VLI) z = 0.40 p = 0.686; NF condi-
tion: VLI z = 1.21 p = 0.225, Abs (VLI) z = 0.40 p =
0.686).
Rotational bias
All our dolphins were strongly lateralized, they swam
significantly more frequently in one direction than with-
out direction (binomial test: lateralized versus no direc-
tion, p < 0.001). Four of the five dolphins preferred to
swim counter-clockwise (Figure 2). At the group level
our dolphins also showed a preference to swim counter-
clockwise (ttest RI, t = -3.39, df = 4, p = 0.027).
Table 1 Variation of the laterality index (IVL) according
the level of object familiarity for the first reaction, p:
binomial test, bold character: significant results,
p < 0.05, L: left eye used
CECIL PEOS MININOS THEA AMTAN
Familiar-Manipulated
VLI -0.88 -0.58 -0.29 -0.63 -0.29
P0.001 0.019 0.424 0.021 0.332
Bais LL ns Lns
Familiars-Never
Manipulated
VLI -0.56 -0.47 -0.83 0.07 0.06
P0.031 0.118 0.006 1.000 1.000
Bais Lns Lns ns
Unfamiliar
VLI 0.29 0.18 0.37 0.43 0.33
P 0.424 0.629 0.167 0.180 0.238
Bais ns ns ns ns ns
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Figure 1 Visual laterality index (VLI) in relation to stimulus category. FM: familiar, previously manipulated objects, FNM: familiar, never
manipulated objects, UF: unfamiliar objects. Stars: results of t test,
*
: p < 0.01,
**
: p < 0.002.
Blois-Heulin et al.BMC Neuroscience 2012, 13:9
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4. Discussion
Our data showing that all our dolphins used monocular
vision spontaneously more frequently than binocular
vision confirmed previous reports [26]. This is certainly
due to the lateral eye position determining a small bino-
cular visual field in this species. A bias to use their left
eye (right hemisphere) to look at very familiar previously
manipulated objects emerged clearly at the group level
for both the first gaze and the following reactions. The
first gaze reaction to unfamiliar objects revealed a prefer-
ence to use the right eye (left hemisphere). However, this
bias disappeared during the subsequent reactions. No eye
preference was found for familiar never manipulated
objects. Our dolphins also showed a counter-clockwise
bias when swimming.
We can first confirm that our dolphins were strongly
lateralized when swimming and when looking at objects.
The fact that very familiar objects were visually inspected
with the left eye while unfamiliar objects were visually
inspected with the right eye, support the first of our three
predictions based on the information treatment modality
highlighted by Navon [44,45].
This difference of laterality at the group level between
previously manipulated stimuli (use of left eye) and unfa-
miliar stimuli (use of right eye) might thus be explained
by the way information leading to identification of
objects is treated. During the first inspection of unfami-
liar stimuli, dolphins might analyze details of the objects
notably to build a spatial mental representation in three
dimensions of the different parts of the object. This type
of analysis is characteristic of information treatment by
the left hemisphere [46,50,51]. Conversely, visual analysis
of very familiar objects remains global and is characteris-
tic of information treatment by the right hemisphere.
Our results confirm the difference between treatments:
dolphins used their left eye (right hemisphere) to look at
very familiar objects (global analysis) and their right eye
(left hemisphere) to look at unfamiliar objects (local ana-
lysis). No eye preference was found for the inspection of
objects presenting an intermediate familiarity value
(familiar non manipulated objects). However, as soon as
a previously unfamiliar object has been seen once, this
object becomes familiar, but still not manipulated, so no
more eye preference is found in the subsequent visual
inspections. This change fromusingthelefthemisphere
when treating visual information of an unknown shape to
using the right hemisphere when that shape has become
familiar has been reported previously [48]. The prefer-
ence to use the right eye to explore details of objects con-
firm previous reports on the visual discrimination
capacities of dolphins [17,26-29]. Dolphins discriminated
visually better and solved visio-spatial tasks better using
their right eye.
This rapid switch of classes from unfamiliar to familiar
support studies that concluded in favor of a rapid visual
memorization in dolphins [52,53]. The difference of
treatment between very familiar and familiar objects also
highlights the importance of the manipulation in dol-
phins. We can suppose that dolphins may possibly have
difficulties in constructing a spatial mental representation
of familiar never manipulated objects and of unfamiliar
objects that have become familiar solely through visual
modalities. If this is the case, manipulation of objects by
dolphins could facilitate their construction of a global
representation of an object enabling dolphins subse-
quently to categorize it directly, as echolocation and
vision are generally linked [53-56].
In a previous study with the same dolphins we found a
left-eye preference to look at familiar and unfamiliar
human beings [30]. This shows that any human being is
treated visually as are very familiar objects, a global
inspection being sufficient to have a mental representa-
tion of this kind of stimulus. We must acknowledge that
1
*
* *
*
*
*
* * *
0
10
20
30
40
50
60
70
80
90
100
CECIL PEOS MININOS THEA AMTAN
Figure 2 Swimming categories: numbers of observations of
each swimming type for each dolphin. White bars: all rotations;
black bars: swimming without direction; dark grey bars: clockwise
rotation, light grey bars: counter-clockwise rotation. *: results of
binomial test p < 0.05.
Table 2 Variation of the laterality index (IVL) according
the level of object familiarity for the reaction following
the first reaction, p: binomial test, bold character:
significant results, p < 0.05, L: left eye used
CECIL PEOS MININOS THEA AMTAN
Familiar-Manipulated
VLI -0.28 -0.61 -0.67 -0.78 -0.03
P 0.132 0.000 0.000 0.000 1.000
Bais ns LLLns
Familiars-Never
Manipulés
VLI -0.48 -0.60 -0.50 -0.25 0.29
P0.003 0.035 0.146 0.454 0.332
Bais LL ns ns ns
Unfamiliar
VLI -0.69 0.10 -0.14 0.25 0.73
P0.000 0.711 0.511 0.454 0.007
Bais Lns ns ns R
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a human observer was present in this study near the
exposed object and that this could have influence the
visual response of our dolphins. However, the observer
was the same person for all object presentations and
always stood at the same place. The fact that the eye
used changes with the object category let us think that
the presence of the observer had no impact on our data.
In addition to perceptual laterality, we also analyzed
swimming laterality and could thus control that the
visual laterality observed here was not a direct conse-
quence of swimming preferences. Our dolphins were
lateralized at the motor level. Our group revealed a pre-
ferred rotation direction (counter-clockwise), thus sup-
porting most previous reports on this theme [16,24,25].
This verified our third hypothesis. This rotational bias
alonecannotexplainthepredominanceoftheuseof
one eye since the direction of their visual laterality is
influenced by stimulus category.
As dolphins are migrant species they are confronted to a
changing environment. Being able to categorize new ver-
sus familiar objects allows dolphins a best and a rapid
adaptation to novel environment. Since we have demon-
strated that dolphins used more their left eye to inspect
well-known objects (this paper) as well as humans [30],
future investigations should explore about the visual pre-
ference of dolphins when looking at conspecifics. As dol-
phins are social species and as other cetacean species, like
beluga whale (calves were more on the right side of their
mother) [21], expressed social laterality, it will be legiti-
mate to wonder whether dolphins will also use their left
eye to look at all kinds of congeners or if the familiarity
with the conspecifc has some importance. This social
laterality at population level could play an important role
in the daily life of species like bottlenose dolphins present-
ing a fission-fusion social system, i.e. with opportunities to
meet conspecifics of different degrees of familiarity.
Conclusion
We clearly show the influence of a familiarity gradient on
dolphinsvisual laterality. A bias to use their left eye
(right hemisphere) to look at familiar previously manipu-
lated objects emerged clearly at the group level, whereas
we found a bias to use the right eye (left hemisphere) to
look at unfamiliar objects. A global vs detailed visual
treatment can explain the observed laterality.
Swimming laterality was strong but no link was found
between visual and swimming laterality. So our experi-
mental results pointed out some cognitive capacities of
dolphins that are indispensible for their wildlife [52]. To
complete our studies, an analysis of social laterality will
be pertinent. On which side a dolphin approach another
congener and can the familiarity with the congener
modulate this laterality?
Methods
Subjects
Our subjects were five captive-born dolphins: three 5 to
25-year old males (Mininos, Peos and Cecil), and two
females, respectively 8 and 17 years old (Amtan and
Thea). They were housed by the Cité Marine at the Pla-
nète Sauvage Safari Park (44, France) in a large aquatic
facility (4 pools with 8.5 million liters of water). Six
human caretakers fed the dolphins with fish, 6 to 8
times a day, during training and public presentations.
Veterinary assessment of these dolphinsvision
revealed no deficiencies and no pathology that might bias
our research. The dolphins participated in six training
session every day, between 10 oclock and 16clock. They
never participated in a public presentation during the
course of this study.
Methods
The dolphins were tested in the round, 20 m in diameter,
4.85 m deep maximum, nursery pool. Three types of sti-
mulus were presented: familiar, previously manipulated
objects (balls, discs...) (FM), familiar never manipulated
objects (diving mask, watering can, boots...) (FNM) and
unfamiliar objects (unknown: storage box, kettle, cycle
helmet, thermos flask...) (UF). The size range of dolphins
toys varying in size (0.2 m to 1 m), as well as in shape
and color. Each stimulus was presented once. Twenty
objects of each category were used to test the dolphins
and each stimulus was presented once.
Before a stimulus was presented, it was hidden behind
a curtain so that the dolphins could not see it. The cur-
tain was suspended from a 2 m high, 1.20 m wide PVC
frame with which the dolphins were already familiar [56].
This curtain was placed 1.20 m from the pool edge.
Behind the curtain the object was placed on a wooden
box (35 × 40.5 × 45.5 cm) with which the dolphins were
also familiar. This box was used to raise the stimulus
making it easier to see (preliminary experiment). The sti-
muli were presented in air for practical reasons and can
be done because dolphinsvisual acuteness is globally
similar in above and below the water surface [57-59].
Moreover, underwater dolphins might have used not
only vision but also echolocation. This frame + box were
put in place, two minutes before a test. A trial started
when the experimenter opened the curtain. The object
remained visible for three minutes. No previous training
was necessary, and no reinforcement was given. Dolphins
were observed during 180 minutes (20 objects of each
category × 3 categories × 3 minutes per object).
During a presentation, all the reactions of the dolphins
to the experimental set-up at the surface were recorded,
but observations were restricted to the half of the pool
close to the objects (20 m × 9 m) [30]. So our laterality
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study only concentrated on short-distance visual inspec-
tion, which means that all dolphins had the chance to
first see the object from far before approaching, a still
reasonable distance to appreciate whether the object
was novel or not. The subjects were filmed in this area
ofthepoolbyavideo-camera(JVCEverioGZ-
MG332HE) placed on top of the frame [30]. The obser-
ver, standing randomly either to the left or to the right
of the curtain, described, using a dictaphone (SCOTT
DVR 500), all the reactions observed in the area not
covered by the camera. The following variables were
recorded:
The identity of the dolphins in the area
The total number of short gazes at the water sur-
face and the eye with which the subject perceived
the stimulus. We first distinguished short and long
gazes (i.e. lasting respectively less and more than 2
seconds) (Kuczaj, Pers. Com.). But dolphins per-
formed too few long gazes to possibly include them
in the analysis.
At least 15 minutes elapsed after a feeding session, an
interaction with careers or a previous test before a test.
Three to eight (mean 5.71) tests were made per day and
occurred at various time of the day (between 10 h and
18 h).
MC conducted a blinded analysis of videos
Independent of experimental tests, the direction of dol-
phinsspontaneous rotations in the pool was investigated.
Hourly instantaneous scan observations between 9.30
oclock and 16.30 oclock recorded either rotation direc-
tion (clockwise or counter-clockwise) or the absence of
rotation for each dolphin. Eight scans were performed per
day, yielding 112 scans.
Statistical analyses
Friedman tests analyzed the numbers of trials when a sub-
ject approached the objects of a given category sponta-
neously in order to look at them and the numbers of gazes
at each object. Wilcoxon tests compared use of monocular
vision to use of binocular vision.
The first reaction of each dolphin, i.e., the first time a
subject observed the object and all the reactions following,
the first reaction (= following reactions in the text), were
considered separately to estimate laterality. Thus, a visual
laterality index (VLI) was calculated for each dolphin
using the formula: (R-L)/(R+L), R and L are the numbers
of times the right eye and the left eye were used to observe
objects. This index varies from -1 to +1, negative values
indicate a preference to use the left eye and positive values
a preference to use the right eye. In addition, the absolute
value of VLI estimates strength of laterality. Binomial tests
evaluated each subjects preference to use one eye by com-
paring the numbers of times the right eye and the left eye
were used for each experimental category. At the popula-
tion level, ttests, applied to VLI values, estimated the pre-
sence of laterality at the group level. Friedman tests on
VLI values and on their absolute values evaluated varia-
tions of direction and of strength of laterality between
experimental conditions. Wilcoxon tests compared direc-
tion and strength of laterality between the first reaction
and the following reactions.
Finally, binomial tests compared 1) the number of
times a subjects swimming presented a lateralized rota-
tion direction to the number of times its swimming pre-
sented no precise rotation direction, and 2) the number
of times it swam clockwise to the number of times it
swam counter-clockwise. A rotation index (RI): (number
oftimesasubjectswamclockwise-numberoftimesit
swam counter-clockwise)/(total number of rotations)
was calculated for each subject. A ttest on these RI
values estimated the presence of a preferred direction at
the group level.
Significance level for all statistical analyses was p <
0.05.
Experimental research reported in this manuscript has
been performed with the approval of ethics committee
(DDSV n° 04672).
Acknowledgements
We thank all caretakers of Planète Sauvage Zoo for technical support, and
Ann Cloarec for translation.
Author details
1
UMR 6552 University of Rennes 1 - CNRS, Station Biologique, 35380
Paimpont, France.
2
Département scientifique, Planète Sauvage, 44710 Port-
Saint-Père, France.
Authorscontributions
MC participated in the design of the study, conducted the experiments, and
performed the video and statistical analysis. MB participated in the design of
the study and conducted the experiment. AL initiated the study, participated
in the design of the study and participated in the preparation of the
manuscript. CBH initiated the study, contributed to the design of the study,
participated in the statistical analysis, and in the preparation of the
manuscript. All authors have read and approved this manuscript.
Received: 12 July 2011 Accepted: 12 January 2012
Published: 12 January 2012
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Cite this article as: Blois-Heulin et al.: Visual laterality in dolphins:
importance of the familiarity of stimuli. BMC Neuroscience 2012 13:9.
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... Most studies conducted in this animal category (i.e., [64][65][66][67]69,70]) evaluated with experimental methods visual laterality in the processing of positive/familiar vs. novel/negative stimuli or people. Results obtained in these investigations were at variance with the hypothesis assuming that the LVF (right hemisphere) may be involved in negative/unfamiliar stimulus processing and the RVF in the treatment of positive/familiar stimuli. ...
... Results obtained in these investigations were at variance with the hypothesis assuming that the LVF (right hemisphere) may be involved in negative/unfamiliar stimulus processing and the RVF in the treatment of positive/familiar stimuli. Only one study [70] found that dolphins were visually left-lateralized for negative stimuli, whereas three investigations [65,66,69] found that the RVF (left hemisphere) was preferentially used to explore negative unfamiliar stimuli. One further study [63] found that dolphins used their LVF to look at both familiar and unfamiliar stimuli and another [66] reported no clear visual laterality preference for familiar or unfamiliar stimuli. ...
... Only one study [70] found that dolphins were visually left-lateralized for negative stimuli, whereas three investigations [65,66,69] found that the RVF (left hemisphere) was preferentially used to explore negative unfamiliar stimuli. One further study [63] found that dolphins used their LVF to look at both familiar and unfamiliar stimuli and another [66] reported no clear visual laterality preference for familiar or unfamiliar stimuli. ...
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... Furthermore, as in other vertebrates, information from right eye therefore travels towards the left hemisphere (and left eye to the right hemisphere) 69 . Lateralized visual responses have been observed for familiar and non-familiar objects 56,70,71 and familiar and non-familiar humans 72,73 . However, Hill et al. 74 did not find any visual laterality bias whether dolphins looked at a familiar or unfamiliar human. ...
... Further studies also showed patterns of visual lateralization in dolphins according to familiarity when attending non-human stimuli. Some of these findings were opposite to those found here: Blois-Heulin et al. 70 found that dolphins used their left eye when viewing familiar objects and the right eye for unfamiliar ones while. Siniscalchi et al. 56 found that wild striped dolphins had a higher use of right eye for unfamiliar items floating at sea. ...
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Visual attention is an intrinsic part of intra- and inter-specific interactions. Its structure (e.g. short glances vs. long gazes) depends on the species, type and expected outcome of the interaction. The outcomes of earlier repeated interactions determine the resulting valence of the relationships. Human-animal relationships rely upon species-specific cognitive abilities and attentional characteristics for associative learning and memory formation. Visual attention is crucial in cognitive processing and relationships construction, but its structure may depend on species-specific characteristics and relationships’ quality. Dolphins are renowned for their cognitive abilities and in human-care settings they have regular interactions with caretakers. Dolphins’ visual attention structure and laterality both differ depending on the visual stimulus to which the animal is attending (species-specific, non-biological). We hypothesized that visual attentional characteristics and associated behaviours, in a group of 9 captive bottlenose dolphins (Tursiops truncatus), would differ according to past experience and familiarity with humans. Human motionless tests showed a role of experience (time spent) in the facility on play and vocal production near humans regardless of familiarity. However, familiarity influenced dolphin presence near humans and visual laterality: they stayed longer and used their right eye more to glance at familiar humans. These findings provide new insights on how dolphins cognitively process stimuli according to familiarity and past experiences, as well as on how human – animal relationships evolve in captive settings.
... [41][42][43][44] Despite the human perception of their ''anatomical smile'' as a friendly feature, 45 the role of facial communication in managing playful encounters remains unexplored in dolphins, although there is evidence that they rely on the visual sensory modality in their social life. [46][47][48][49] Here, by recording the free activities (outside the training and feeding sessions) of captive bottlenose dolphins, we explore the presence and possible functions of open mouth display (OM) during solitary, interspecific (human-dolphin), and intraspecific free play (spontaneously evoked according to the second Burghardt's criterion, 9 ) by testing the following hypotheses. ...
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The investigation of individual responses to unexpected stimuli or outcomes provides insights into basic cognitive processes, such as mental representations, emotional states of surprise, and detections of anomalies. Three experiments using a violation of expectation paradigm were conducted with 12 belugas and 17 bottlenose dolphins in managed care to test two classes of stimuli (humans and objects) in manipulated sequences of familiar and unfamiliar humans (Study 1, trainers and strangers), familiar and unfamiliar objects (Study 2, typical enrichment devices and new objects), and finally objects and humans (Study 3). Gaze durations were assessed for each condition in a given study during free-swim contexts. The results supported previous findings that visual stimuli, regardless of class, were stimulating and intriguing for both belugas and bottlenose dolphins. Belugas were more likely to gaze longer at human and object stimuli and tended to gaze longer at unexpected experiences than control or expected experiences. Bottlenose dolphins showed similar trends except when objects were involved. Individual variability was present for both species with some individuals showing stronger patterns of responses for expected experiences than others. After 2 years of intermittent experiments, belugas and bottlenose dolphins in managed care maintained their curiosity about visual stimuli, for which they received no primary reinforcement. Investigating responses to unexpected stimuli with animals in managed care may provide insight into how these animals respond to biologically relevant conditions, such as boat presence, predators, and unfamiliar conspecifics.
... Using experimental designs, several studies have documented eyeuse preferences while viewing objects and completing visual tasks. Overall, bottlenose dolphins typically showed a right eye preference while viewing objects, especially those more unfamiliar or unpredictable (e.g., Blois-Heulin et al., 2012;Clark and Kuczaj, 2016;Lilley et al., 2020a;Yeater et al., 2017). This pattern also extends to bottlenose dolphins completing experimental visual tasks (e.g., von Fersen et al., 2000;Yaman et al., 2003); however, some studies have found competing results (e.g., Matrai et al., 2019). ...
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Chapter
This chapter covers methods of measuring eye and ear preferences to attend to sensory information and methods revealing hemispheric differences in processing sensory information. It begins with monocular occlusion as a way of measuring differences in type and strength of response elicited by visual stimuli. Depending on the type of stimulus presented, a preference for responding using the left or right eye can be found (e.g., domestic chicks show a right-eye preference when searching for food grains and a left-eye preference when attacking a conspecific or responding to a predator). Especially in species with their eyes positioned laterally and hence with small binocular visual fields, differences between responses elicited after applying a patch to the left- or right-eye reflect differences in processing by the left and right sides of the brain respectively. In these species, it is also possible to test responses to stimuli presented in the left versus right monocular visual fields without having to apply eye patches. A method of determining the extent of the monocular and binocular visual fields is explained. Then a modification of the monocular testing method involving rotation of the stimulus around the animal is discussed: as shown in frogs and toads, response to prey moved in this manner differs between clockwise and anticlockwise rotation. Eye preferences can also be determined using binocular presentation of stimuli that elicit head turning to permit monocular fixation of the stimulus before a specific response is made (e.g., before attacking a conspecific, as scored in chicks and horses). Angles adopted by fish when viewing their image in a mirror have been used to measure lateralization of attending to a “conspecific.” Another approach is the simultaneous introduction of identical stimuli into the monocular field of each eye and assessment of side biases in responding (as in toads striking at insect prey). Visual pathways and strategies of monocular viewing are discussed briefly to help explain how eye preferences reveal brain lateralization. Next, several methods of measuring lateralization of processing and responding to auditory stimuli are covered and finally some points are made about future directions of research along these lines. The suitability of these methods for testing different species is considered in all sections of the chapter.
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The midsagittal surface area of the corpus callosum was determined by computer-assisted morphometry in juvenile and adult members of 13 species of the cetacean family Delphinidae. In 57 brains, absolute callosal areas ranged from 104 to 829 mm2. When compared to other mammal groups possessing a corpus callosum, callosal area in dolphins was smaller in relation to brain mass with a ratio range (mm2/g)) of 0.08-0.31. The corpus callosum was decreased relative to brain mass in the larger-brained odontocetes, suggesting that increases in brain size were not necessarily allied with needs for equivalent increases in callosal linkage. One delphinid species, Tursiops truncatus, for which the largest single- species sample was available, was examined for sex differences in callosal size relative to brain mass. Among 10 males and 5 females the averaged ratio was not distinguishable between sexes.
Book
On the cutting edge of neuropsychology and cognitive science, this book investigates lateral asymmetries in the human brain and contrasts these with asymmetries in primates as well as invertebrates, primitive vertebrates, birds, and other mammals. Nine illustrated chapters present asymmetries in lower life forms, progress to hominoids and hominids, and discuss how such asymmetries are responsible for the development of language, upright posture, tool use, intellect, and self-awareness in humans.
Article
Geometries of the iris, retinal cell distributions, and the optical characteristics of the lens and cornea have evolved to optimize the visual adaptations of the bottlenose dolphin (Tursiops truncatus) to the oceanic environment. Under high ambient light conditions, the operculum of the iris shields the lens and forms two asymmetrical slit pupils. Under these conditions, light entering the eye is channeled and focused onto the two areas of the retina having a finer retinal mosaic of ganglion cells (typically associated with higher image resolution). The paths of light determined by tracing rays in the reverse direction through these pupils coincide with a dolphin's behaviorally observed preferred viewing directions. These rays aid in determining the interdependence between the graininess of the retinal mosaic and resolution spot sizes in the object space. For oblique forward and downward viewing directions in air, the larger temporal pupil admits light which passes through the weakly refractive margin of a bifocal lens, counterbalancing the optically strong cornea in air. In water, light passing through the optically strong lens core is focused from a wide lateral and downward field-of-vision. Although other explanations for comparable aerial and underwater vision remain plausible, a dolphin eye model incorporating a bifocal lens offers an explanation consistent with ophthalmoscopic refractive state measurements. The model is also consistent with visual acuity study results conducted in air and in water under both high and low ambient light levels. From insight gained after applying a common data analysis technique to visual acuity studies conducted by other researchers and tracing oblique rays through the asymmetric double-slit pupils, a re-examination of explanatory hypotheses for the paradoxical observations of comparable aerial and underwater vision is presented. Based in part on these findings and supportive evidence from dolphin vision researchers, the unique distinguishing characteristics of dolphin vision are summarized.
Article
Examined eye preference during courtship in 44 testosterone-treated domestic chicks and in 12 male zebra finches. Observations of both types of birds provide evidence for the theory that lateralization of function in the central nervous system (CNS) of birds might be accompanied by preferential use of right or left eye according to need. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
The extent of eye and hand preference and their correlation was tested, 1st in 19 naive, immature Ss and then in 7 experienced adolescent-to-mature animals. There was no significant correlation between the 2 functions in either group. Hand preference, but not eye preference, was significantly greater in the older than in the younger monkeys. (PsycINFO Database Record (c) 2012 APA, all rights reserved)