Laterality, previously considered to be exclusively a human characteristic, has been show in many vertebrates as well as invertebrate species (for example: [1
]). 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 cerebral hemispheres and to the implication of a given hemisphere. This link is modulated by subjects' internal 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
] and novelty [13
] are known to influence perceptual laterality.
The anatomical characteristics of the visual nervous system make visual laterality a good candidate to study perceptual 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 information faster (crossed fibers) than that received by the ipsilateral hemisphere (uncrossed fibers) [8
]. So the involvement of each cerebral hemisphere depends on the organization, the quantity and the transmission speed of nervous impulses [15
]. Dolphins are particularly interesting model for hemispheric laterality investigations for at least four reasons. First, their eyes are situated laterally and all their optic fibers cross [16
] 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
]. Preferential 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
]. Second, several reports evidence the existence of lateralized behavior in marine mammals (whales: [20
]; dolphins: [16
]). For example, the general tendency of dolphins to swim counter-clockwise [16
] might indicate the presence of laterality in this species. Third, previous reports indicated 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
]. However, 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 brain's morphological traits differ from those of terrestrial mammals [31
]: their brains present anatomical structures similar to those of highly evolved brains, but at the same time, the organization of their rudimentary neocortex recalls more that of the hypothetical ancestor of mammals [35
]. Analysis of their perceptual laterality should help understand the implication of each hemisphere 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 certain 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
], fish: [39
]) and/or to be better at processing or storing visual information which allows recognition of individual conspecific [41
]. 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
], 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
]. 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 mammals perceive, analyze and treat visual stimuli with different 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
], 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 prediction 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, regardless 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 control that the visual laterality observed was not a direct consequence of swimming preferences.