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1 Brief Communication 29 How birds use their eyes: Opposite left-right specialization for the lateral and frontal visual hemifield in the domestic chick Giorgio Vallortigara*, Claudio Cozzutti, Luca Tommasi, and Lesley J. Rogers Recent evidence has demonstrated that, in animals lateralization of attack and some other visually guided with laterally placed eyes, functional cerebral responses in the chick [8, 9], we used both chicks hatched asymmetry is revealed by preferential use of either from eggs maintained in the dark until hatching (D-chicks) the left or right eye in a range of behaviors (birds: and chicks hatched from eggs exposed to light during [1, 2, 3]; fish: [4, 5]; reptiles: [6, 7]). These findings the last three days before hatching (L-chicks). For light pose a theoretical problem. It seems that there exposure, a 60 W lamp provided 300 Lux within the would be disadvantages in having a substantial incubator. We reared 40 L-chicks and 36 D-chicks in pairs degree of asymmetry in the use of the two eyes; a at a controlled temperature (30 35 C)in metal cages (30 deficit on one side would leave the organism cm)that were illuminated from above by fluorescent vulnerable to attack on that side or unable to lamps. For each pair of companion chicks, another exploit resources appearing on one side. We here pair was selected, and the two pairs were tested simultaneously report a possible solution to the problem. We have (either as pairs of companions or pairs of strangers) found that domestic chicks show selective use of in two separate cages ( cm). The behavior the lateral visual field of the left eye and of the of the chicks was videorecorded for 5 min. Since data for right hemifield in the binocular, frontal visual field an individual subject could not be considered to be entirely when they peck at strangers but not at cagemates. independent of the other chick in the pair, data for Thus, during social recognition, there seems to be each pair were considered together as one score (light opposite and complementary left-right companions, N 10; light strangers, N 10; dark com- specialization for the lateral and frontal visual fields panions, N 8; dark strangers, N 10). The numbers of the two eyes. These findings can reconcile the of pecks directed to the conspecific and to the environ- computational advantages associated with ment (at the floor or walls of the cage)were measured asymmetry of the left and right sides of the brain from the videotapes. In addition, we measured the fre- with the ecological demands for an animal to quency with which the chick used its lateral and frontal perceive and respond equally well to the left and fields of vision to fixate before pecking. We made these right sides of its midline. measurements by using transparencies to superimpose protractors on the monitor screen (Figure 1). We classified Addresses: *Department of Psychology, Animal Cognition and angles between 15 degrees of the midline as use of the Comparative Neuroscience Laboratory, University of Trieste, and B.R.A.I.N. Centre for Neuroscience, Trieste 34123, Italy. Department frontal (binocular)visual field and the remaining angles of General Psychology, University of Padova, Padova 35131, Italy. as use of the lateral visual field [1]. Note that, although School of Biological Sciences, Division of Zoology, University of New the chick pecks by a ballistic movement of its head for- England, Armidale NSW 2351, Australia. ward from its midline, it fixates and decides whether to peck or not prior to this by turning its head to view the Correspondence: Giorgio Vallortigara vallorti@univ.trieste.it stimulus and using the high-acuity regions of its retina. Received: 6 October 2000 Revised: 8 November 2000 Accepted: 21 November 2000 Published: 9 January 2001 Current Biology 2001, 11:29 33 Figure 2 shows that, as expected, both L- and D-chicks pecked more at strangers than at companions. Pecks at the environment, in contrast, were higher in D-chicks than in L-chicks and tended to be higher among strangers in L-chicks and among companions in D-chicks /01/$ see front matter Use of the lateral and frontal visual fields before pecking 2001 Elsevier Science Ltd. All rights reserved. shows opposite directions of lateralization in D-chicks (Figure 3): D-chicks preferentially used the left, lateral Results and discussion monocular field and the right, frontal hemifield before Chicks were tested, on day 3 after hatching, in pairs com- pecking at strangers. L-chicks showed significant use of posed of companions (cagemates)or strangers. Social the left, lateral monocular field but, in contrast to the pecking by each chick at its test partner was scored. Since D-chicks, no differences with respect to the frontal hemifields. previous work had revealed that exposure of the embryo A more detailed analysis of the different targets of to light during the final days of incubation determines pecking (Figure 4)confirmed these data and showed that

2 30 Current Biology Vol 11 No 1 Figure 1 Schematic representation of a chick s use of the frontal or lateral field of vision before pecking ( indicates the angle used to peck at the target in this case). Figure 2 Number of pecks directed at a conspecific and at the environment in pairs of companion and stranger chicks. There were more pecks at strangers than at companions in both L- and D-chicks [test condition: F(1, 34) , p 0.001; hatching condition: F(1, 34) (not significant, or ns ); test hatching: F(1, 34) (ns)]. Separate analyses showed that the companions/strangers difference was evident (see bottom row) only for pecks at the head [F(1, 34) , p 0.003], and the body [F(1, 34) , p 0.001] but not for pecks at the feet [F(1, 34) (ns)]. Pecking at the environment was the same among pairs of companions and strangers [F(1, 34) 0.470, p 0.498]; however, pecking at the environment was higher among D- than among L-chicks [F(1, 34) 6.087, p 0.019], and there was a tendency [interaction: F(1,34) 3.815, p 0.059] in L-chicks for higher pecking among strangers and in D-chicks for higher pecking among companions.

3 Brief Communication 31 Figure 3 Chicks use of the lateral field before pecking at a conspecific showed (ns)]; the test hatching interaction was, however, significant [F(1,34) a significant effect of testing conditions [F(1, 34) 7.387, p 0.010] 5.335, p 0.05]. D-chicks, but not L-chicks, showed a significant in both L- and D-chicks; there were no other statistically significant preference (one-sample t-test, two-tailed; see figure) for using the right effects [hatching: F(1,34) 0.18 (ns); test hatching: F(1,34) frontal field when tested as pairs of strangers (ns)]. Chicks showed a significant preference (one-sample There were no statistically significant effects associated with eye use t-test; two-tailed; see figure) for using the left lateral field when they before pecking at the environment [lateral field hatching, F(1,34) were tested in pairs of strangers. Use of the frontal field before pecking 0.023; test, F(1,34) 0.066; test hatching, F(1, 34) at a conspecific showed a significant effect of testing conditions Frontal field hatching, F(1,34) 0.035; test, F(1,34) 1.820; [F(1,34) 4.175, p 0.05], but not of hatching [F(1,34) test hatching, F(1,34) 0.810]. the effects were largely confined to hemifield use before pecks at the head. No significant preferences in hemifield use were apparent before pecking at the environment (Figure 3). These findings provide a solution to a puzzling phenome- non. A number of independent reports have provided convincing evidence that animals with laterally placed eyes show preferential left and right use in different tasks (reviewed in [10]). For instance, chicks use the left eye to look at an aerial predator [2] and the right eye to look at a familiar imprinting stimulus [1, 11]. Anolis lizards [6, 7] and toads [12, 13] use the left eye during agonistic encounters, and fish use the right eye to look at a danger- ous stimulus [14] and the left eye to look at conspecifics [5]. Results of studies that use selective occlusion of one eye complement these results by showing that birds performance in a variety of tasks depends on which eye they use (reviews in [15, 16, 17]). However, having one eye that is better at responding to a predator or recognizing a partner appears to be a disadvantage on ecological grounds; other things being equal, these stimuli might happen to be located on either side at random. The answer that has been provided so far is that the computational advantages associated with possession of an asymmetric brain [18, 19, 20] should compensate for the ecological disadvantages of perceiving and responding with less efficiency to one or the other side of the body. However, our results suggest a different answer. The two eyes of the domestic chick seem to provide visual information that can be used for social recognition, but they utilize different parts of the visual field; of the two lateral fields, the left is used preferentially, whereas in the binocular field the area to the right of the midline (right binocular hemifield)is used preferentially. Interestingly, previous evidence had shown that chicks wearing monocular eye patches were unable to discriminate between companions and strangers when they were using their right eye [21, 22] and that, in contrast, chicks with blinkers covering the right frontal field (but leaving the lateral field unob- structed)showed difficulty in inhibiting pecks at compan- ions [23]. This is now understandable because use of eye

4 32 Current Biology Vol 11 No 1 Figure 4 Chicks use of the lateral field before pecking at different parts of the conspecific revealed a significant difference between companions and strangers for pecks at the head [F(1, 34) , p 0.001], whereas use of the frontal field revealed a significant difference for both pecks at the head [F(1, 34) 5.510, p 0.025] and pecks at the feet [F(1, 34) 0.047]. There were no other statistically significant effects. patches prevents (or disturbs)use of the frontal visual field and thus reveals only part of the true specialization of the two eyes. It is interesting to note that, in both D- and L-chicks, the left eye sends its input via the thalamofugal pathway more strongly to the right hemisphere than to the left hemisphere and via the fast relay system of the tecto- fugal pathway also only to the right hemisphere (i.e., via the rotundal-ectostriatal connections without collateral branches [26]). (Note that it is likely that the slower system of the tectofugal pathway, via the unmyelinated ro- tundal-ectostriatal projections with collateral branches that cross the midline, is not used for attack pecking [26].) Inputs from the right eye differ in D- and L-chicks. In L-chicks, the right eye sends inputs to both hemispheres via the thalamofugal pathway and, again, via the fast system of the tectofugal pathway to only the left hemisphere [27]. In contrast, the right eye of D-chicks sends inputs almost entirely to the left hemisphere via both systems. The left and right frontal fields of D-chicks are, therefore, less integrated than those of L-chicks, and that could explain why the frontal-field asymmetry is revealed only in D-chicks. Unlike the pigeon, the chick has only one region of high ganglion-cell density, providing high-acuity vision, that is directed primarily to the lateral monocular field [24, 25]. This area of the retina of only the left eye is used before a peck is directed toward a stranger. An area of high but somewhat lower ganglion-cell density extends away from this central region in the horizontal plane and just into the temporal retina (i.e., it receives input from the frontal field). This provides acuity vision into the binocular fields, but there is no overlap across the midline of the highacuity regions of each eye (see Figure 10 of [24])unless the eyes are converged. It is, therefore, likely that when a chick fixates binocularly before pecking, it may be using only the right half of the binocular field. We might therefore conclude that, before pecking a stranger, the chick uses either the lateral field of its left eye (right hemisphere)or the right frontal field (left hemisphere or perhaps both hemispheres if the eyes are converged). Thus, it appears that there is a form of complementary specialization of the eye fields, at least in the case of chicks incubated in the dark. Chicks exposed to light also show preferential use of the left lateral field for pecking a stranger, but they use both the left and right binocular fields. These findings may indicate better integration of the hemispheres, which could result because early experience with light allows better coordination of visual input from the two eyes.

5 Brief Communication 33 a stroll through left and right animals perceptual worlds. Brain and Language 2000, 73: In conclusion, there is complementary specialization of the left lateral and right frontal visual fields for fixation 20. Güntürkün O, Diekamp B, Manns M, Nottelmann F, Prior H, Schwarz before pecking. These preferences make use of different A, et al.: Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol 2000, 10:1079- high-acuity regions of each retina and, presumably, might provide qualitatively different information to the visual 21. Vallortigara G, Andrew RJ: Lateralization of response to change regions of the hemispheres. One might ask why eye (and in a model partner by chicks. Animal Behaviour 1991, 41: hemisphere)use is lateralized in this way, and the answer 22. Vallortigara G: Right hemisphere advantage for social could lie in the specialization of the right hemisphere for recognition in the chick. Neuropsychologia 1992, 9: McKenzie R, Andrew RJ, Jones RB: Lateralization in chicks and processing topographical information [28] because this hens: new evidence for control of response by the right eye might require use of the wide-angle, lateral field of the system. Neuropsychologia 1998, 36: left eye. No such requirement would be demanded by 24. Ehrlich D: Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion the left hemisphere (and right eye)even though it, too, cell layer. J Comp Neurol 1981, 195: directs agonistic pecking. 25. Morris VB: An afoveate area centralis in the chick retina. J Comp Neurol 1982, 210: Deng C, Rogers LJ: Bilaterally projecting neurons in the two visual pathways of chicks. Brain Res 1998, 794: References 27. Rogers LJ, Deng C: Light experience and lateralization of the 1. Dharmaretnam M, Andrew RJ: Age- and stimulus-specific use of two visual pathways in the chick. Behavioural Brain Res 1999, right and left eyes by the domestic chick. Animal Behaviour 98: , 48: Rashid N, Andrew RJ: Right hemisphere advantage for 2. Evans CS, Evans L, Marler P: On the meaning of alarm calls: topographical orientation in the domestic chick. functional references in the avian vocal system. Animal Neuropsychologia 1989, 27: Behaviour 1993, 46: Vallortigara G, Regolin L, Bortolomiol G, Tommasi L: Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behavioural Brain Res 1996, 74: Bisazza A, De Santi A, Vallortigara G: Laterality and cooperation: mosquitofish move closer to a predator when the companion is on their left side. Animal Behaviour 1999, 57: Sovrano V, Rainoldi C, Bisazza A, Vallortigara G: Roots of brain specializations: preferential left-eye use during mirrorimage inspection in six species of teleost fish. Behavioural Brain Res 1999, 106: Deckel AW: Laterality of aggressive responses in Anolis. Journal of Experimental Zoology 1995, 272: Deckel AW: Hemispheric control of territorial aggression in Anolis carolinensis: effects of mild stress. Brain Behaviour and Evolution 1998, 51: Rogers LJ: Light experience and asymmetry of brain function in chickens. Nature 1982, 297: Rogers LJ: Light input and the reversal of functional lateralization in the chicken brain. Behavioural Brain Res 1990, 38: Vallortigara G, Rogers LJ, Bisazza A: Possible evolutionary origins of cognitive brain lateralization. Brain Res Reviews 1999, 30: Vallortigara G, Regolin L, Pagni P: Detour behaviour, imprinting, and visual lateralization in the domestic chick. Cognitive Brain Res 1999, 7: Robins A, Lippolis G, Bisazza A, Vallortigara G, Rogers LJ: Lateralization of agonistic responses and hind-limb use in toads. Animal Behaviour 1997, 56: Vallortigara G, Rogers LJ, Bisazza A, Lippolis G, Robins A: Complementary right and left hemifield use for predatory and agonistic behaviour in toads. NeuroReport 1998, 9: Facchin L, Bisazza A, Vallortigara G: What causes lateralization of detour behaviour in fish? Evidence for asymmetries in eye use. Behavioural Brain Res 1999, 103: Andrew RJ: The nature of behavioural lateralization in the chick. In Neural and Behavioural Plasticity. Edited by Andrew RJ. Oxford: Oxford University Press; 1991: Güntürkün O:Avian visual lateralization: a review. Neuroreport 1997, 8: Rogers LJ: Behavioral, structural and neurochemical asymmetries in the avian brain: a model system for studying visual development and processing. Neuroscience and Biobehavioral Reviews 1996, 20: Rogers LJ: Evolution of hemispheric specialization: advantages and disadvantages. Brain and Language 2000, 73: Vallortigara G: Comparative neuropsychology of the dual brain:

S21-2 Relative contributions of the two visual pathways to avian behavior

52(Supplement): 379 383, 2006 S21-2 Relative contributions of the two visual pathways to avian behavior Chao DENG Dept. of Anatomy, School of Medical Sciences, University of New South Wales, Sydney, NSW