- Email: [email protected]
Lateralization of response to social stimuli in fishes: A comparison between different methods and species
Physiology & Behavior 74 (2001) 237 – 244
Lateralization of response to social stimuli in fishes: A comparison between different methods and species Valeria Anna Sovranoa,*, Angelo Bisazzaa,1, Giorgio Vallortigarab a
b
Department of General Psychology, University of Padua, Via Venezia 8, 35131 Padua, Italy Department of Psychology and BRAIN Centre for Neuroscience, University of Trieste, Via S. Anastasio 12, 34123 Trieste, Italy Received 13 March 2001; received in revised form 20 April 2001; accepted 28 May 2001
Abstract We measured the time spent in monocular viewing during inspection of their own mirror images in females of three species of fish (Xenotoca eiseni, Gambusia holbrooki and Xenopoecilus sarasinorum) using a rectangular tank in which animals could observe their own reflections in two mirrors positioned along the major walls, and in females of five species of fish (X. eiseni, G. holbrooki, X. sarasinorum, Danio rerio and Gnatonemus petersii) using a quasi-circular tank in which fish could rotate clockwise or anticlockwise and observe their own reflections in a mirror positioned along the outer wall. Results revealed a consistent left-eye preference during initial sustained fixation in all species irrespective of the apparatus. However, in the quasi-circular tank, fish showed more variability of response. The asymmetry was apparent during the first 5 min of observation and tended to fade thereafter, probably as a result of habituation. These findings add to current evidence for a quite invariant pattern in the direction of lateralization in similar tasks in a variety of vertebrate species, with a preferential involvement of structures located to the right side of the brain in response to the viewing of images of conspecifics. D 2001 Elsevier Science Inc. All rights reserved. Keywords: Lateralization; Asymmetry; Social recognition; Right hemisphere; Fish
1. Introduction Research on animal lateralization is slowly moving from initial demonstrations of mere existence to investigations on proximate and ultimate causal mechanisms. We now know that behavioural lateralization is widespread in a variety of mammalian [10,14], avian [1,2,22,38,46], amphibian [9,36,52], reptilian [17,18], and fish [6,12] species. One interesting open issue is whether there is a fixed and invariant pattern in the direction of lateralization in the different species. Similarities in the direction of lateralization in different tasks among different species may be seen as evidence for possible homologies (see Ref. [49] for a discussion). But what is more important is the fact that if some ‘‘cluster’’ of information-processing mechanisms would appear consistently associated with the same side of the encephalon in * Corresponding author. Fax: +39-49-827-6600. E-mail addresses: [email protected] (V.A. Sovrano); [email protected] (A. Bisazza); [email protected] (G. Vallortigara). 1 Fax: + 39-49-827-6600.
otherwise very different species, that would provide clues to what may constrain the basic organization of the vertebrate nervous systems. There are indeed quite impressive suggestions of similarities in the direction of lateralization among vertebrates. One example concerns the selective involvement of the right side of the brain in spatial tasks. This has been largely documented in birds (i.e., chicks [35,42,43,50,51] and Parus [13]; but see Refs. [21,44] for a discussion of different spatial tasks) and in mammals [15,16]. Another example concerns the specialisation of the right hemisphere for face recognition in humans [40], which might be an elaboration of similar processes found in social recognition in nonhuman species. Sheep exhibit a lateral bias to the left visual field (right hemisphere) in visual recognition of familiar and unfamiliar faces [34]. Split-brain monkeys show similar specialisations of the right hemisphere to discriminate faces [24,55] and in birds the left eye seems to be involved in recognition of individual conspecifics [45,47,48]. Recently, evidence for a left-eye bias during scrutiny of conspecifics in some species of fish has been reported [41]
0031-9384/01/$ – see front matter D 2001 Elsevier Science Inc. All rights reserved. PII: S 0 0 3 1 - 9 3 8 4 ( 0 1 ) 0 0 5 5 2 - 2
238
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
(see also Refs. [3,19]). The basic finding was that species belonging to different families all showed a left-eye preference for looking at their own visual images in a mirror during a 5-min observation period (measures of eye use was confined to the lateral, monocular, visual field, which is known to project almost exclusively to the contralateral side of the nervous system; see Discussion for details of fish neuroanatomy). Although not particularly striking in strength when compared with other forms of human and nonhuman asymmetries, the lateralization in eye use was present at the population level and in the same direction in all the six species. More importantly, while most of the previous data concerned comparisons of animals of different taxonomic groups, here evidence arose from animals pertaining to the same class but different families. The aim of the present paper is threefold. Firstly, we wanted to check for the generality of the findings of Sovrano et al. [41] using a different experimental set up. Our original mirror test employed two parallel mirrors that generated a multiple-reflection phenomenon, so that the environment was very unusual for the fish with respect to the home-tank. Moreover, the fish was limited in its movement: when reaching one end of the mirror, it lost contact with its mirror reflection and was forced to move back and forth along the wall. Thus, we tried to develop a ‘‘quasi-circular’’ apparatus, with only one set of mirrors located on one wall so that the simple direction of circling, clockwise, and anticlockwise, could force (and reflect) preferential scrutinizing of the image using either the left or right eye. Secondly, we were interested to measure how preferential eye use changed with time. Does protracted exposure to the mirror image produce habituation and shift towards a balanced left- and right-eye use? Since we had available long-term videorecording of fish behaviour from previous experiments not analyzed yet, we could compare changes in eye use with time in both the ‘‘rectangular tank’’ and the ‘‘quasi-circular tank’’ mirror test. Finally, we extended the number of species analyzed. We tested in the novel apparatus three of the species already studied with the old apparatus (Xenotoca eiseni, Gambusia holbrooki
and Xenopoecilus sarasinorum) and two completely novel species (Danio rerio and Gnatonemus petersii).
2. Experiment 2.1. Materials and methods 2.1.1. Subjects Females of X. eiseni (n = 14), G. holbrooki (n = 16), X. sarasinorum (n = 7), D. rerio (n = 30), and G. petersii (n = 26) were used. Fish were kept in vegetation-rich (Ceratophyllum sp.) 120 – 150-l glass tanks, lit from above by fluorescent lamps (30 W) under a 14/10 light/dark period. Water temperature was maintained between 22C and 25C and fish were fed dry food twice a day. G. petersii was additionally fed with Chironomus larvae. 2.1.2. Procedure 2.1.2.1. ‘‘Rectangular tank’’ mirror test. The apparatus has been described in details elsewhere [41]. Testing was performed within a tank (44 22 30 cm), inserted into a larger tank (60 36 35 cm), with mirrors as the two longer walls and opaque screens as the shorter walls (see Fig. 1). The tank was lit from above by a neon lamp (18 W). Water was 25 cm high. Above the testing apparatus, a videocamera was mounted in order to videotape the fish behaviour. Each fish was tested singly, by placing it into the test apparatus and videorecording its behaviour for 10 min (for subsequent analysis, this period was split into two blocks of 5 min in order to check for variation in lateralization as a function of time; see below). Fish positions were then scored every 2 s and the frequency of use of the left/right monocular visual field was estimated on the basis of the fish angle with respect to the closest mirror (see Ref. [41] for details). An index of eye use was calculated as: [(frequency of right-eye use)/(frequency of right-eye use + frequency of left-eye use)] 100. Significant departures from chance level (50%) were estimated by one- or two-
Fig. 1. Schematic representation of the rectangular mirror test apparatus showing the position of the mirrors.
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
239
Fig. 2. Schematic representation of the quasi-circular mirror test, showing the position of the mirrors.
tailed one-sample t tests. Differences between species and between the first and the second 5 min were estimated by analysis of variance (ANOVA). 2.1.2.2. ‘‘Quasi-circular tank’’ mirror test. Testing was performed within a square-shaped tank (67 67 37.5 cm) within which a quasi-circular swim-way was inserted (Fig. 2). The outer wall of the swim-way was composed of a series of eight identical mirrors (36.5 26 cm) arranged in a circular fashion. At the junctions between pairs of mirrors, plastic green strips (1 15 cm) were located in order to avoid the formation of double-image reflections. The inner wall of the swim-way was formed by the same plastic material, with elements that corresponded to the mirrors but of reduced size (16.5 16.5 cm). Access to the swim-way was made possible through a central compartment with a small door (3.5 8.5 cm) that could be opened automatically by the experimenter pulling a thread, without disturbing the test fish. The apparatus was lit from above by four fluorescent lamps (15 W) square-shaped arranged. Above the testing apparatus, a videocamera was mounted in order to videotape the fish behaviour. Each fish was tested singly. It was first placed into the central compartment for 10 min in order to be accustomed to the environment. Then the door
was opened and the fish was allowed to enter the quasicircular swim-way. The fish behaviour was videorecorded for 10 min (for subsequent analysis, this period was split into two blocks of 5 min in order to check for variation in lateralization as a function of time; see below). Fish positions were then scored every 2 s and the frequency of use of the left/right monocular visual field was estimated on the basis of the fish angle with respect to the mirror, as in the previous experiment. An index of eye use was used identical to that employed with the rectangular tank. Significant departures from chance level (50%) were estimated by one-sample t tests. Differences between species and between the first and the second 5 min were estimated by ANOVA.
3. Results The results for the quasi-circular mirror test are shown in Fig. 3. An overall ANOVA with species as a betweensubjects factor and time (first 5 min vs. second 5 min) as a within-subjects factor was performed. The ANOVA did not reveal any significant difference between the five species [ F(4,86) = 0.71, n.s.]. On the other hand, the ANOVA revealed a significant effect of time
240
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
Fig. 3. Laterality index indicating preferences for left- and right-eye use (means ± S.E.M. are shown) during the first and second 5 min of the test in the five species of fish tested with the quasi-circular apparatus. The rightmost columns represent the combined data for the five species.
[ F(1,86) = 7.24, P =.009] without any Species Time interaction [ F(4,86) = 0.95, n.s.]. We performed a onesample (two-tailed) t test to check whether a significant preference for using the left or the right eye was apparent in the species studied for the overall period of 10 min. The t test revealed indeed a highly significant preference for using the left eye [t(92) = 3.35, P = .001]. However, as revealed by the significant main effect of time in the ANOVA, one-sample t tests restricted to the first 5 min showed a significant left-eye preference [t(92) = 3.97, P = .0001], whereas no preference appeared during the second 5 min [t(92) = 1.30, n.s.]. Fig. 4 shows the results obtained with the rectangular mirror test. An ANOVA with species (X. eiseni, G. holbrooki, and X. sarasinorum) as a between-subjects factor and time (first 5 min vs. second 5 min) revealed a significant main effect of time [ F(1,29) = 17.98, P = .0001] without any effect of species [ F(2,29) = 0.86, n.s.] or Species Time interaction [ F(2,29) = 0.84, n.s.]. There was a significant preference for using the left eye during the first 5 min of test [one-sample t test: t(31) = 4.67, P = .0001], but not during the second 5 min [t(31) = 1.42, n.s.]. In order to compare more directly these data with those obtained with the novel apparatus, an ANOVA with three factors was performed: species (X. eiseni, G. holbrooki, X. sarasinorum), time (first 5 min vs. second 5 min), and testing apparatus (rectangular vs. quasi-circular mirror test). The ANOVA did not reveal any significant heterogeneity associated with species [ F(2,63) = 0.19, n.s.] or apparatus [ F(1,63) = 3.17, n.s.], nor any significant inter-
action [Time Apparatus: F(1,63) = 0.24; Time Species: F(2,63) = 1.69; Apparatus Species: F(2,63) = 1.41; Time Apparatus Species: F(2,63) = 0.35]. The only statistically significant effect was that associated with time [ F(1,63) = 19.44, P =.0001]. We were concerned, however, with the fact that the variances in the two testing apparatus were not homogeneous (see below) and thus, the results of the ANOVA should be treated with caution in this case. Since the variances remained not homogeneous even after data transformation [Levene test: first 5 min, F(5,63) = 3.50, P = .007; second 5 min, F(5,63) = 7.25, P = .0001], we performed nonparametric tests. The Friedman ANOVA revealed a significant difference between the first and the second 5 min of test (c2 = 9.06, df = 1, P < .003), but the Kruskal – Wallis analysis showed that there were no differences associated with testing apparatus (first 5 min: c2 = 0.71, df = 1, P = n.s.; second 5 min: c2 = 0.39, df = 1, P = n.s.) or species (first 5 min: c2 = 2,30, df = 2, P = n.s.; second 5 min: c2 = 0.48, df = 2, P = n.s.). Thus, results with the quasi-circular mirror test fully confirmed those with the rectangular mirror test. In both tests, all species showed a significant left-eye preference during the first minutes of test. Subsequently, the eye preference vanished and fish resumed a more balanced left- and right-eye use. It should be noted, however, that results with the quasi-circular apparatus are less striking than those with the rectangular mirror apparatus (compare Figs. 3 and 4) due to a larger dispersion of the data with the former test. Variances in the quasi-circular mirror test
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
241
Fig. 4. Laterality index indicating preferences for left- and right-eye use (means ± S.E.M. are shown) during the first and second 5 min of the test in the three species of fish tested with the rectangular apparatus. The rightmost columns represent the combined data for the three species.
were higher than in the rectangular mirror test [Levene test: F(1,67) = 11.84, P = .001].
4. Discussion The results of the experiments showed that there was a strikingly similar pattern of lateralization across species and across the two different methods. The left eye was mainly used during scrutinizing of the fish’s own image in a mirror. This was apparent during the initial phase of test (first 5 min), after which the asymmetry disappeared. It is likely that habituation to the novel social stimulus (fish had no previous experience with mirrors and, therefore, are likely to have seen the image as a stranger conspecific) occurred after the first 5 min. These findings are also supported by independent evidence for a similar preferential left-eye use in a task (the detour test) involving inspection of natural conspecifics rather than of mirror images (though in this case, evidence was limited to a more restricted range of species). Bisazza et al. [4,5] showed that male mosquitofish G. holbrooki, faced with an obstacle (a barrier of vertical bars) behind which a sexual stimulus was visible (i.e., a group of females), preferentially circled around the obstacle in a leftward direction (thus, fixating the target with their right eye). The same leftward bias was observed with a simulated predator as a target. On the other hand, with social stimuli as target (i.e., conspecifics of the same sex), females
showed a consistent rightward bias, while there was no bias in males [41], which are not gregarious (which is also the reason why we used females in the experiments described here [8]). Similar asymmetries have been reported in Girardinus falcatus fish [3]. Thus, left-eye use seems to be specific of gregarious responses, for when stimuli provided by conspecifics activate sexual responses (as in the case of males tested with females as target in the detour task), the right eye is used instead. This suggests that it is the type of response that has to be performed (or the information processing that has to be carried on) and not the physical stimulus per se, which is important in determining the direction of lateralization. In fish, optic nerve axons, originating in retinal ganglion cells, cross completely at the optic chiasm [54]. Visual fibres from each eye project mainly to the optic tectum (actually, other distinct nuclear groups, nucleus geniculatus lateralis, nucleus praetectalis and nucleus corticalis appear to receive connections from the optic tract). Projections are mainly contralateral and transfer of information between the two halves of the brain is thought to be minimal [54]. It is likely, therefore, that preferential eye use is a behavioural manifestation of a different specialisation of the right and left side of the fish brain in the analysis of incoming visual information. This is supported by the fact that similar phenomena have been observed in a quite different test, the detour test (above), and that asymmetries in the detour test do correlate with preferences in eye use during monoc-
242
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
ular viewing [49]. Asymmetries at the more peripheral level, e.g., differences in visual acuity, are unlikely to be a satisfactory explanation of these data because the stimuli to be analysed in all these cases subtended very large visual angles and, most important, because in detour tests [3– 5] and in viewing tests [31,32,49], fish show different patterns of eye use depending on the (same-size) type of stimulus to be scrutinized. Obviously, we do not know exactly with what aspects of the stimulus lateralization is associated. It could be that lateralization is associated with species recognition. Alternatively, more subtle aspects might be involved, such as recognition of familiarity and novelty in social partners (i.e., individual recognition, which seems to be available in these species of fish). This awaits further research. Selective involvement of structures located in the right side of the brain in visual analysis of social stimuli has been widely described among vertebrates. It comprises responding to videotapes of conspecifics [29], face recognition [24], and facial expression of emotions in primates [26,28], recognition of familiar and unfamiliar faces in sheep [11,34], as well as agonistic responding towards conspecifics among reptiles [17,18], toads [36], and chicks [53], and conspecific recognition among birds [45,47,48]. With some caution, a case can be made for the maintenance of an invariant pattern of visual lateralization for the analysis of stimuli provided by conspecifics in all vertebrate species. In fish, comparative analyses within the same class is now extensive. Considering the previous data reported by Sovrano et al. [41] and the evidence reported here, there appears to be eight different species of fish all showing an identical left-eye preference during visual scrutiny of conspecifics. These species belong to five different orders; four orders belong to the modern teleosts and are representative of both Ostariophysi and Acanthopterygii, the two major superorders of Euteleostei. One species, G. petersii, belongs to the Osteoglossomorpha, which is considered an ancestral group of teleost fish [5– 7]. Two major issues remain to be addressed. The first refers to the neurobiological correlates of behavioural lateralization. Neuroanatomical asymmetries have been described in the nervous system of fish [25,33], but they seem to be mainly related to escape responses (e.g., asymmetries of Mauthner cells) rather than to processing of complex visual stimuli as conspecifics (see also Ref. [27]). The second issue refers to the advantages and disadvantages for animals with laterally placed eyes to exhibit such a striking difference of function between the two eyes (hemispheres) systems. The evidence reported here and in other similar studies suggests that fish (but also reptiles, amphibians, birds and, to some extent, mammals with laterally placed eyes; see Ref. [46] for a review) seem to actively use their left or right eye according to the nature of the task. Clearly, there should be important advantages associated with such extreme lateralization of function. There is now some indication of
what these advantages could be. Rogers [39] reported that strongly lateralized chicks detect a stimulus resembling a predator with shorter latency than weakly lateralized chicks. It has been shown that in cats reach durations are shorter for the preferred paw than for the nonpreferred paw; moreover, cats that are lateralized in this action tend to prefer their left paws and have shorter movement times than cats that do not exhibit lateralized reaching behaviour [20]. McGrew and Marchant [30] reported that wild chimpanzees showing stronger and more complete handedness are also more efficient at fishing for termites than those with incomplete handedness. Finally, Gu¨ntu¨rku¨n et al. [23] showed that an increase of visual asymmetry enhances success in visually guided foraging of pigeons. It is less clear, however, whether such advantages could be important enough to counterbalance the obvious ecological disadvantages associated with responding differentially to stimuli appearing on the left and on the right side of an animal’s midline. 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, in a natural environment these stimuli might happen to be located on either the left or the right side at random (e.g., see Ref. [39] for evidence of asymmetries in predator detection in chicks). Actually, a very recent study [53] has provided evidence that in birds things may be more complicated: domestic chicks (provided they are incubated in the dark) seem to exhibit complementary and opposite left – right specialisations for the lateral (monocular) and the frontal (binocular) hemifields, thus possibly compensating within each eye for the disadvantages associated with asymmetries in the use of the left and right eye. However, no evidence for similar phenomena has been observed in fish [49]. Note, however, that the supposed ecological disadvantages only operate if lateralization occurs at the population level. Asymmetries in the use of the eyes with an equiprobable distribution (50% of the animals favouring the left eye and 50% favouring the right eye) would not convey any possibility by prey/predators to exploit regularities associated with asymmetries, because no bias would be apparent at the population level. This raises a crucial question: if the computational advantages (mentioned above) associated with brain asymmetries can be apparent and effective even at the individual level, why then do so many vertebrates exhibit them at the population level (with the associated disadvantages in terms of predictability of behaviour)? We have suggested elsewhere that the response may lie in the peculiar ecological demands associated with living in groups [7,49] (see also Ref. [37]). Even in species with very primitive forms of sociality, behaviourally asymmetric organisms have to interact with each other and, as a result, disadvantages are likely to arise for an individual if the direction of its behavioural asymmetries is different from that of the majority of the other asymmetric individuals of the group. Not surprisingly, therefore, consistency in the pattern of direction of lateralization is observed when looking at social stimuli, i.e., when
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
interaction and coordination of behaviour with other individuals of the same species is crucial for responses such as courtship and predator evasion.
Acknowledgments We thank Silvia Brunelli and Maurizio Capocchiano for help in conducting the experiments. This research was founded by a MURST 40% grant.
References [1] Andrew RJ. The nature of behavioural lateralization in the chick. In: Andrew RJ, editor. Neural and behavioural plasticity. The use of the chick as a model. Oxford: Oxford Univ. Press, 1991. pp. 536 – 54. [2] Andrew RJ, Tommasi L, Ford N. Motor control by vision and the evolution of cerebral lateralization. Brain Lang 2000;73:220 – 35. [3] Bisazza A, De Santi A, Vallortigara G. Laterality and cooperation: mosquitofish move closer to a predator when the companion is on their left side. Anim Behav 1999;57:1145 – 9. [4] Bisazza A, Pignatti R, Vallortigara G. Detour tests reveal task- and stimulus-specific neural lateralization in mosquitofish (Gambusia holbrooki). Behav Brain Res 1997;89:237 – 42. [5] Bisazza A, Pignatti R, Vallortigara G. Laterality in detour behaviour: interspecific variation in poeciliid fish. Anim Behav 1997;54:1273 – 81. [6] Bisazza A, Rogers LJ, Vallortigara G. The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, amphibians, and reptiles. Neurosci Biobehav Rev 1998;22: 411 – 26. [7] Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G. Population lateralization and social behaviour: a study with sixteen species of fish. Laterality 2000;5:269 – 84. [8] Bisazza A, Facchin L, Pignatti R, Vallortigara G. Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual motivation. Behav Brain Res 1998;91:157 – 64. [9] Bisazza A, Cantalupo C, Robins A, Rogers L, Vallortigara G. Rightpawedness in toads. Nature 1996;379:408. [10] Bradshaw JL, Rogers LJ. The evolution of lateral asymmetries, language, tool use, and intellect. San Diego: Academic Press, 1993. [11] Broad KD, Mimmack ML, Kendrick KM. Is right hemisphere specialization for face discrimination specific to humans? Eur J Neurosci 2000;12:731 – 41. [12] Cantalupo C, Bisazza A, Vallortigara G. Lateralization of predatorevasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 1995;33:1637 – 46. [13] Clayton NS, Krebs JR. Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 1994;174: 371 – 9. [14] Cowell P, Denenberg V. Development of laterality and the role of corpus callosum in rodents and humans. In: Andrew RJ, Rogers LJ, editors. Comparative vertebrate lateralization. Cambridge: Cambridge Univ. Press, in press. [15] Cowell PE, Waters NS, Denenberg VH. The effects of early environment on the development of functional laterality in Morris maze performance. Laterality 1997;2:221 – 32. [16] Crowne DP, Novotny MF, Mier SE, Vitols RW. Spatial deficits and their lateralization following unilateral parietal cortex lesions in the rat. Behav Neurosci 1992;106:808 – 19. [17] Deckel AW. Laterality of aggressive responses in Anolis. J Exp Zool 1995;272:194 – 200. [18] Deckel AW. Effects of alcohol consumption on lateralized aggression in Anolis carolinensis. Brain Res 1997;756:96 – 105.
243
[19] De Santi A, Sovrano VA, Bisazza A, Vallortigara G. Mosquitofish display differential left- and right-eye use during mirror-image scrutiny and predator-inspection responses. Anim Behav 2001;61: 305 – 10. [20] Fabre-Thorpe M, Fagot J, Lorincz E, Levesque F, Vaucliar J. Laterality in cats: paw preference and performance in a visuomotor activity. Cortex 1993;29:15 – 24. [21] Gagliardo A, Ioale’ P, Odetti F, Bingman VP, Vallortigara G. Homing in pigeons: differential role of left and right hippocampal formation in the acquisition of the navigational map. Eur J Neurosci 2001;13: 1617 – 24. [22] Gu¨ntu¨rku¨n O. Avian visual lateralization: a review. NeuroReport 1997;8:3 – 11. [23] Gu¨ ntu¨ rku¨n O, Diekamp B, Manns M, Nottelmann F, Prior H, Schwarz A, Skiba M. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol 2000;10:1079 – 81. [24] Hamilton CR, Vermeire BA. Complementary hemispheric specialization in monkeys. Science 1988;242:1691 – 4. [25] Harris JA, Guglielmotti V, Bentivoglio M. Diencephalic asymmetries. Neurosci Biobehav Rev 1996;20:637 – 43. [26] Hauser MD. Right hemisphere dominance for the production of facial statement in monkeys. Science 1993;261:475 – 7. [27] Heuts BA. Lateralization of trunk muscle volume, and lateralization of swimming turns of fish responding to external stimuli. Behav Process 1999;47:113 – 24. [28] Hook-Costigan MA, Rogers LJ. Hand, mouth and eye preferences in the common marmoset (Callithrix jacchus). Folia Primatol 1995; 64:180 – 91. [29] Ifune CK, Vermeire BA, Hamilton CR. Hemispheric differences in split-brain monkeys viewing and responding to videotape recordings. Behav Neural Biol 1984;41:231 – 5. [30] McGrew WC, Marchant LF. Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 1999;40:509 – 13. [31] Miklosi A, Andrew RJ. Right eye use associated with decision to bite in zebrafish. Behav Brain Res 1999;105:199 – 205. [32] Miklosi A, Andrew RJ, Savage H. Behavioural lateralisation of the tetrapod type in the zebrafish (Brachydanio rerio). Physiol Behav 1998;63:127 – 35. [33] Moulton JM, Barron SE. Asymmetry in the Mauthner cells of the goldfish brain. Copeia 1967;836 – 7. [34] Peirce JW, Leigh AE, Kendrick KM. Configurational coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychologia 2000;38:475 – 83. [35] Rashid NY, Andrew RJ. Right hemisphere advantage for topographical orientation in the domestic chick. Neuropsychologia 1989;27: 937 – 48. [36] Robins A, Lippolis G, Bisazza A, Vallortigara G, Rogers LJ. Lateralized aggressive responses and hindlimb use in toads. Anim Behav 1998;56:875 – 81. [37] Rogers LJ. Laterality in animals. Int J Comp Psychol 1989;3:5 – 25. [38] Rogers LJ. Behavioral, structural and neurochemical asymmetries in the avian brain: a model system for studying visual development and processing. Neurosci Biobehav Rev 1996;20:487 – 503. [39] Rogers LJ. Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 2000;73:236 – 53. [40] Sergent J, Signoret J-L. Functional and anatomical decomposition of face processing: evidence from prosopagnosia and PET study of normal subjects. Philos Trans R Soc London Ser B 1992;335:55 – 62. [41] Sovrano VA, Rainoldi C, Bisazza A, Vallortigara G. Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish. Behav Brain Res 1999;106:175 – 80. [42] Tommasi L, Vallortigara G. Encoding of geometric and landmark information in the left and right hemispheres of the avian brain. Behav Neurosci, in press. [43] Tommasi L, Andrew RJ, Vallortigara G. Eye use in search is determined by the nature of the task in the domestic chick. Behav Brain Res 2000;112:119 – 26.
244
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
[44] Ulrich C, Prior H, Duka T, Leschchins’ka I, Valenti P, Gu¨ntu¨rku¨n O, Lipp H-P. Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav Brain Res 1999;104:169 – 78. [45] Vallortigara G. Right hemisphere advantage for social recognition in the chick. Neuropsychologia 1992;30:761 – 8. [46] Vallortigara G. Comparative neuropsychology of the dual brain: a stroll through left and right animals’ perceptual worlds. Brain Lang 2000;73:189 – 219. [47] Vallortigara G, Andrew RJ. Lateralization of response to change in a model partner by chicks. Anim Behav 1991;41:187 – 94. [48] Vallortigara G, Andrew RJ. Differential involvement of right and left hemisphere in individual recognition in the domestic chick. Behav Process 1994;33:41 – 58. [49] Vallortigara G, Bisazza A. How ancient is brain lateralization? In: Andrew RJ, Rogers LJ, editors. Comparative vertebrate lateralization. Cambridge: Cambridge Univ. Press, in press.
[50] Vallortigara G, Regolin L, Pagni P. Detour behaviour, imprinting and visual lateralization in chicks. Cognit Brain Res 1999;7:307 – 20. [51] Vallortigara G, Regolin L, Bortolomiol G, Tommasi L. Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behav Brain Res 1996;74:135 – 43. [52] Vallortigara G, Rogers LJ, Bisazza A, Lippolis G, Robins A. Complementary specializations of the right and left hemifield for predatory and agonistic behaviour in toads. NeuroReport 1998;9:3341 – 4. [53] Vallortigara G, Cozzutti C, Tommasi L, Rogers LJ. How birds use their eyes: opposite left-right specialization for the lateral and frontal visual hemifield in the domestic chick. Curr Biol 2001;11:29 – 33. [54] Vanegas H, Ito H. Morphological aspects of the teleostean visual system: a review. Brain Res Rev 1983;6:117 – 37. [55] Vermeire BA, Hamilton CR, Erdmann AL. Right-hemispheric superiority in split-brain monkeys for learning and remembering facial discriminations. Behav Neurosci 1998;112:1048 – 61.
Lateralization of response to social stimuli in fishes: A comparison between different methods and species Valeria Anna Sovranoa,*, Angelo Bisazzaa,1, Giorgio Vallortigarab a
b
Department of General Psychology, University of Padua, Via Venezia 8, 35131 Padua, Italy Department of Psychology and BRAIN Centre for Neuroscience, University of Trieste, Via S. Anastasio 12, 34123 Trieste, Italy Received 13 March 2001; received in revised form 20 April 2001; accepted 28 May 2001
Abstract We measured the time spent in monocular viewing during inspection of their own mirror images in females of three species of fish (Xenotoca eiseni, Gambusia holbrooki and Xenopoecilus sarasinorum) using a rectangular tank in which animals could observe their own reflections in two mirrors positioned along the major walls, and in females of five species of fish (X. eiseni, G. holbrooki, X. sarasinorum, Danio rerio and Gnatonemus petersii) using a quasi-circular tank in which fish could rotate clockwise or anticlockwise and observe their own reflections in a mirror positioned along the outer wall. Results revealed a consistent left-eye preference during initial sustained fixation in all species irrespective of the apparatus. However, in the quasi-circular tank, fish showed more variability of response. The asymmetry was apparent during the first 5 min of observation and tended to fade thereafter, probably as a result of habituation. These findings add to current evidence for a quite invariant pattern in the direction of lateralization in similar tasks in a variety of vertebrate species, with a preferential involvement of structures located to the right side of the brain in response to the viewing of images of conspecifics. D 2001 Elsevier Science Inc. All rights reserved. Keywords: Lateralization; Asymmetry; Social recognition; Right hemisphere; Fish
1. Introduction Research on animal lateralization is slowly moving from initial demonstrations of mere existence to investigations on proximate and ultimate causal mechanisms. We now know that behavioural lateralization is widespread in a variety of mammalian [10,14], avian [1,2,22,38,46], amphibian [9,36,52], reptilian [17,18], and fish [6,12] species. One interesting open issue is whether there is a fixed and invariant pattern in the direction of lateralization in the different species. Similarities in the direction of lateralization in different tasks among different species may be seen as evidence for possible homologies (see Ref. [49] for a discussion). But what is more important is the fact that if some ‘‘cluster’’ of information-processing mechanisms would appear consistently associated with the same side of the encephalon in * Corresponding author. Fax: +39-49-827-6600. E-mail addresses: [email protected] (V.A. Sovrano); [email protected] (A. Bisazza); [email protected] (G. Vallortigara). 1 Fax: + 39-49-827-6600.
otherwise very different species, that would provide clues to what may constrain the basic organization of the vertebrate nervous systems. There are indeed quite impressive suggestions of similarities in the direction of lateralization among vertebrates. One example concerns the selective involvement of the right side of the brain in spatial tasks. This has been largely documented in birds (i.e., chicks [35,42,43,50,51] and Parus [13]; but see Refs. [21,44] for a discussion of different spatial tasks) and in mammals [15,16]. Another example concerns the specialisation of the right hemisphere for face recognition in humans [40], which might be an elaboration of similar processes found in social recognition in nonhuman species. Sheep exhibit a lateral bias to the left visual field (right hemisphere) in visual recognition of familiar and unfamiliar faces [34]. Split-brain monkeys show similar specialisations of the right hemisphere to discriminate faces [24,55] and in birds the left eye seems to be involved in recognition of individual conspecifics [45,47,48]. Recently, evidence for a left-eye bias during scrutiny of conspecifics in some species of fish has been reported [41]
0031-9384/01/$ – see front matter D 2001 Elsevier Science Inc. All rights reserved. PII: S 0 0 3 1 - 9 3 8 4 ( 0 1 ) 0 0 5 5 2 - 2
238
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
(see also Refs. [3,19]). The basic finding was that species belonging to different families all showed a left-eye preference for looking at their own visual images in a mirror during a 5-min observation period (measures of eye use was confined to the lateral, monocular, visual field, which is known to project almost exclusively to the contralateral side of the nervous system; see Discussion for details of fish neuroanatomy). Although not particularly striking in strength when compared with other forms of human and nonhuman asymmetries, the lateralization in eye use was present at the population level and in the same direction in all the six species. More importantly, while most of the previous data concerned comparisons of animals of different taxonomic groups, here evidence arose from animals pertaining to the same class but different families. The aim of the present paper is threefold. Firstly, we wanted to check for the generality of the findings of Sovrano et al. [41] using a different experimental set up. Our original mirror test employed two parallel mirrors that generated a multiple-reflection phenomenon, so that the environment was very unusual for the fish with respect to the home-tank. Moreover, the fish was limited in its movement: when reaching one end of the mirror, it lost contact with its mirror reflection and was forced to move back and forth along the wall. Thus, we tried to develop a ‘‘quasi-circular’’ apparatus, with only one set of mirrors located on one wall so that the simple direction of circling, clockwise, and anticlockwise, could force (and reflect) preferential scrutinizing of the image using either the left or right eye. Secondly, we were interested to measure how preferential eye use changed with time. Does protracted exposure to the mirror image produce habituation and shift towards a balanced left- and right-eye use? Since we had available long-term videorecording of fish behaviour from previous experiments not analyzed yet, we could compare changes in eye use with time in both the ‘‘rectangular tank’’ and the ‘‘quasi-circular tank’’ mirror test. Finally, we extended the number of species analyzed. We tested in the novel apparatus three of the species already studied with the old apparatus (Xenotoca eiseni, Gambusia holbrooki
and Xenopoecilus sarasinorum) and two completely novel species (Danio rerio and Gnatonemus petersii).
2. Experiment 2.1. Materials and methods 2.1.1. Subjects Females of X. eiseni (n = 14), G. holbrooki (n = 16), X. sarasinorum (n = 7), D. rerio (n = 30), and G. petersii (n = 26) were used. Fish were kept in vegetation-rich (Ceratophyllum sp.) 120 – 150-l glass tanks, lit from above by fluorescent lamps (30 W) under a 14/10 light/dark period. Water temperature was maintained between 22C and 25C and fish were fed dry food twice a day. G. petersii was additionally fed with Chironomus larvae. 2.1.2. Procedure 2.1.2.1. ‘‘Rectangular tank’’ mirror test. The apparatus has been described in details elsewhere [41]. Testing was performed within a tank (44 22 30 cm), inserted into a larger tank (60 36 35 cm), with mirrors as the two longer walls and opaque screens as the shorter walls (see Fig. 1). The tank was lit from above by a neon lamp (18 W). Water was 25 cm high. Above the testing apparatus, a videocamera was mounted in order to videotape the fish behaviour. Each fish was tested singly, by placing it into the test apparatus and videorecording its behaviour for 10 min (for subsequent analysis, this period was split into two blocks of 5 min in order to check for variation in lateralization as a function of time; see below). Fish positions were then scored every 2 s and the frequency of use of the left/right monocular visual field was estimated on the basis of the fish angle with respect to the closest mirror (see Ref. [41] for details). An index of eye use was calculated as: [(frequency of right-eye use)/(frequency of right-eye use + frequency of left-eye use)] 100. Significant departures from chance level (50%) were estimated by one- or two-
Fig. 1. Schematic representation of the rectangular mirror test apparatus showing the position of the mirrors.
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
239
Fig. 2. Schematic representation of the quasi-circular mirror test, showing the position of the mirrors.
tailed one-sample t tests. Differences between species and between the first and the second 5 min were estimated by analysis of variance (ANOVA). 2.1.2.2. ‘‘Quasi-circular tank’’ mirror test. Testing was performed within a square-shaped tank (67 67 37.5 cm) within which a quasi-circular swim-way was inserted (Fig. 2). The outer wall of the swim-way was composed of a series of eight identical mirrors (36.5 26 cm) arranged in a circular fashion. At the junctions between pairs of mirrors, plastic green strips (1 15 cm) were located in order to avoid the formation of double-image reflections. The inner wall of the swim-way was formed by the same plastic material, with elements that corresponded to the mirrors but of reduced size (16.5 16.5 cm). Access to the swim-way was made possible through a central compartment with a small door (3.5 8.5 cm) that could be opened automatically by the experimenter pulling a thread, without disturbing the test fish. The apparatus was lit from above by four fluorescent lamps (15 W) square-shaped arranged. Above the testing apparatus, a videocamera was mounted in order to videotape the fish behaviour. Each fish was tested singly. It was first placed into the central compartment for 10 min in order to be accustomed to the environment. Then the door
was opened and the fish was allowed to enter the quasicircular swim-way. The fish behaviour was videorecorded for 10 min (for subsequent analysis, this period was split into two blocks of 5 min in order to check for variation in lateralization as a function of time; see below). Fish positions were then scored every 2 s and the frequency of use of the left/right monocular visual field was estimated on the basis of the fish angle with respect to the mirror, as in the previous experiment. An index of eye use was used identical to that employed with the rectangular tank. Significant departures from chance level (50%) were estimated by one-sample t tests. Differences between species and between the first and the second 5 min were estimated by ANOVA.
3. Results The results for the quasi-circular mirror test are shown in Fig. 3. An overall ANOVA with species as a betweensubjects factor and time (first 5 min vs. second 5 min) as a within-subjects factor was performed. The ANOVA did not reveal any significant difference between the five species [ F(4,86) = 0.71, n.s.]. On the other hand, the ANOVA revealed a significant effect of time
240
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
Fig. 3. Laterality index indicating preferences for left- and right-eye use (means ± S.E.M. are shown) during the first and second 5 min of the test in the five species of fish tested with the quasi-circular apparatus. The rightmost columns represent the combined data for the five species.
[ F(1,86) = 7.24, P =.009] without any Species Time interaction [ F(4,86) = 0.95, n.s.]. We performed a onesample (two-tailed) t test to check whether a significant preference for using the left or the right eye was apparent in the species studied for the overall period of 10 min. The t test revealed indeed a highly significant preference for using the left eye [t(92) = 3.35, P = .001]. However, as revealed by the significant main effect of time in the ANOVA, one-sample t tests restricted to the first 5 min showed a significant left-eye preference [t(92) = 3.97, P = .0001], whereas no preference appeared during the second 5 min [t(92) = 1.30, n.s.]. Fig. 4 shows the results obtained with the rectangular mirror test. An ANOVA with species (X. eiseni, G. holbrooki, and X. sarasinorum) as a between-subjects factor and time (first 5 min vs. second 5 min) revealed a significant main effect of time [ F(1,29) = 17.98, P = .0001] without any effect of species [ F(2,29) = 0.86, n.s.] or Species Time interaction [ F(2,29) = 0.84, n.s.]. There was a significant preference for using the left eye during the first 5 min of test [one-sample t test: t(31) = 4.67, P = .0001], but not during the second 5 min [t(31) = 1.42, n.s.]. In order to compare more directly these data with those obtained with the novel apparatus, an ANOVA with three factors was performed: species (X. eiseni, G. holbrooki, X. sarasinorum), time (first 5 min vs. second 5 min), and testing apparatus (rectangular vs. quasi-circular mirror test). The ANOVA did not reveal any significant heterogeneity associated with species [ F(2,63) = 0.19, n.s.] or apparatus [ F(1,63) = 3.17, n.s.], nor any significant inter-
action [Time Apparatus: F(1,63) = 0.24; Time Species: F(2,63) = 1.69; Apparatus Species: F(2,63) = 1.41; Time Apparatus Species: F(2,63) = 0.35]. The only statistically significant effect was that associated with time [ F(1,63) = 19.44, P =.0001]. We were concerned, however, with the fact that the variances in the two testing apparatus were not homogeneous (see below) and thus, the results of the ANOVA should be treated with caution in this case. Since the variances remained not homogeneous even after data transformation [Levene test: first 5 min, F(5,63) = 3.50, P = .007; second 5 min, F(5,63) = 7.25, P = .0001], we performed nonparametric tests. The Friedman ANOVA revealed a significant difference between the first and the second 5 min of test (c2 = 9.06, df = 1, P < .003), but the Kruskal – Wallis analysis showed that there were no differences associated with testing apparatus (first 5 min: c2 = 0.71, df = 1, P = n.s.; second 5 min: c2 = 0.39, df = 1, P = n.s.) or species (first 5 min: c2 = 2,30, df = 2, P = n.s.; second 5 min: c2 = 0.48, df = 2, P = n.s.). Thus, results with the quasi-circular mirror test fully confirmed those with the rectangular mirror test. In both tests, all species showed a significant left-eye preference during the first minutes of test. Subsequently, the eye preference vanished and fish resumed a more balanced left- and right-eye use. It should be noted, however, that results with the quasi-circular apparatus are less striking than those with the rectangular mirror apparatus (compare Figs. 3 and 4) due to a larger dispersion of the data with the former test. Variances in the quasi-circular mirror test
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
241
Fig. 4. Laterality index indicating preferences for left- and right-eye use (means ± S.E.M. are shown) during the first and second 5 min of the test in the three species of fish tested with the rectangular apparatus. The rightmost columns represent the combined data for the three species.
were higher than in the rectangular mirror test [Levene test: F(1,67) = 11.84, P = .001].
4. Discussion The results of the experiments showed that there was a strikingly similar pattern of lateralization across species and across the two different methods. The left eye was mainly used during scrutinizing of the fish’s own image in a mirror. This was apparent during the initial phase of test (first 5 min), after which the asymmetry disappeared. It is likely that habituation to the novel social stimulus (fish had no previous experience with mirrors and, therefore, are likely to have seen the image as a stranger conspecific) occurred after the first 5 min. These findings are also supported by independent evidence for a similar preferential left-eye use in a task (the detour test) involving inspection of natural conspecifics rather than of mirror images (though in this case, evidence was limited to a more restricted range of species). Bisazza et al. [4,5] showed that male mosquitofish G. holbrooki, faced with an obstacle (a barrier of vertical bars) behind which a sexual stimulus was visible (i.e., a group of females), preferentially circled around the obstacle in a leftward direction (thus, fixating the target with their right eye). The same leftward bias was observed with a simulated predator as a target. On the other hand, with social stimuli as target (i.e., conspecifics of the same sex), females
showed a consistent rightward bias, while there was no bias in males [41], which are not gregarious (which is also the reason why we used females in the experiments described here [8]). Similar asymmetries have been reported in Girardinus falcatus fish [3]. Thus, left-eye use seems to be specific of gregarious responses, for when stimuli provided by conspecifics activate sexual responses (as in the case of males tested with females as target in the detour task), the right eye is used instead. This suggests that it is the type of response that has to be performed (or the information processing that has to be carried on) and not the physical stimulus per se, which is important in determining the direction of lateralization. In fish, optic nerve axons, originating in retinal ganglion cells, cross completely at the optic chiasm [54]. Visual fibres from each eye project mainly to the optic tectum (actually, other distinct nuclear groups, nucleus geniculatus lateralis, nucleus praetectalis and nucleus corticalis appear to receive connections from the optic tract). Projections are mainly contralateral and transfer of information between the two halves of the brain is thought to be minimal [54]. It is likely, therefore, that preferential eye use is a behavioural manifestation of a different specialisation of the right and left side of the fish brain in the analysis of incoming visual information. This is supported by the fact that similar phenomena have been observed in a quite different test, the detour test (above), and that asymmetries in the detour test do correlate with preferences in eye use during monoc-
242
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
ular viewing [49]. Asymmetries at the more peripheral level, e.g., differences in visual acuity, are unlikely to be a satisfactory explanation of these data because the stimuli to be analysed in all these cases subtended very large visual angles and, most important, because in detour tests [3– 5] and in viewing tests [31,32,49], fish show different patterns of eye use depending on the (same-size) type of stimulus to be scrutinized. Obviously, we do not know exactly with what aspects of the stimulus lateralization is associated. It could be that lateralization is associated with species recognition. Alternatively, more subtle aspects might be involved, such as recognition of familiarity and novelty in social partners (i.e., individual recognition, which seems to be available in these species of fish). This awaits further research. Selective involvement of structures located in the right side of the brain in visual analysis of social stimuli has been widely described among vertebrates. It comprises responding to videotapes of conspecifics [29], face recognition [24], and facial expression of emotions in primates [26,28], recognition of familiar and unfamiliar faces in sheep [11,34], as well as agonistic responding towards conspecifics among reptiles [17,18], toads [36], and chicks [53], and conspecific recognition among birds [45,47,48]. With some caution, a case can be made for the maintenance of an invariant pattern of visual lateralization for the analysis of stimuli provided by conspecifics in all vertebrate species. In fish, comparative analyses within the same class is now extensive. Considering the previous data reported by Sovrano et al. [41] and the evidence reported here, there appears to be eight different species of fish all showing an identical left-eye preference during visual scrutiny of conspecifics. These species belong to five different orders; four orders belong to the modern teleosts and are representative of both Ostariophysi and Acanthopterygii, the two major superorders of Euteleostei. One species, G. petersii, belongs to the Osteoglossomorpha, which is considered an ancestral group of teleost fish [5– 7]. Two major issues remain to be addressed. The first refers to the neurobiological correlates of behavioural lateralization. Neuroanatomical asymmetries have been described in the nervous system of fish [25,33], but they seem to be mainly related to escape responses (e.g., asymmetries of Mauthner cells) rather than to processing of complex visual stimuli as conspecifics (see also Ref. [27]). The second issue refers to the advantages and disadvantages for animals with laterally placed eyes to exhibit such a striking difference of function between the two eyes (hemispheres) systems. The evidence reported here and in other similar studies suggests that fish (but also reptiles, amphibians, birds and, to some extent, mammals with laterally placed eyes; see Ref. [46] for a review) seem to actively use their left or right eye according to the nature of the task. Clearly, there should be important advantages associated with such extreme lateralization of function. There is now some indication of
what these advantages could be. Rogers [39] reported that strongly lateralized chicks detect a stimulus resembling a predator with shorter latency than weakly lateralized chicks. It has been shown that in cats reach durations are shorter for the preferred paw than for the nonpreferred paw; moreover, cats that are lateralized in this action tend to prefer their left paws and have shorter movement times than cats that do not exhibit lateralized reaching behaviour [20]. McGrew and Marchant [30] reported that wild chimpanzees showing stronger and more complete handedness are also more efficient at fishing for termites than those with incomplete handedness. Finally, Gu¨ntu¨rku¨n et al. [23] showed that an increase of visual asymmetry enhances success in visually guided foraging of pigeons. It is less clear, however, whether such advantages could be important enough to counterbalance the obvious ecological disadvantages associated with responding differentially to stimuli appearing on the left and on the right side of an animal’s midline. 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, in a natural environment these stimuli might happen to be located on either the left or the right side at random (e.g., see Ref. [39] for evidence of asymmetries in predator detection in chicks). Actually, a very recent study [53] has provided evidence that in birds things may be more complicated: domestic chicks (provided they are incubated in the dark) seem to exhibit complementary and opposite left – right specialisations for the lateral (monocular) and the frontal (binocular) hemifields, thus possibly compensating within each eye for the disadvantages associated with asymmetries in the use of the left and right eye. However, no evidence for similar phenomena has been observed in fish [49]. Note, however, that the supposed ecological disadvantages only operate if lateralization occurs at the population level. Asymmetries in the use of the eyes with an equiprobable distribution (50% of the animals favouring the left eye and 50% favouring the right eye) would not convey any possibility by prey/predators to exploit regularities associated with asymmetries, because no bias would be apparent at the population level. This raises a crucial question: if the computational advantages (mentioned above) associated with brain asymmetries can be apparent and effective even at the individual level, why then do so many vertebrates exhibit them at the population level (with the associated disadvantages in terms of predictability of behaviour)? We have suggested elsewhere that the response may lie in the peculiar ecological demands associated with living in groups [7,49] (see also Ref. [37]). Even in species with very primitive forms of sociality, behaviourally asymmetric organisms have to interact with each other and, as a result, disadvantages are likely to arise for an individual if the direction of its behavioural asymmetries is different from that of the majority of the other asymmetric individuals of the group. Not surprisingly, therefore, consistency in the pattern of direction of lateralization is observed when looking at social stimuli, i.e., when
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
interaction and coordination of behaviour with other individuals of the same species is crucial for responses such as courtship and predator evasion.
Acknowledgments We thank Silvia Brunelli and Maurizio Capocchiano for help in conducting the experiments. This research was founded by a MURST 40% grant.
References [1] Andrew RJ. The nature of behavioural lateralization in the chick. In: Andrew RJ, editor. Neural and behavioural plasticity. The use of the chick as a model. Oxford: Oxford Univ. Press, 1991. pp. 536 – 54. [2] Andrew RJ, Tommasi L, Ford N. Motor control by vision and the evolution of cerebral lateralization. Brain Lang 2000;73:220 – 35. [3] Bisazza A, De Santi A, Vallortigara G. Laterality and cooperation: mosquitofish move closer to a predator when the companion is on their left side. Anim Behav 1999;57:1145 – 9. [4] Bisazza A, Pignatti R, Vallortigara G. Detour tests reveal task- and stimulus-specific neural lateralization in mosquitofish (Gambusia holbrooki). Behav Brain Res 1997;89:237 – 42. [5] Bisazza A, Pignatti R, Vallortigara G. Laterality in detour behaviour: interspecific variation in poeciliid fish. Anim Behav 1997;54:1273 – 81. [6] Bisazza A, Rogers LJ, Vallortigara G. The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, amphibians, and reptiles. Neurosci Biobehav Rev 1998;22: 411 – 26. [7] Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G. Population lateralization and social behaviour: a study with sixteen species of fish. Laterality 2000;5:269 – 84. [8] Bisazza A, Facchin L, Pignatti R, Vallortigara G. Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual motivation. Behav Brain Res 1998;91:157 – 64. [9] Bisazza A, Cantalupo C, Robins A, Rogers L, Vallortigara G. Rightpawedness in toads. Nature 1996;379:408. [10] Bradshaw JL, Rogers LJ. The evolution of lateral asymmetries, language, tool use, and intellect. San Diego: Academic Press, 1993. [11] Broad KD, Mimmack ML, Kendrick KM. Is right hemisphere specialization for face discrimination specific to humans? Eur J Neurosci 2000;12:731 – 41. [12] Cantalupo C, Bisazza A, Vallortigara G. Lateralization of predatorevasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 1995;33:1637 – 46. [13] Clayton NS, Krebs JR. Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 1994;174: 371 – 9. [14] Cowell P, Denenberg V. Development of laterality and the role of corpus callosum in rodents and humans. In: Andrew RJ, Rogers LJ, editors. Comparative vertebrate lateralization. Cambridge: Cambridge Univ. Press, in press. [15] Cowell PE, Waters NS, Denenberg VH. The effects of early environment on the development of functional laterality in Morris maze performance. Laterality 1997;2:221 – 32. [16] Crowne DP, Novotny MF, Mier SE, Vitols RW. Spatial deficits and their lateralization following unilateral parietal cortex lesions in the rat. Behav Neurosci 1992;106:808 – 19. [17] Deckel AW. Laterality of aggressive responses in Anolis. J Exp Zool 1995;272:194 – 200. [18] Deckel AW. Effects of alcohol consumption on lateralized aggression in Anolis carolinensis. Brain Res 1997;756:96 – 105.
243
[19] De Santi A, Sovrano VA, Bisazza A, Vallortigara G. Mosquitofish display differential left- and right-eye use during mirror-image scrutiny and predator-inspection responses. Anim Behav 2001;61: 305 – 10. [20] Fabre-Thorpe M, Fagot J, Lorincz E, Levesque F, Vaucliar J. Laterality in cats: paw preference and performance in a visuomotor activity. Cortex 1993;29:15 – 24. [21] Gagliardo A, Ioale’ P, Odetti F, Bingman VP, Vallortigara G. Homing in pigeons: differential role of left and right hippocampal formation in the acquisition of the navigational map. Eur J Neurosci 2001;13: 1617 – 24. [22] Gu¨ntu¨rku¨n O. Avian visual lateralization: a review. NeuroReport 1997;8:3 – 11. [23] Gu¨ ntu¨ rku¨n O, Diekamp B, Manns M, Nottelmann F, Prior H, Schwarz A, Skiba M. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol 2000;10:1079 – 81. [24] Hamilton CR, Vermeire BA. Complementary hemispheric specialization in monkeys. Science 1988;242:1691 – 4. [25] Harris JA, Guglielmotti V, Bentivoglio M. Diencephalic asymmetries. Neurosci Biobehav Rev 1996;20:637 – 43. [26] Hauser MD. Right hemisphere dominance for the production of facial statement in monkeys. Science 1993;261:475 – 7. [27] Heuts BA. Lateralization of trunk muscle volume, and lateralization of swimming turns of fish responding to external stimuli. Behav Process 1999;47:113 – 24. [28] Hook-Costigan MA, Rogers LJ. Hand, mouth and eye preferences in the common marmoset (Callithrix jacchus). Folia Primatol 1995; 64:180 – 91. [29] Ifune CK, Vermeire BA, Hamilton CR. Hemispheric differences in split-brain monkeys viewing and responding to videotape recordings. Behav Neural Biol 1984;41:231 – 5. [30] McGrew WC, Marchant LF. Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 1999;40:509 – 13. [31] Miklosi A, Andrew RJ. Right eye use associated with decision to bite in zebrafish. Behav Brain Res 1999;105:199 – 205. [32] Miklosi A, Andrew RJ, Savage H. Behavioural lateralisation of the tetrapod type in the zebrafish (Brachydanio rerio). Physiol Behav 1998;63:127 – 35. [33] Moulton JM, Barron SE. Asymmetry in the Mauthner cells of the goldfish brain. Copeia 1967;836 – 7. [34] Peirce JW, Leigh AE, Kendrick KM. Configurational coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychologia 2000;38:475 – 83. [35] Rashid NY, Andrew RJ. Right hemisphere advantage for topographical orientation in the domestic chick. Neuropsychologia 1989;27: 937 – 48. [36] Robins A, Lippolis G, Bisazza A, Vallortigara G, Rogers LJ. Lateralized aggressive responses and hindlimb use in toads. Anim Behav 1998;56:875 – 81. [37] Rogers LJ. Laterality in animals. Int J Comp Psychol 1989;3:5 – 25. [38] Rogers LJ. Behavioral, structural and neurochemical asymmetries in the avian brain: a model system for studying visual development and processing. Neurosci Biobehav Rev 1996;20:487 – 503. [39] Rogers LJ. Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang 2000;73:236 – 53. [40] Sergent J, Signoret J-L. Functional and anatomical decomposition of face processing: evidence from prosopagnosia and PET study of normal subjects. Philos Trans R Soc London Ser B 1992;335:55 – 62. [41] Sovrano VA, Rainoldi C, Bisazza A, Vallortigara G. Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish. Behav Brain Res 1999;106:175 – 80. [42] Tommasi L, Vallortigara G. Encoding of geometric and landmark information in the left and right hemispheres of the avian brain. Behav Neurosci, in press. [43] Tommasi L, Andrew RJ, Vallortigara G. Eye use in search is determined by the nature of the task in the domestic chick. Behav Brain Res 2000;112:119 – 26.
244
V.A. Sovrano et al. / Physiology & Behavior 74 (2001) 237–244
[44] Ulrich C, Prior H, Duka T, Leschchins’ka I, Valenti P, Gu¨ntu¨rku¨n O, Lipp H-P. Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav Brain Res 1999;104:169 – 78. [45] Vallortigara G. Right hemisphere advantage for social recognition in the chick. Neuropsychologia 1992;30:761 – 8. [46] Vallortigara G. Comparative neuropsychology of the dual brain: a stroll through left and right animals’ perceptual worlds. Brain Lang 2000;73:189 – 219. [47] Vallortigara G, Andrew RJ. Lateralization of response to change in a model partner by chicks. Anim Behav 1991;41:187 – 94. [48] Vallortigara G, Andrew RJ. Differential involvement of right and left hemisphere in individual recognition in the domestic chick. Behav Process 1994;33:41 – 58. [49] Vallortigara G, Bisazza A. How ancient is brain lateralization? In: Andrew RJ, Rogers LJ, editors. Comparative vertebrate lateralization. Cambridge: Cambridge Univ. Press, in press.
[50] Vallortigara G, Regolin L, Pagni P. Detour behaviour, imprinting and visual lateralization in chicks. Cognit Brain Res 1999;7:307 – 20. [51] Vallortigara G, Regolin L, Bortolomiol G, Tommasi L. Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behav Brain Res 1996;74:135 – 43. [52] Vallortigara G, Rogers LJ, Bisazza A, Lippolis G, Robins A. Complementary specializations of the right and left hemifield for predatory and agonistic behaviour in toads. NeuroReport 1998;9:3341 – 4. [53] Vallortigara G, Cozzutti C, Tommasi L, Rogers LJ. How birds use their eyes: opposite left-right specialization for the lateral and frontal visual hemifield in the domestic chick. Curr Biol 2001;11:29 – 33. [54] Vanegas H, Ito H. Morphological aspects of the teleostean visual system: a review. Brain Res Rev 1983;6:117 – 37. [55] Vermeire BA, Hamilton CR, Erdmann AL. Right-hemispheric superiority in split-brain monkeys for learning and remembering facial discriminations. Behav Neurosci 1998;112:1048 – 61.