Lateralization in chicks and hens: new evidence for control of response by the right eye system

~

Pergamon

PII: S0028-3932(97)00108-5

Neuropsychologia, Vol. 36, No. 1, pp. 51-58, 1998 ((~ 1998 Published by Elsevier Science Ltd. All rights reserved Printed in Great Britain 0028-3932 / 98 $19.00 + 0.00

Lateralization in chicks and hens: new evidence for control of response by the right eye system R. M c K E N Z I E , *

R . J. A N D R E W * t

a n d R. B. J O N E S : ~

*Sussex Centre for Neuroscience, School of Biological Sciences, University of Sussex, Brighton BN1 9QG, U.K.; SDivision of Environment and Welfare, Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, U.K.

(Received 7 April 1997; accepted 10 July 1997) Abstract--Domestic chicks show marked lateralization of visually evoked behaviour: left eye use is associated with, and has advantage for, the detection of novelty; right eye use is associated with the use of selected cues to determine what response should be given. Experiments undertaken to see how far such lateralization might be a transient feature of development showed similar patterns in both adults and chicks: (i) use of the right, but not the left, frontal field allowed the inhibition of pecks at a familiar social partner; (ii) in distant viewing, there was spontaneous preference for more use of the left eye when the social partner was familiar rather than unfamiliar. The chick data, in particular, support the hypothesis that the visual system fed by the right eye is especially competent in the control of response. This is shown by the ability of birds that are using the right eye to inhibit approach to an entirely novel potential social partner, and inhibit pecks at a familiar partner. The resemblances between chick and hen are sufficient to show that the basic adult pattern is already present in the young chick: the various developmental changes in features of lateralization, such as days of bias to control by one or other hemisphere, thus do not cause the appearance of the adult pattern. © 1998 Published by Elsevier Science Ltd. All rights reserved Key Words: asymmetric eye use; right eye inhibition.

Introduction

stimulus which they are viewing [6]. Direct insult to one or other cerebral hemisphere has confirmed for some of these tasks (e.g., pebble floor [19]) that the asymmetry of performance depends on particular specializations of the structures, which receive the direct visual input from the contralateral eye. Differences have also been described between chicks using the fight and the left eye in sexual and aggressive behaviour: following treatment with testosterone, such behaviour is more strongly evoked when the chick is using the left eye [18]. A largely unanswered question is the way in which cerebral lateralization present in the chick changes, during development, to the adult condition. Asymmetries of the thalamo-telencephalic visual projections are marked in young chicks, but reduce or disappear during later development, as do differences between the performance of right- and left-eyed chicks in one test (learning to inhibit pecks at pebbles, when these are presented mixed with food [17, 20]). This has been thought [18] to imply that at least some asymmetries in visually evoked behaviour in chicks are generated by these anatomical asymmetries, and are as a result transient features of the behaviour of the young chick. This proposition has been weakened by the recent

Cerebral lateralization is very well developed in the young domestic chick, apparently as a result of differing specialization of the right and left sides of the brain. In brief, left eye use (right hemisphere) facilitates analysis based on all the properties of an object or experience, including its spatial context, whilst right eye use (left hemisphere) makes more likely the selection of specific cues, which can be used to decide what response is appropriate [2]. The evidence for this, in the chick, has come from a variety of tasks: learning to choose food rather than pebbles (pebble floor [12]); choosing between a partner or a fellow [22], or between a model of the type with which the chick lives and a transformation of it [23]; the degree of dishabituation produced by different types and degree of change in a familiar small target [2]; and ability to use distant cues in order to find a point in space [16]. Chicks also spontaneously use either the right or left eye in lateral fixation, according to the nature of the tAddress for correspondence: Sussex Centre for Neuroscience, University of Sussex, Brighton BN1 9QG, U.K.; email: bafe8Ca~central.sussex.ac.uk; fax: 44 (0)1273 678535. 51

52

R. McKenzie et al./Lateralization in chicks and hens

finding (Rogers and Andrew, in preparation) that the condition which generates the asymmetry in the visual pathway, namely illumination of only the right eye during late foetal life (a natural consequence of light entering through the shell and the fact that the foetus holds its head so that the right eye faces outwards and the left is shielded), is not necessary to produce the usual asymmetries in visually evoked behaviour. It now seems more likely that the transient asymmetry in the visual pathways is a stage in development which generates persistent asymmetries (perhaps in the forebrain), whose consequences for behaviour are yet to be identified. It is also worth noting that auditory and olfactory lateralization have both been demonstrated in young chicks [13, 24]; it is not clear that asymmetries of visual pathways can play any part in their generation. In addition, the cerebral lateralization, which is present in young chicks, is itself probably necessary for a number of steps in the development of behaviour. A series of age-dependent shifts in bias to control by one or other hemisphere occur during the first 2 weeks of life: thus (for example) bias is to the left hemisphere on day 8 and to the right hemisphere on days 10-12. It has been argued [1] that the days of marked bias allow learning which is particularly relevant to one or other hemisphere to take place. It is thus important on a variety of grounds that the patterns of adult lateralization in fowl be properly understood, as the final goal towards which the chick is developing. Two studies show that lateralization is certainly present in hens: higher levels of aggressive behaviour occur in hens when the left, rather than the right, eye is in use [18]. Hens that respond to a playback of an aerial predator alarm call by rolling their head to one side to look up are more likely to use their left eye for this purpose [7]. One of the most studied lateralized abilities of young chicks is the recognition of social partners. This ability has recently been examined in adults [4, 5], resulting in the interesting suggestion that here recognition of fellows only occurs when close-up binocular views are possible. This is consistent with earlier work [3], using photographic images, which suggested that hens discriminate between individuals visually, using cues from the facial region (which may be clearly visible only when close). In the chick [23], distinctions between strangers and partners, in choice tests, in which the objects to be discriminated (chicks or models) are initially at distances of about 20 cm, are made only when the chick is able to use its left eye. It is likely that this is part of a more general ability of the right hemisphere (in the chick as in humans) to hold detailed records of complex stimuli, and to use them to detect novelty. On the other hand, chicks prefer to use their right lateral visual fields, when inspecting potential new social partners (e.g., the first sight of a hen) at comparable distances [6]. There are thus two immediate problems: (i) chicks clearly differentiate between partner and stranger at a distance, but hens may

not; (ii) if chicks are incompetent in choosing between partner and stranger when using the right eye, why should they prefer to use it when viewing a novel potential partner? We present here data which allow us to compare visual lateralization in similar tests, in chicks and in adults. Issue (i) was resolved, in that hens proved, like chicks, to behave differently to strangers and partners, even at a distance. The more fundamental issue (ii: the reasons for right eye use) was also resolved (see General Discussion).

Experiments with hens Methods

Thirty-six ISA Brown hens (a medium-hybrid strain originally derived from a Rhode Island Red x Rhode Island White cross) were obtained as chicks from a commercial source (Isa Poultry Services, Peterborough, U.K., which also supplied the chicks that were used in later experiments). The hens were housed at the Roslin Institute, first in brooders and then in rearing cages. At approximately 18 weeks they were transferred in pairs to cages (60 cmx 45 cm x 45 cm, length x breadth x height), distributed across all tiers of a three-tier battery. These cages had wire fronts and sides, so that there was some opportunity to see birds in other cages on either side, and to see those at a greater distance by catching sight of heads put out of cage fronts. Only the cage partner could be seen at close quarters, and full social interaction was possible only with the partner. Birds wore coloured leg rings and numbered wing tags. Food and water were available ad libitum. Tests were carried out in a separate room. Two cages (43 cmx 37.5 cm × 47 cm), each containing a single hen at test, were placed so that the front of that containing the viewing hen was separated by 1.2 m from the side of that containing the hen which was being viewed (stimulus hen). The minimal viewing distance was thus a little greater than 1.2 m. The cage housing the test hen was covered with hardboard, a centrally placed hole in the front of which gave the hen its only opportunity to look out to see the stimulus hen. When the viewing hen had her head out, the stimulus hen was clearly and continuously visible through the side of its cage. It is likely that the stimulus hen could sometimes also be seen through the hole when the head was not out. Cages were made of l-cm vertical steel rods, set 7 cm apart. At approximately 43 weeks of age the hens were accustomed to the test cage, and the general surroundings of the test room, by two 3-hr sessions during the course of the week preceding testing. The hens were alone in the test room, the cage which at test would contain the stimulus hen being empty. Food (trough at front of cage) and water (nipple drinkers at rear of cage) were available ad libitum. The sides, but not the front of the cage, were covered by hardboard panels during the first session. During the second, the front was also covered by the panel (with a central spyhole), which was present at test. Tests (44weeks of age) lasted 10 min, with a second hen in the stimulus cage, which was either the partner or a stranger. The latter was chosen so as to have had minimal opportunity for visual interaction with the test hen: it was usually from a different cage row (and then never from a cage immediately above or below that of the test hen); when from the same row it was from a cage at least three cages away. The viewing hen was recorded with a video camera placed directly above the spyhole. Each hen was tested twice, once with the partner and once with a stranger, in a balanced pseudo-random order.

R. McKenzie et a/./Lateralization in chicks and hens The duration of time during viewing (defined as periods when the head was out of the cage aperture), with the left and the right eye turned towards the stimulus hen, was measured from the video recordings, together with time spent turned to the back of the cage (and so definitely not seeing the other hen). Asymmetry of viewing was measured by an index (time of left viewing/time of left and right viewing). This index was used in an analysis of variance (ANOVA; Factors= Partner/Stranger and Order of testing). Significance of bias to the use of the right or left eye within a group of birds was assessed by t-tests, comparing time using the right and left eye within each individual. All significance levels in pairwise tests were two-tailed. The main question of the study was whether right/left differences were present, so that these were pre-planned comparisons.

Experiment 1. Viewing partners and strangers Results

More time was spent facing the front than in facing the rear when the partner was visible (Fig. 1A; t = 2 . 9 3 , P = 0.006); a similar trend, which was present when the stranger was present, was not significant (t = 0.92). There were no significant differences in the time spent viewing partner and stranger (112.0_+30.7sec for partner; 107.8 _+ 24.4 sec for stranger). There was no effect o f order o f test on asymmetry of viewing [on left use index; time for left eye/time for left and right eye: F(1,22) = 0.01; NS]. However (Fig. I B), the two conditions of viewing differed significantly (comparison o f left use index for partner and stranger: t = 3.69, P = 0 . 0 0 3 ) . W h e n viewing their partner, hens showed significant bias to use o f the left eye ( n = 13; t = 2 . 4 4 , P = 0 . 0 3 1 ) , whereas there was a non-significant bias in the opposite direction (t = - 1.49, P = 0.16) when viewing the stranger.

53

were drawn by adult hens between partner and stranger only at much shorter distances (perhaps 30 cm, or even less). However, her measure was entirely different from ours, namely distance at which a clear choice of familiar partner was made, when the hen was faced with a single point (the end o f a partition), at which it must choose whether to a p p r o a c h one or other hen. In addition, our hens had to distinguish one partner from any other individual, whereas Dawkins' hens were faced with the more difficult task of distinguishing any one o f seven companions from a genuine stranger. It is also possible that hens take little care about how close they come to other hens, even t h o u g h these have been recognized, until they are almost within pecking range. It is worth noting that, in our experiments, all or almost all hens used both eyes at some point in viewing. The data therefore do not prove that only with the left eye can a bird be identified as a stranger, although they are consistent with such a hypothesis. The significant preference for viewing the partner with the left eye, and the absence or reversal of this pattern for the stranger, provides a clear point of comparison with chicks.

Experiment 2. Occlusion of visual fields The evidence that left eye use facilitates aggressive response in both chicks and adults (Introduction) suggested a second approach, which would examine behaviour at much closer quarters. In an earlier study with adults [18], blinkers were used which obscured only the frontal field, and this procedure was followed here.

Discussion

Methods

It is clear that stranger and partner are treated differently during viewing from a distance o f a b o u t 1.2 m (or a little more). Dawkins [4] found evidence that distinctions

The same 36 hens were used. Blinkers were attached to latex fittings, which were made in advance to fit one of three sizes of hen beak, whilst leaving the external nostrils quite free. A 2ram nylon nut was attached to the top of each fitting, and a 2-

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PARTNER

0.6

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0.4

0.2

100

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0 FACE FRONT

FACE REAR

Fig. 1. The mean time (+S.E.) spent in facing the front or rear of the viewing cage (A) and the mean index of left eye use (left/left + right; B) are shown for hens viewing a partner or a stranger.

54

R. McKenzie et al./Lateralization in chicks and hens

cm white plastic circle was attached to the nut by a nylon bolt. This allowed some adjustment of the exact position of the circle (the 'blinker') after mounting on the hen's bill. This was done with low odour non-irritant glue (Loctite low odour), whilst the hen was gently but firmly restrained by an assistant. Any hen whose blinker became detached during the 20 min allowed between attachment and test, which the hens spent singly in carrying boxes, was excluded from test. Birds were tested in pairs, in a cage l m × 0.45 m x 0.45 m, made of 4-cm wire mesh. The floor was 0.6 m above the ground. The cage was surrounded by white plastic shower curtains, forming a featureless enclosure 3 m square. Video recordings were made simultaneously from above and from one side. Both members of each pair were treated in the same way (i.e. right, left or neither frontal field obscured). The aim was to test all birds with both the partner and a stranger. We succeeded in testing in this way five birds with left frontal field in use, five with the right in use and 10 with no blinkers. All pecks, apart from ones directed at the blinker of the other bird, were recorded. Encounters were carefully watched, so that hens could be separated at once if fighting began; this was necessary only once.

P = 0.006], which was due in part to low pecking at the partner by R F but not L F [restriction to R F vs LF: F ( 1 , 8 ) = 14.66, P = 0 . 0 0 5 ; Fig. 2].

Discussion

Rogers [18] f o u n d more aggression in L F hens. However, the tests were carried out in established social groups (14 hens in each). O u r data too would show higher rates o f pecking in L F hens were we to lump pecks at partners with pecks at strangers. We suggest that, in established social groups, most hens are equivalent to 'partners' in the sense that pecks at them are suppressed m o s t o f the time, and that the elevation o f aggressive responses reported by Rogers [18] in hens within such groups represents failure to inhibit pecks at 'partners'.

Experiments with chicks Results

When both frontal fields were in use (Bin) more pecks were directed at the stranger than the partner (Fig. 2; n = 10; t = 4.45, P = 0.0016). N o clear distinction could be drawn in our data between investigatory and aggressive pecking; most pecks were relatively gentle. Pecking rates were in general considerably lower for birds with only one frontal field in use. Despite this, birds with the right frontal field (RF) in use showed the same significant asymmetry as Bin, with R F pecking the stranger more than the partner ( n = 5 ; t = 2 . 8 1 , P = 0 . 0 4 8 ) . Birds with the left frontal field (LF) in use showed no hint o f any difference between pecking at stranger and partner (n = 5; t=-0.79, P = 0 . 4 7 ) . A n A N O V A (Eye by Stranger/Partner) showed a significant difference between the three eye conditions in the way in which the pecks were distributed across stranger and partner [F(2,17)= 7.11,

40 STRANGER 09

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PARTNER

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A l t h o u g h a wide range o f behaviours are lateralized in chicks, experiments closely comparable with those described above for hens had not been performed previously. Two are reported below.

General methods

Chicks (ISA Brown) were housed singly, on removal from the hatcher or on arrival from the hatchery, in cages (17cm x 25cm × 20 cm). These were painted matt grey and illuminated and warmed from above by 40-W tungsten lamps (240 V, run at c. 180 V). Food (starter mash) and water were available ad libitum.

Experiment 3. viewing of imprinting object It was already k n o w n that chicks preferentially use the right eye when viewing a live adult hen for the first time [6], but it was not certain how far this represented the effect of strong releasers presented by the hen as against its novelty per se. Experiment 3 provides data for viewing an imprinting object before and after prior exposure to the object. The object was thus exactly the same for all tests, so that differences in eye use are not caused by the presence or absence o f particular releasers.

20

I.M In

Method

Z

0

BIN

RF

LF

Fig. 2. The mean number ( + S.E.) of pecks which were directed at a stranger or a partner are shown for hens using both eyes (BIN), the right frontal field (RF) or the left frontal field (LF).

Male and female chicks (M and F) from three batches of eggs were hatched in darkness in individual compartments in an incubator (35-38°C). Within 24 hr of hatching they were housed singly (General Methods). In the case of one treatment (exposed: E), a red table tennis ball was suspended at about eye level in the centre of the cage by a fine thread, so that it moved readily when touched by the chick. Such balls had been shown to be very attractive to chicks as social companions in prior

R. McKenzie et al./Lateralization in chicks and hens work [23]. A number of durations of exposure were used (1, 2, 3 and 4 hr), but no differences due to length of exposure were found, and the data from all exposed groups (E) were therefore combined. The other treatment (naive: N) had no ball. Resulting group sizes were n = 25, 22, 54. 48 for NM, NF, EM and EF respectively. At test, which occurred at the end of day 1, each chick was placed in the centre of a straight runway (61.2cmx 20.5cm x 30.5cm: length by width by height) with grey walls, at one end of which was suspended a red ball, like that present in home cages. Each test lasted 3.5 min and was video-recorded from above. Latency to move, head position during the last 15 sec before setting off in directed locomotion towards the ball, and distance from the ball in successive 30sec periods were measured. Head angle in relation to an imaginary line, connecting the chick's head with the ball, was measured by superimposing a computer-generated cursor on the midline of the head, as seen in the video recording. On a scale running from 0' (directly facing the ball) round through 9 0 (left side of head at right angles to the ball), 180~(facing directly away) and 27ff (right side of head at right angles to the ball), we used 2070° as representing left eye use and 290-340 c~as right eye use. The use of 20-70 ° was based on the finding [6] that the two main lateral fixation positions of the head were centred on 35c and 63'~. Binocular fixation was taken to lie between 339' and 19:.

Results Only females showed a clear bias to the use of one eye; a sex difference of this sort was expected from earlier work [6]. N females used the right eye markedly more than the left, whilst E females used right and left more nearly equally (Fig. 3). E and N males showed no significant bias to the use of either eye. Binocular fixation was in general used less than either right or left fixation, and did not differ much between groups. As a result of the differences in the use of left and right eyes, in an A N O V A (Angle by Experience by Sex) there was a significant main effect associated with head position [right,

55

left or binocular, 'Angle': F(2,208)= 28.53, P < 0.001] and significant interactions [Angle by Experience: F(2,208) = 10.01, P<0.001; Angle by Sex: F(2,208)=6.65, P=0.002; Angle by Sex by Experience: F(2,208) = 3.47, P = 0.033]. The interactions associated with Experience were due to females [Experience by Angle, restricted to females: F(2,96)= 14.21, P<0.001], and stemmed from the differential use of the right eye in N, but not E, females [right vs left in N females: F(1,14) = 25.87, P < 0.001]. Sex differences were also clear in readiness of approach and closeness of association with the ball. When mean distance from the ball in each of the seven 30-sec periods from start to 3.5min was analysed (Fig. 4), E animals spent more time overall near the ball, particularly late in the test [Experience by Time Segment: F(6,863)=5.36, P < 0.001]. Sex differences were concentrated early in the test, and as a result there was a significant interaction [Sex by Time Segment: F(6,836)=2.68, P=0.014]. This was largely due to special features of the second time segment: N F showed an initial large decrease in distance, similar to that shown by experienced birds (EF and EM). Only thereafter did N F delay any further approach, so that their mean distances came to be the same as those of the other naive group, NM. At the same time, N F scores diverged markedly from those of EF, over the period from 30 to 120sec. As a result, restrictions to pairwise comparisons (Table 1) showed that significant differences between E and N chicks were present in males from the second segment onwards, but in females only from the third onwards. In the second segment, in N groups males were further away than females, whereas the reverse was true for E groups. In the third, fourth and fifth segments all significant sex differences reflected a general tendency in both E and N groups for males to be at shorter distances than females.

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Fig. 3. The mean time (±S.E.) spent viewing an imprinting object with the left eye (LE), the right eye (RE) or both eyes (BIN) is shown for male or female (M, F) chicks, which have either already been exposed to the object (experienced: E), or which are seeing it for the first time (naive: N).

i

i

L

i

i

i

i

0

30

60

90

120

150

180

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Fig. 4. The mean distance (_ S.E.) from the imprinting object is shown for successive time blocks of 30 sec during an exposure of 3.5 min (0 = block beginning at 0 sec). Four groups of chicks are shown: N, naive; E, experienced; M, male; F, female.

56

R. McKenzie et al./Lateralization in chicks and hens Table 1. Analysis of variance for distance from ball: restrictions within the ANOVA. Time segment (sec) 0-29 30-59 60-89 90-119 120-149 150-179 180-209

N males/N females

E males/E females

1.07 3.91 * 4.03* 0.05 5.38* 0.09 0.63

0.12 5.21 * 2.13 3.94* 0.01 0.10 0.12

E males/N males 1.60 9.79"* 6.07** 23.34*** 4.98* 9.19"* 10.59"*

E females/N females 0.13 1.27 9.60** 5.33* 20.84*** 10.61"* 5.31"

F values obtained as the result of restrictions, within an overall ANOVA of distance from the ball, to pairwise comparisons, are shown for each 30-sec time segment from the beginning to the end of the test. Significance levels are shown as: *P < 0.05; **P < 0.01; ***P < 0.001. Degrees of freedom for N (naive) males vs N females, E (exposed) males vs E females, E males vs N males and E females vs N females were, respectively: 1,45; 1,99; 1,76; 1,69.

Discussion The odd group out, both in eye use in viewing and in readiness to approach the imprinting object, is thus N females. This group shows an early decrease of distance, which is identical with that shown by E females; this is probably due to a proportion of birds taking the decision to begin approach without much attempt to examine and assess the ball. The divergence of slope between the curves for N and E females, thereafter, is due to a large proportion of N females delaying any further approach until the penultimate and final time segments. In other words, N females strongly inhibit close approach until they have thoroughly examined the ball. We suggest that the N females are inhibiting close approach until they come to a clear decision that the ball is a potential social partner. This would agree with the results of another similar study (McKenzie, unpublished observations), in which a proportion of male chicks did not approach the ball at all during test. Those which approached showed predominantly left eye viewing, and those which did not showed predominantly right eye viewing. Thus, when males do inhibit approach in sustained fashion, they also use the right eye preferentially. The data reported here are consistent with those for chicks viewing a hen for the first time [6]; in this case too the right eye was used to view an intrinsically attractive but quite unfamiliar potential social partner. Again, the bias was much clearer in females. It is usual for female chicks to show much clearer patterns of eye use in viewing than males. This has been argued [2] to reflect a greater likelihood in females that control by one or other hemisphere will persist, once begun. The sex differences in approach behaviour reported here could be caused in a similar way: more effective left hemisphere control in females might not only be revealed by right eye use, but might also allow better control of approach in N females. (Note that N females take an initial decision to begin approach sooner than N males, but then inhibit further approach over the period from 30 to 120sec.) In N males, shifts in control

between the hemispheres may result both in less clear bias to use of one eye and to relative failure to inhibit approach. Finally, it is relevant that Japanese Quail chicks, housed in groups of three, discriminated in a choice test between a cagemate and a stranger, each visible at the opposite ends of a runway and each at a distance of about 70 cm [10]. Choice (as opposed to asymmetries of viewing) at a considerable distance thus occurs in chicks of a related species, as well as in domestic chicks [23].

Experiment 4. Use of frontal fields in chicks The finding (Experiment 2) that in hens use of the right, but not the left, frontal visual field produced differences in response to partners and to strangers was unexpected. It offered a new approach to the question: how far do chick and adult fowl show similar lateralization?

Method Male chicks (n = 12) were housed singly on arrival from the hatchery on the second day of life. Conditions were as in Experiment 1. On day 5 they were deprived of food and water for 1 hr in preparation for ether anaesthesia. Once unconscious, the upper surface of the bill was carefully cleaned with a pad moistened with IMS to remove any grease. A holder (a half section of a small plastic tube, about the shape of the bill) was attached with Loctite low-odour adhesive. A nylon nut had already been attached to the upper surface of the tube. The chicks were placed in a warmed container under careful observation for about 10 min, by which time all were fully recovered. They were then returned to their home cage for about 2 hr, when testing began. Just before test a circular light plastic blinker (2 cm diameter) was attached by a small nylon bolt to the nut in such a way (Experiment 2) that either the right or the left frontal field was blocked. The test chick was then placed with another chick (a stranger) in a cage similar to the home cage. After a settling period of 30 sec, all pecks at the stimulus chick were recorded for 120 sec. After 30 min the test was repeated with the other frontal field covered; the conditions right frontal or left frontal visual field in use (RF and LF) were administered in a balanced

R. McKenzie et al./Lateralization in chicks and hens pseudo-random order. Eight birds were successfully tested under both conditions; the other four lost the holder prior to one or other test.

Results and discussion

Pecks were more numerous in the RF condition. The index (pecks in RF/pecks in R F + p e c k s in LF) was 0.65_+0.04, which differed significantly from random (n=8; t=3.48, P=0.01). The basic finding of the hen study was thus replicated in chicks (admittedly male, not female). Again, strangers are pecked more in the RF than the LF condition. Our findings, here and in Experiment 2, suggest that the greater intensity of agonistic behaviour, which has been found in chicks and adult fowl to be associated with right hemisphere involvement, may not be entirely due to motivational differences between the hemispheres (such as are suggested by the depression of distress behaviour by right, but not left, amygdalar lesions in the chick [14]). Instead (or in addition), hemispheric differences in the analysis of perceptual input may be important, with left visual systems distinguishing sharply between what is a stranger and so to be pecked, and what is not (General Discussion).

General discussion Hens and chicks thus do show similar patterns of lateralization. This is clearer for the tests involving occlusion of one or other frontal field, in which the test objects were in both cases conspecifics. Here both hens and chicks inhibited pecks at partners when using the right frontal field, but pecked partners freely when using the left frontal field. In the case of the tests of viewing from a distance, the stimuli were conspecifics for the hens, but models for the chicks; further, for naive chicks the model was not simply a transformation of familiar conspecifics, but an object of a kind never seen before (and so very novel, as well as attractive as a social partner). Both hens and chicks showed the same direction of change in eye use when 'stranger' and partner were compared. However, significant deviation from equal use of the two eyes was present in hens when viewing the partner (left lateral field use), but in chicks when viewing the model for the first time ('stranger': right lateral field use). A first question is: are the patterns of lateralization suggested by distant viewing and by close frontal response fundamentally different or are they similar in essentials? There is evidence [8] that, in birds with laterally placed eyes (as are those of domestic fowl), the use of lateral visual fields (e.g., when viewing social partners from a distance) involves only one of the two main visual projection routes, the retino-thalamic route which feeds the Wulst in the forebrain. In contrast, the use of the

57

binocular field in close-up inspection largely depends on the other visual projection, the retino-tectal, which continues on to different forebrain destinations. It would therefore be possible, if unexpected, for the two visual systems to show different lateralization, which is what, on the face of it, the data suggest: if it is assumed that in distant viewing the eye is used which allows a stranger to be identified as such, then this is the left eye. However, when the use of the left frontal field is forced by occlusion, no distinction is made between stranger and partner. The alternative hypothesis is that both types of test actually reveal the same basic pattern of hemispheric specialization. Taken as a whole, the published findings for the chick [2] suggest that the visual systems fed by the left eye ('left eye system': LES; presumably predominantly right, rather than left hemisphere) detect, and are affected by, change in almost any property of a previously experienced stimulus, including its spatial context. In brief, the LES is interested in, and detects, novelty. The right eye system (RES) often ignores change by which the LES is affected. As a result, the RES will treat as equivalent a range of variations of an object of which it has had extensive experience. On the other hand, when a particular cue is consistently associated with reinforcement (food, ill taste), the RES draws markedly more consistent distinctions than does the LES. Taken together, these properties of the RES suggest the formation of categories of stimuli, with which an appropriate response is associated. The present findings are the first, using transformations of social partners, in which situations were used which strongly called for response. The new findings are (i) that right eye use appears when approach is being inhibited because of the novelty of the stimulus object, and (ii) that when use of the right frontal field is forced, there is differential control of pecking at stranger and partner, which is absent for the left frontal field. These are in fact consistent with earlier work: in both cases, use of the RES goes with control of response on the basis of what is perceived. The data for viewing in hens suggest that, when there is no strong need for control of response, the left eye is used for distant viewing of an object like a familiar conspecific. This may be a particular example of a more general phenomenon: the use of the LES because of its special ability to examine all the detailed properties of a complex stimulus. Support for the hypothesis that there is a general pattern of lateralization in the chick is provided by studies using other sensory modalities. (1) Right nostril input (reaching the right hemisphere) causes chicks to respond to changes in scent of the model social partner, whereas these are ignored with left nostril input [24]. This is comparable to the interest of the left, but not right, eye in change in a particular visual feature of the model [23] (2) Chicks turn the left ear to a completely familiar hen cluck to which they are fully attached [13], just as they use the

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R. McKenzie et al./Lateralizationin chicks and hens

left eye for a partner. They tend to use the right ear when first exposed to the sound of clucking, just as was found here for eye use to the first sight of a potential social partner. The hypothesis which has just been set out has much in common with that advanced for human perception by Warrington [25], by which the right hemisphere uses purely perceptual properties to assess similarity between stimuli, but the left hemisphere tends to use function (i.e. the purposes for which the stimuli might be used) as well. An instructive comparison is possible with the lateralization of facial recognition in humans and other primates. Right hemisphere advantage for the recognition of familiar faces (i.e. ones seen at least once before) is clear for rhesus monkeys [9], whilst current opinion [21] stresses the special involvement of right hemisphere structures in this task in adult humans. However, one important exception is right visual field advantage for the recognition of 'famous faces', where particular salient features may be used in recognition, rather than overall configuration [11]. Categorization of conspecifics by fowl may show similar shifts of hemisphere advantage, according to whether perceptual analysis requires consideration of many detailed features, or the selection of particular cues so as to assign an animal to a category like 'partner: not to be pecked'. In conclusion, the basic pattern of lateralization appears to be very similar in chick and hen. Events in development, like days of strong bias to control by one or other hemisphere [1, 2] or transient asymmetry in the retino-thalamic route to the Wulst, are not involved in the generation of the basic pattern. The transient asymmetry may be instead involved in the generation of sex differences in later lateralization, since it is less marked in females [15].

8.

9. 10.

11. 12. 13.

14.

15.

16. 17. 18. 19.

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