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International Journal of Comparative Psychology
Title
Laterality in Animals
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https://escholarship.org/uc/item/9h15z1vr
Journal
International Journal of Comparative Psychology, 3(1)
ISSN
0889-3667
Author
Rogers, Lesley J.
Publication Date
1989
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The International Journal of Comparative Psychology, Vol. 3, No. 1, Fall 1989
LATERALITY IN ANIMALS
Lesley J. Rogers
University of New England
We now know that laterality in various forms is acharacteristic
of awide range of species, and that it apparently developed very early
in evolution. Yet, some hundred years had to elapse after the discov-
ery that there was lateralization, or asymmetry, for control of speech
in the human brain, before any earnest attempts were made to dis-
cover or recognise the presence of laterality in nonhuman species (see
Robinson, Becker &Camp, 1983). The reason for this delay appears to
have been the belief that lateralization of brain function was achar-
acteristic unique to the human species, placing our species above all
other species.
This belief had been preceded by awell-developed mythology sur-
rounding the sinistral-dextral dichotomy of handedness in humans
(Corballis, 1983, pp. 1-9), and the belief that dextrality was also a
uniquely human characteristic. It has been argued that shared tool
use by humans caused laterality of limb use and, in turn, specializa-
tion of the left hemisphere for language (Frost, 1980; Bradshaw &
Nettleton, 1982).
Thus, the population bias in handedness in humans was seen to
be intimately related to our superior ability to use tools, and the pop-
ulation bias in lateralization of function in the cerebral hemispheres
was seen to be the basis of our superior ability for language. Not
surprisingly, these unique attributes afforded to the human species
were reluctantly relinquished by many psychologists, some (e.g. Levy,
1974, 1979) clinging to them well after lateralization of function in
the nervous system had been clearly demonstrated in more than one
nonhuman species, in particular for control of singing in song-birds
(Nottebohm, 1971; see later).
Address correspondence to Lesley J. Rogers, Physiology Department, University of
New England, Armidale, NSW 2351, Australia.
©1989 Human Sciences Press
THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
LATERALITY OF LIMB USE
When in the 1950s and 1960s psychologists first set about look-
ing for laterality* in nonhuman species, their aim was to see if they
could find evolutionary evidence for asymmetry in humans. It is
therefore not surprising that they chose to look for evidence of hand-
edness in primates. The overall conclusion drawn from alarge num-
ber of studies was that nonhuman primates do not have handedness
like that of humans (e.g. Warren, 1958; Brookshire &Warren, 1962;
or summarised in Corballis, 1983, pp. 113-116; Walker, 1980, pp.
348-351 and Warren, 1980, pp. 535-554). Although individual pri-
mates were found to show apreference for using one hand, in contrast
to the human species, there was no overall bias in handedness at the
population level, and it was generally considered that the individual
lateralities in hand use were artifacts of the methods used to test the
animals (Warren, 1980).
This view that nonhuman species lacked apopulation bias in lat-
erality of limb use was reinforced by Collins' (1975) report that mice
tested in atask requiring them to reach into atube to obtain afood
reward showed paw preferences as individuals but, as reported for
nonhuman primates, there was no population bias of "pawedness".
Moreover, raising the mice in right- or left-biased worlds was found to
influence the distribution of paw preferences in the expected direc-
tion, confirming that experience is afactor influencing preference for
limb use.
Arecent report by MacNeilage, Studdert-Kennedy and Lindblom
(1987) has, however, taken issue with the earlier reports of lack of
handedness in nonhuman primates and, on re-examination of the
data, the authors have reached the conclusion that there is more than
simply suggestive evidence indicating that anumber of species of
macaques have aleft-hand preference (see Ward, 1989, for asum-
mary of reports of left-hand bias in prosimians). For primates in gen-
eral, the authors propose that there is aleft-hand preference for visu-
ally guided reaching movements and aright-hand preference for
manipulation of objects. The remnants of this division of labour be-
tween hands may still be evident in humans despite our right-hand-
edness, as there is some evidence that dextrals performing atask re-
*It should be noted that the terms laterality and asymmetry are used inter-
changeably when referring to functional differences between the left and right sides,
but asymmetry is the term used for structural differences between the sides. This arti-
cle will keep to the use of the term laterality unless there is aclear left-right structural
difference involved.
LESLEY J. ROGERS
quiring fast reaching for avisual target are more accurate than when
using the left-hand (Guiard, Diaz &Beaubaton, 1983).
It is not my aim to discuss the relative merits of this particular
theory. The data for handedness in primates are still amatter of con-
troversy (see the peer review section following MacNeilage et al.,
1987). If the earlier researchers had been able to move further away
from the human species and look for laterality of limb use in birds,
their search would have been more fruitful, and just as shattering for
the belief that laterality of limb use at the population level was
unique to humans and possibly caused by shared tool use. In anum-
ber of species of parrots and cockatoos there is apopulation bias in
"footedness", as strong as that of handedness in humans.
Friedman and Davis (1938) reported left-footedness for manipu-
lating food objects in several species of African parrots. Even though
the sample sizes in this study were very small, it is important to note
that this report was overlooked by those researchers looking for lat-
erality in nonhuman species and focussing on primates. Australian
cockatoos and parrots also have footedness for manipulating food ob-
jects (Rogers, 1981; and see Table 1). Astrong bias for left-footedness
was found in eight of the nine species scored. The exception was
Platycercus elegans, the crimson rosella, which showed right-footed-
ness.
Footedness appears to occur only in those avian species which use
their feet in feeding. Pigeons do not manipulate food objects with
their feet, and Giintiirkun, Kesch and Delius (1988) have recently
reported the absence of footedness in pigeons tested by sticking a
piece of tape on the tip of the beak and scoring the foot used in the
first attempt to remove it (see Table 1). They found no bias in foot use
at either the population or individual level. This lack of footedness in
pigeons is species rather than task specific: they tested asmall num-
ber of parrots on the same task and found the preferred foot used to
remove the tape was consistent with their footedness for manipula-
tion of food objects. Ducker, Luscher and Schulz (1986) have observed
right-footedness (100%) in gold finches, Carduelis carduelis, tested on
atask requiring the birds to open doors and catches using the beak
and afoot in order to obtain afood reward. These data support the
general hypothesis that limb use preferences occur only in species
which use their limbs for manipulative activities (Walker, 1980).
We therefore decided to test this hypothesis using aspecies of
parrot which does not manipulate objects with its feet. Budgerigars
were tested for foot use in removal of apiece of sticky tape from the
beak (Workman &Rogers, in preparation; see Table 1). Nine individ-
uals were scored for amean of 20 trials each. They showed no footed-
ness either at the population level or as individuals. This supports the
THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
TABLE 1
Footedness in Birds.
LESLEY J. ROGERS
hj^othesis that laterality in limb use occurs only when the feet are
used to manipulate objects.
Yet, contrary to this hypothesis we have recently found footed-
ness in aspecies which does not use its feet to manipulate objects.
Chickens (Gallus gallus) do not use their feet to pick up and manipu-
late food or other objects, but they frequently scratch the ground
when searching for food. Workman and Rogers (in preparation) scored
the first foot used to rake the ground at the beginning of about of
ground scratching. Six animals were scored for 40 scratching bouts
each. Though both feet are used in this behaviour, there was asignifi-
cant tendency to initiate about of ground scratching by using the
right foot (68 ±.03% right-footedness, mean and standard error;
p<.05). When 10-day old chicks were tested on the task requiring
removal of sticky tape from the beak astronger right-foot bias was
found (84%; p<.01; the first foot chosen to scratch the tape was
scored, thus giving one score per individual, n=37). Apparently, it is
not manipulative ability alone which confers footedness on avian spe-
cies, but also active use of the feet in feeding or searching for food.
The fact that chickens show right footedness in searching for food
is not insignificant as they have dominance of the right eye in tasks
requiring them to search for food and to perform visual discrimina-
tion learning. By testing chickens monocularly on a task requiring
search for food grains Andrew, Mench and Rainey (1982) and Zappia
and Rogers (1987) have shown that the right eye learns to discrimi-
nate grains from small pebbles more rapidly than does the left eye.
Also chickens trained binocularly on avisual discrimination task
have dominance of the right eye for recall of the task (Gaston &Gas-
ton, 1984). Given this dominance of the right eye in searching for food
and the fact that chickens have laterally placed eyes with only a
small area of binocular overlap, it makes logical sense that chickens
have right footedness for initiating scratching of the ground to expose
grains of food.
The pigeon has the same lateralization of eye use in visual dis-
crimination learning as does the chicken (Giintiirkiin, 1985), but it
does not have footedness and it does not use the feet to scratch the
ground while feeding. This suggests that footedness (in both feeding
and non-feeding tasks) in avian species may have developed sec-
ondarily to lateralization of visual functions at the perceptual level,
and only in species which actively use their feet in feeding, either to
manipulate the food or to uncover it by scratching the ground.
In other words, if the feet are used in feeding, laterality of foot
use may occur as aresult of the constraints placed upon it by lateral-
ization in perceptual or cognitive processes linked to either eye.
If one tentatively considers extending this hypothesis to mam-
malian species, it may be argued that handedness followed on from
10 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
the presence of laterality at the cognitive or perceptual level of brain
organisation, rather than it being an antecedent of the latter, as im-
plied by McNeilage et al. (1987) and as stated by Kimura (1979) and
Frost (1980) (see later for evidence of lateralization of cognition in
mammalian species).
Unfortunately, we know nothing as yet of lateralization of func-
tion in the forebrain of parrots or cockatoos, except that Amazona
amazonica, which is 75% left-footed (Friedman &Davis, 1938), does
not have lateralization of control of vocalisation (Nottebohm, 1976b).
Nevertheless, it is highly likely that parrots and cockatoos do have
laterality for other forebrain functions. Zebra finches, for example,
have no, or possibly only slight, laterality for control of their vocalisa-
tions (Nottebohm, personal communication) but they show strong
functional laterality for copulation responses: the male views the fe-
male with his right eye when performing courtship behaviour (Work-
man &Andrew, 1986). The right footedness of Platycerus elegans may
indicate adifferent, if not inverted, laterality at higher levels of cen-
tral processing in this species.
With the development of greater manipulative ability (e.g. with
the evolution of the opposable thumb in primates) laterality of limb
use, though perhaps originally developed for feeding, would become
manifest in arange of activities, including tool use. As primates be-
came more able to adopt an upright posture they needed to use the
originally non-specialised (right) fore-limb less often for supporting
the body. MacNeilage et al. (1987) argue that this may have altered
the evolutionary course of handedness, as the right hand could now
take over and specialise for manipulation while the left remained spe-
cialised for visually guided reaching. In birds there is no possibility
for simultaneous use of both limbs to "handle" an object as one limb is
always needed to support the body. Thus, in birds the foot first spe-
cialised to hold food may be retained for all manipulative functions.
So saying, one must recognise that the question as to why some spe-
cies are left-footed and others right-footed remains open. It may per-
haps depend on the particular direction of laterality in the perceptual
processes used in feeding behaviour in the given species or, indeed, in
the given individual. Alternatively, it may depend on the type of
searching strategy which the particular species utilises in feeding.
Andrew, Mench and Rainey (1982) have found that the left eye of the
chicken is specialised for analysis of the spatial position of objects,
whereas the right eye is specialised for discriminating and categoris-
ing objects, particularly food versus non-food, irrespective of their po-
sition in space. Left-footedness may occur in species in which foraging
involves greater use of spatial cues rather than detailed discrimina-
tion of food objects from the background, and vice versa for right-
footed species.
LESLEY J. ROGERS 11
LATERALITY OF COGNITIVE FUNCTION
It is in perceptual and cognitive functioning that we find the
clearest examples of laterality in animals at the population level. In
Japanese macaques the left hemisphere is specialised for processing
their species-specific vocalisations (Peterson, Beecher, Zoloth, Moody
&Stebbins, 1979). Denenberg (1981) has shown that rats have lat-
eralization of "affective behaviour", measured in terms of taste aver-
sion and muricide. The data suggest that the right hemisphere is
more fearful than the left, and that the left hemisphere can inhibit
this aspect of functioning in the right (Denenberg &Yutzey, 1985).
Denenberg's extensive studies on laterality in rats have led him to
conclude that the right hemisphere of this species is specialised for
"strong emotional" behaviours and some spatial processes (Denen-
berg, 1984b).
In aseries of experiments testing rats in operant conditioning
tasks Bianki (1983, 1988) has demonstrated that the left hemisphere
is specialised for processing sequentially presented visual stimuli
while the right is specialised for processing simultaneously presented
visual stimuli. Bianki's findings are strikingly reminiscent of the lat-
eralized organisation present in humans.
These lateralities of hemispheric functions in rats are correlated
with asymmetries in the structure of the cortex and in the cellular
densities. In male Long-Evans rats most areas of the cortex are
thicker on the right side than the left (Diamond, 1984), and this
greater thickness results from having ahigher number of both neuro-
nal and glial cells (McShane et al., 1988), although it is not known
whether, or how, these structural differences pertain to functional
lateralization.
It should be noted again that this population bias in cortical lat-
erality in rats is not manifest in "pawedness" at the population level,
although there is at least one motor output pattern which shows a
population bias. Rats handled in early life show aleft side bias in the
direction in which they make their first move when placed in the
open field (Sherman, Garbanati, Rosen, Yutzey &Denenberg, 1980).
Intact, non-handled rats show no spatial bias, but ablation of the left
hemisphere generates aleft-side bias while ablation of the right gen-
erates aless marked right-side bias. Hence, Sherman et al. (1980)
deduced that handling in early life produces aright hemispheric dom-
inance, and so unmasks population laterality in the direction of mov-
ing off in the open field.
The direction of the first move made in the open field is not re-
lated to turning behaviour in rats, as studied by Glick (see Glick,
1983, and Glick &Shapira, 1985). Glick has looked at turning or cir-
cling behaviour which occurs in apreferred direction in the Individ-
12 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
ual either spontaneously at night or after treatment with drugs such
as amphetamine or apomorphine. Examination of agroup of over 600
rats revealed that 54.8% circled to the right and this was calculated
to be asignificant population bias (Glick 1983, p. 18), although it is
by no means an impressively sized bias. Ross, Glick and Meibach
(1981) and Denenberg et al. (1982) have shown asimilarly sized sig-
nificant population bias in the direction in which neonatal rats hold
their tails, the actual direction of the bias depending on both the sex
and strain of the rats.
The direction of circling in an individual correlates with the rela-
tive concentrations of dopamine in the striata on the left and right
sides of the brain: the rats rotate contralaterally to the side with the
higher dopamine level. Moreover, tail posture in neonates predicts
both the rotational bias and dopamine asymmetry (Rosen, Finkle-
stein, Stoll, Yutzey &Denenberg, 1984). Pawedness can be generated
at the individual level by conditioning, and there is some suggestion
that in this case it correlates with laterality in dopamine levels
(Schwarting, Nagel &Huston, 1987). Dopamine levels are higher in
the amygdalae ipsilateral to the paw used in the task. It would be
interesting to know how this relates to the direction of turning. That
is, whether the direction of rotation is also changed by this condition-
ing process.
Thus, in rats there are individual lateralities at one level of brain
organisation (in the striata and amygdalae) and apopulation bias at
another level of organisation (cortex). Different types, degrees, and
directions of asymmetry occur in different regions of the brain. There
is, however, no obvious hierarchical organisation as to which form of
laterality occurs at the various levels of complexity in processing be-
cause, like the cortex, the hypothalamus also displays laterality of
functioning at the population level. Implantation of oestradiol into
either the left or right side of the hypothalamus of neonatal female
rats causes different effects on sexual behaviour in adulthood (Nor-
deen &Yahr, 1982). Implanting oestradiol into the ventromedial nu-
cleus on the left side of the hypothalamus was found to suppress lor-
dosis by amean of approximately 35%, while implants in the right
ventromedial nucleus had no effect on this behaviour. Implants of
oestradiol into the preoptic area on the right side of the hypo-
thalamus elevated mounting by atwo-fold factor, while implanting
the equivalent region on the left side had no effect.
The hypothalamus of the rat also has laterality for control of hor-
monal output from the pituitary (Bakalkin et al. 1984). In Wistar
rats, the right side of the hypothalamus has ahigher concentration of
luteinizing hormone releasing factor; in an albino rat strain it is the
other way around.
LESLEY J. ROGERS 13
Many of the earlier concepts of lateralized brain function incorpo-
rated the idea that it was present only in the cortex and required a
corpus callosum to interconnect the two hemispheres so that one
hemisphere (the left in most cases) could suppress the other (see Gaz-
zaniga, 1974; Denenberg, 1981). Gazzaniga and Le Doux (1978) postu-
lated that evolution of the corpus callosum was essential for the ap-
pearance of laterality in the brain. They based their argument on
empirical evidence that lateralization of language in humans does not
develop until the fibres in the corpus callosum are fully myelinated
(Gazzaniga, 1974). It is not difficult to see that their general hypoth-
esis for the presence or absence of laterality is human-centred and
based on the original premise that laterality is unique to humans and
their capacity for language. Denenberg (1981) extrapolated this idea
to include all mammalian brains and developed amodel to explain
his data for laterality in rats (see earlier), involving suppression of
the right hemisphere by the left via the corpus callosum. Berrebi et
al. (1988) have now found evidence that handling increases the size of
the corpus callosum in male rats aged 110 days, which certainly sup-
ports arole for the corpus callosum in functional laterality at the
level of the cortex since, as discussed previously, handling unmasks
laterality in the direction of moving off in the open field. Neverthe-
less, laterality in the hypothalamus cannot easily be tied to the
corpus callosum unless the laterality in the hypothalamus is confer-
red upon it by higher centres in the cortex.
Evidence of laterality in the avian brain conclusively shows that
the corpus callosum is not necessary for asymmetry to occur, as there
is no corpus callosum in the avian brain. Pathways do cross from left
to right in the avian brain in the supra-optic decussation and the
tectal posterior and anterior commissures but these are small path-
ways. Also the supra-optic decussation does not connect homologous
regions of the brain, the latter being the essential property of the
corpus callosum and its chief attribute thought to be used by one side
to inhibit the other and so generate functional lateralization.
The avian forebrain has some fine examples of laterality. In a
number of species of song-birds, singing is controlled by the left hemi-
sphere (in chaffinches, Nottebohm, 1971; in crowned sparrows, Not-
tebohm, 1976a; and in canaries, Nottebohm, 1977). Lesions of the hy-
perstriatum ventrale, pars caudalis (HVc) on the left side eliminate
singing, whereas lesions of the right HVc have no effect. This striking
finding has been widely quoted in terms of its analogy to the human
condition with language on the left side, particularly given the paral-
lels which have been drawn between the "syntactical" structure of
bird song and human language. Yet, there is adistinct difference be-
tween the two systems. There are anatomical asymmetries associated
14 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
with the functional laterahzation of language/speech in humans, but
no structural asymmetries are present in the centres controlling sing-
ing in the song-birds.
In humans the region involved in speech comprehension (Wer-
nicke's area) is larger on the left side (Geschwind and Levitsky,
1968), and damage to this area in adults leads to aphasia with the
right side being unable to take over to produce speech. In contrast,
birds have the full complement of structures which control singing on
both sides of the brain. If the left HVc of canaries is lesioned in one
reproductive season no singing will occur in that season, but in the
next season the right HVc takes over and the full song repertoire is
regained. It is not known how much, if any, of the previous season's
song is retained. The function of the right HVc in an intact brain is
not known. Perhaps it is used in analysis and comprehension of the
songs of other birds, or in storing amemory of the individual's own
song. Given the absence of acorpus callosum interconnecting homolo-
gous regions in the forebrain, one wonders how the left HVc sup-
presses the right HVc in the intact brain. Also why does the right
HVc remain suppressed for the rest of the singing season when the
left is lesioned? In other words, when the left HVc has been lesioned,
why is there adelay until after the sex steroid hormone levels have
subsided and re-elevated before the right HVc can take over and con-
trol singing? Elevated testosterone levels permit neurogenesis in the
adult canary brain (Nottebohm, 1987, 1989), and this neural plas-
ticity is clearly necessary for the right HVc to assume control of sing-
ing after lesioning the left. Possibly rising levels of testosterone at
the beginning of the reproductive season are essential to trigger the
combined processes of song production and neural plasticity. There
are many interesting questions yet to be answered. It should be noted
that in chaffinches, which unlike canaries do not embellish their song
repertoire each season, the right HVc does not take over the control of
song after the left HVc is lesioned (Nottebohm, 1987). Canaries are,
according to Nottebohm, "open-ended learners" which retain neural
and functional plasticity in adulthood, while chaffinches are "critical-
period learners" which lose and never regain the ability to add to
their repertoire.
As mentioned briefly before, the chicken (Gallus gallus) brain
has laterality for anumber of functions. Our original studies revealed
laterality by injecting the protein synthesis inhibitor, cycloheximide
(CXM) into either the left or right forebrain hemisphere in early life.
Treatment of the left produced apermanent deficit in the ability to
learn atask requiring the chick to discriminate between grains of
food and small pebbles adhered to the floor (the 'pebble floor task')
and retarded habituation to both visual and auditory stimuli (Rogers
&Anson, 1979). Treatment of the right hemisphere did not affect
LESLEY J. ROGERS 15
these behaviours. These results were subsequently confirmed by test-
ing uninjected chicks monocularly. The avian nervous system has an
anatomical feature which makes it admirably suited to studying lat-
erality; viz. the optic nerves decussate completely so that the primary
visual connections go only to the contralateral side of the brain
(Cowan, Adamson &Powell, 1961). Thus monocular testing achieves
the same unilateral input to the brain as does the complicated ta-
chistoscopic presentation to humans of stimuli placed in the extreme
peripheral fields of vision. In this respect, the bird brain may be con-
sidered as a "split-chiasma" mammalian brain.
When tested monocularly on the 'pebble floor' visual discrimina-
tion task, young male chicks using the right eye learn as well as
binocularly tested controls, but in those tested using the left eye
learning is retarded (Mench &Andrew, 1986; Zappia &Rogers,
1987). By the age of 23 days post-hatching this laterality in perform-
ing the pebble floor task has disappeared as both eyes now learn well
(Rogers, 1990b).
The presence of this functional lateralization for visual discrimi-
nation learning in young male chicks correlates with astructural
asymmetry in the visual projections from the thalamus to the visual
Wulst, or hyperstriatum, of the forebrain (Boxer &Stanford, 1985;
Rogers &Sink, 1988). The left side of the thalamus, which receives
input from the right eye only, sends projections to hyperstriata on
both sides of the forebrain. The right side of the thalamus, which
receives input from the left eye only, projects to the right hyper-
striatum but very few projections cross over to go the hyperstriatum
on the left side. This better connectivity of the right eye to both sides
of the hyperstriatum may well explain its superior performance in
visual discrimination learning. By the beginning of the third week of
life post-hatching the projections from the right side of the thalamus
to the left hyperstriatum have developed and there is no longer any
asymmetry in the organisation of these thalamofugal visual path-
ways. The loss of this structural asymmetry parallels the loss of func-
tional laterality in visual learning ability on the pebble floor, sug-
gesting adirect connection between the two.
Newly hatched female chicks have no asymmetry in the orga-
nisation of their visual projections from thalamus to hyperstriatum
(Adret &Rogers, 1989) and no difference in visual learning ability
between the left and right eyes (Zappia &Rogers, 1987). It is possible
that the visual pathways develop over adifferent time-course in fe-
males and that they do have asymmetry in them at an age not yet
sampled, possibly before hatching.
In young male chicks the left eye is more responsive to novel
stimuli and shows more fear responses to apurple coloured bead (An-
drew &Brennan, 1983). This form of laterality is also transient, dis-
16 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
appearing by the second week of life, which is earUer than the loss of
asymmetry in the thalamofugal visual projections.
Young female chicks do not have laterality in their fear re-
sponses: both eyes of the female respond the same as the right eye of
the male (Andrew &Brennan, 1984). Both eyes of the female and the
right eye of the male have their full complement of contralateral vi-
sual projections from each side of the thalamus to the hyperstriatum,
while the left eye of the young male is deficient in contralateral pro-
jections from thalamus to hyperstriatum (Adret &Rogers, 1989),
which suggests at least some link between organisation of the visual
pathways and fear responses to abead.
Phillips and Youngren (1986) have found that unilateral injec-
tion of kainic acid into the right archistriatum of 5day-old chicks
reduces fear responses in the open field, whereas injection of the left
archistriatum does not. It is, as yet, unclear how these results may
link to lateralities in fear responses scored in monocular testing.
Interestingly, there is no sex difference in the effect of unilateral
treatment of the forebrain with glutamate or cycloheximide. Treat-
ment of either the left or right hemisphere reveals the same laterali-
zation for visual discrimination learning in both males and females
even though females tested monocularly on this task show no lat-
erality (Rogers, 1986). The unilateral administration of drugs, there-
fore, reveals that females have laterality at deeper levels of brain
processing (i.e. further removed from the level of perceptual input).
Chickens therefore exhibit laterality at several levels of neural
organisation and there are sex differences at the perceptual level. The
left and right eyes of male chickens perceive entirely different visual
worlds, and there is asymmetry in the visual pathways which carry
information from the mid-brain to the forebrain. Females have no
asymmetry at the perceptual input level but, similar to males, they
have functional asymmetry at higher levels of processing in the fore-
brain.
The left eye of the chicken is used for control of attack and copu-
lation responses (Howard, Rogers &Boura, 1980; Bullock &Rogers,
1986; Rogers, Zappia &Bullock, 1985). For example, chicks treated
with testosterone (or oestrogen) show elevated copulation scores when
they are tested binocularly on standard hand-thrust tests, and also
when they are tested with the right eye occluded (i.e. using the left
eye only). In contrast, when they are tested with the left eye occluded
(i.e. using the right eye only), they show no evidence of having been
treated with the hormone; their scores for attack and copulation are
not elevated above control levels.
Recently, we have shown that asymmetry for attack, at least,
persists into adulthood. Adult hens with the left binocular area of the
visual field occluded by "monocular polypeepers" have alow level of
LESLEY J. ROGERS 17
agonistic behaviour, equivalent to that of hens wearing "binocular
polypeepers". Those with occlusion of the right binocular field have a
high level of agonistic behaviour, equivalent to that of controls not
wearing polypeepers (Rogers &Workman, in preparation). Since this
form of laterality is present in adults and in females, it is unlikely to
depend directly on differential input to the forebrain caused by asym-
metry in the visual projections. Alternatively, if asymmetry in the
visual projections exists at some time during the early development of
the female, this may confer afunctional laterality on the forebrain
which persists after the asymmetry in visual pathways has disap-
peared. For example, asymmetry in visual inputs to the hyper-
striatum may establish an initial laterality in perceptual analysis
and memory formation, which lays the foundations for subsequent
differentiation of processing between the hemispheres.
DOMINANCE VERSUS DIFFERENTIAL USE OF THE HEMISPHERES
Laterality of brain function may involve complete dominance of
one hemisphere over the other so that all of agiven sort of analysis
occurs on one side only, it may be amatter of relative degrees of
involvement of the hemispheres in agiven form of processing, or it
may involve simultaneous but differential use of the hemispheres in
performing agiven function. The latter occurs in imprinting in the
chicken.
The intermediate and medial parts of the hyperstriatum ventrale
(IMHV) on the left and right sides of the forebrain are differentially
involved in imprinting (Cipolla-Neto, Horn &McCabe, 1982; and see
Horn, 1985, pp. 129-150). The memory of imprinting is stored in both
the left IMHV and right IMHV for approximately the first 3hours
after training, but by some 15 hours later the right IMHV no longer
retains its store of the memory while the left does. On the right side
the memory store is shunted to some other region of the hemisphere.
Horn and his colleagues demonstrated this by placing sequential le-
sions in the left and right IMHV regions after imprinting. In one
group of chicks the right IMHV region was lesioned 3hours after
imprinting on day 1of life (the memory of imprinting was retained by
these animals), and then the left IMHV was lesioned some 23 hours
later. After this sequence of lesions no memory of the imprinting was
retained. In another group of chickens the left IMHV was lesioned 3
hours after imprinting (memory being unaffected by this), and then
23 hours later the right IMHV was lesioned. Subsequently, these
chicks were found to have memory of the imprinting stimulus. Thus,
the long-term memory of imprinting is consolidated in different re-
gions of the left and right hemispheres. This differential use of the
18 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
hemispheres may possibly be the reason why imprinting forms a
strong and stable memory trace (Rogers, 1986).
Both hemispheres are also used differentially when young chicks
learn apassive avoidance task which involves pecking of abead
coated with the noxious tasting substance, methyl anthranylate.
There is laterality in the time course of memory events occurring in
each hemisphere. The right eye shows abrief period of improved re-
call 30 to 32 minutes after training, while the left does so at 25 min-
utes after training (Andrew &Brennan, 1985).
In the same task Rose &Csillag (1985) have shown laterality in
neuronal metabolism using the radioactive 2-deoxyglucose technique.
This is an example of 'metabolic' dominance. One can say 'dominance'
since the chicks were tested using both eyes, the bead was held in the
binocular field of vision and competition between the hemispheres
could occur. It is possible to make inferences about laterality from
tasks in which birds are tested monocularly, but dominance can be
determined only by testing them binocularly. The latter requires
competition and one side "winning" over the other.
Subcellular structural components in the IMHV, such as synaptic
apposition length, also change asymmetrically after training on the
passive avoidance bead task (see Stewart, Rose, King, Gabbott &
Bourne, 1984), some of the changes being greater on the left side,
others on the right.
Finally, it is worth mentioning that birds spend aconsiderable
amount of their sleeping time with one hemisphere asleep while the
other is awake. This is monocular sleep in which only the hemisphere
contralateral to the closed eye shows alateralized sleep pattern of
electrical activity (Ball, Amlaner, Shaffery &Opp, 1988). The lat-
erality in brain function generated thus is only transient, but it may
be essential to behaviour and possibly memory formation. It is possi-
ble that abird sleeping in its left hemisphere only would be more
responsive to novel stimuli, and subsequently show agreater likeli-
hood of attacking, compared to one sleeping in its right hemisphere
only. We do not yet know whether one hemisphere sleeps more than
the other, or whether performing certain sorts of behaviour may trig-
ger more sleep on one side than the other.
LATERALIZATION IN INDIVIDUALS AND IN POPULATIONS
Up until now, there has been atendency to underestimate the
importance of laterality at the individual level, and to focus only on
laterality in the population as a whole. This has resulted from an
emphasis on looking for genetic/evolutionary explanations for lat-
erality in humans, but, if abrain needs to be lateralized to function
LESLEY J. ROGERS 19
efficiently, it may not matter on which side it conducts one set of
functions versus the other, only that laterality is present in one direc-
tion or the other.
At least, this would be the case at the level of the individual.
Nevertheless, if lateralization of brain function has arole in social
behaviour, whether or not most (or even all) individuals in the social
group are lateralized in the same direction may be influential. In-
deed, in groups of young chickens the presence or absence of lateraliz-
ation at the population level has been shown to alter the stability of
the social hierarchy (Rogers &Workman, 1989). Chicks hatched from
eggs exposed to light during incubation all have their brains lateral-
ization in the same direction (see later); they have lateralization at
both the individual and the population levels. Those hatched from
eggs incubated in darkness have lateralization at the individual
level, but not at the population level (Rogers, 1982; see later); half of
the individuals have lateralization in one direction and half in the
other. The social groups of chicks exposed to light during incubation
form amore stable and rigid hierarchy, as measured in terms of their
competition for access to afood source. The group structure of chicks
hatched from eggs incubated in darkness was more variable from day
to day, possibly because there was less predictability from individual
to individual within the social group.
To summarise, for solitary behavioural performance the direction
of lateralization for perception, cognition, footedness or handedness
may not matter. However, the presence of apopulation bias in lat-
eralization may well have some influence on social interaction and
group structure. It is, of course, the latter situation which has con-
cerned anthropologists with respect to handedness in the human pop-
ulation and shared tool use.
FACTORS AFFECTING THE DEVELOPMENT OF ASYMMETRY
In the chicken the direction of brain laterality is determined by
differing amounts of light input received by the left and right eyes of
the embryo (Rogers, 1982; Rogers 1986). During the last three or so
days of incubation the chick embryo is oriented in the egg such that
its left eye is occluded by its body and the right eye is exposed to
receive light input entering the egg through the shell and mem-
branes. The greater amount of light received by the right eye during
the sensitive period just prior to hatching stimulates the growth of
visual pathways from that eye in advance of those from the left eye.
If the embryo's head is withdrawn from the egg on day 19 or 20 of
incubation, the right eye occluded and the left eye exposed to light,
there is areversal of both structural and functional laterality in the
20 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
brain. The asymmetry in the visual projections from thalamus to fore-
brain in male chicks is reversed (Rogers &Sink, 1988), and the func-
tional lateralization for attack and copulation behaviour is reversed
(Rogers, 1990a). Chicks hatched from eggs incubated in darkness
show no population laterality for attack and copulation, but appear to
retain laterality at the individual level (Zappia &Rogers, 1983).
Thus, lateralized light input before hatching aligns the direction of
laterality in the population, but it does not actually generate the
asymmetry. (Only 2hours of light is sufficient to do this; Rogers,
1982.) Compare the effects of handling in rats in which the early ex-
perience unmasks or generates alaterality not present in non-han-
dled animals (Sherman et al., 1980; see earlier).
The hormone testosterone can also influence the development of
laterality in male chicks (Zappia &Rogers, 1987). Treatment with
testosterone on day 2causes areversal in the laterality of eye differ-
ences in performance on the visual discrimination, pebble floor task.
Contrary to expectations, treatment of females with testosterone does
not generate lateralized differences between the eyes; that is, it does
not "masculinize" their brains.
Diamond (1985) has reported asymmetries in the thickness of
various regions of the cortex of the rat. In males on the whole the
right cerebral cortex is larger than the left, and the reverse is gener-
ally true in females. Ovariectomising females leads them to have the
male-type pattern. Yet hormones are not the only variables determin-
ing thickness of the cortex as it is also affected by age and experience
in enriched and impoverished environments. These latter factors also
influence the degree of asymmetry between the left and right sides.
Consistent with this, Berrebi et al. (1988) have shown effects of sex,
early experience and age on various regions of the corpus callosum.
There are sex differences in the lateralized bias in tail posture
adopted by neonatal rats, the exact nature depending on the strain
(see Denenberg, 1984a), and Rosen, Berrebi, Yutzey &Denenberg
(1983) have shown that this can be influenced by administering an-
drogens prenatally. Females responded to treatment with tes-
tosterone showing areversal in the bias of their tail posture but the
treatment did not make them the same as males. There was no effect
of testosterone treatment on the males.
Geschwind and Behan (1982) have postulated that testosterone
may have arole in the development of laterality in the human brain
and so account for at least some of the differences in behaviour be-
tween the sexes. Theirs is arather unitary hypothesis giving tes-
tosterone amajor, or even sole, role in determining laterality in the
human brain. As the studies using the chicken brain as amodel dem-
onstrate, testosterone and environmental experience (light input) can
both influence laterality, and these must both interact with genetic
LESLEY J. ROGERS 21
factors (which are likely to determine the orientation of the embryo
in the egg) to produce afinal result in agiven brain. No single factor
can be separated out as the major or sole determinant in its own
right.
Geschwind &Behan (1982) proposed that testosterone acts on the
left hemisphere to retard its development, and thus high levels of
testosterone in the foetus may cause an increased incidence of left-
handedness and mental retardation, both occurring more frequently
in males. High levels of testosterone also, apparently, alter the effi-
ciency of the immune system and anumber of other physiological
processes. Hence, they suggested that exposure of the foetus to high
levels of testosterone causes aconstellation of effects. Geschwind and
Galaburda (1987) have also argued that abnormally high levels of
testosterone may cause "giftedness", and even that homosexuality re-
sults from effects of testosterone on brain lateralization and that is
coupled with an immune system more susceptible to AIDS infection.
This latter hypothesis is based on several assumptions and arather
convoluted path of reasoning. Firstly they believe, without convincing
evidence of support, that male homosexuality depends on lower than
normal levels of circulating free testosterone, and also that it results
from stress during pregnancy. This stress is said to cause atransient
increase in testosterone levels to be followed later by arebound low-
ering of testosterone levels. The transient increase in testosterone,
they hypothesise, causes increased "nonrighthandedness" in homo-
sexuals and possibly an immunological condition more susceptible to
autoimmune disease (pp. 175 of Geschwind and Galaburda, 1987).
There is no evidence from the human species to support these
ideas, and the experimental data obtained from animals demonstrate
clearly that such complex behaviours cannot be tied to aunitary
cause of hormonal action.
CONCLUSIONS
The number of examples of both structural and functional lat-
erality in nonhuman species is growing rapidly, and it is now clear
that lateralization of brain structure and function developed very
early in the course of evolution. Indeed, functional lateralization may
have become an essential aspect of brain function not long after the
brain became bilaterally duplicated in structure. It did not arise sec-
ondarily to shared tool use and handedness in humans, although
these factors may subsequently have influenced the degree and na-
ture of the laterality. Laterality in perceptual and cognitive processes
appears to have been an antecedent to laterality of limb use in both
birds and primates.
22 THE INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
It is timely for psychologists concerned with understanding lat-
erality in the human species to examine the data available in ani-
mals, not simply to find evidence for the evolutionary origins of lat-
erality in humans, but also to discover the factors which influence the
development of laterality. Experience has been shown to play an im-
portant role in the development of laterality in two species so far. The
sex hormones also influence the development of asymmetry, but their
role does not appear to be straightforward in the way postulated by
some psychologists working with humans.
Laterality in the nervous system can occur in anumber of differ-
ent forms: structural and functional, at the population level and the
individual level. Functional laterality may even change from 'mo-
ment-to-moment' as in the case of lateralized sleep in birds. Astatic
view of laterality may have served apurpose while we were still in
the phase of documenting the presence of asymmetries in different
species, but laterality is adynamic phenomenon varying with age,
experience and the particular situation in which the animal finds it-
self. The studies using animals are providing ameans to understand
these dynamic processes in laterality.
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