Social learning in birds
by Enikõ Kubinyi
Until now, much effort has gone into understanding mechanisms of social learning by dividing it into meaningful categories (for reviews, see Byrne & Russon, 1998, Galef, 1988, Whiten & Ham, 1992, Zentall & Akins, 2001). These categories are not mentioned in the present essay. Some light is shed on subtle examples of learning from group-mates during food-consumption, while a top-capacity of a bird-brain, namely movement imitation, is put in the focus of interest. Finally we take a look at the neurobiological background, and become acquainted with Alex, the taking grey parrot.
According to the definition of Whiten and Ham (1992) social learning takes place "when B learns some aspect of the behavioural similarity from A" (p. 248). It is considered to be an important manifestation of intelligence in nonhuman species, and the basis of many human behaviours (Meltzoff, 1988). The adaptive value of social learning is unambiguous: it saves time and energy that might be wasted as an individual learned by trial and error. Different techniques to obtain food can spread by individuals observing more experienced members of the group (e.g. tits, Fisher & Hinde, 1949, Sasvári, 1979; doves, Palameta & Lefebvre, 1985). Individual experiences might interact with socially acquired information (sparrows, Fyday & Greigsmith, 1994). As laboratory studies reveal, (e.g. Sherry & Galef, 1984), social learning does not usually involve the exact copying of the demonstrator's behaviour. Naive observers develop their own, often similar method to obtain the same target as the demonstrator. The possibility for learning in this way is much greater in social species because they spend more time close to others. However, living in a group requires such skills that a lonely individual rarely confronts with. For example, during imitative performance of transitive actions, the subject simultaneously has first-person and third-person experience of a relationship between an action and an object (Barresi and Moore,). There is evidence that for example pigeons and quail imitate beak or feet use to depress a lever (Akins & Zentall, 1996, 1998). Experience of this kind is necessary, although not sufficient, for learning to distinguish first- and third-person perspectives, a crucial component of theory of mind. Crows seem to be able to camouflage their intentions and manipulate the attention of group-mates during food-concealment (Bugnyar & Kotrschal, 2002).
Song learning is a special case of matching behaviour in animals. It is regulated to a large extent by maturation and hormones, however, regional variations in song presume that young birds learn their regional dialect by copying the song of more mature conspecifics (Baptista & Petrinovich, 1986). Importantly, bird song takes place in the auditory modality. Consequently, stimuli produced by the model and the observer can be a close match, because comparisons between one's own utterances and that of others is relatively easy. This is not the case with copying body movements: there visual information must be translated into matching motor output. Below an evolutional and a theoretical account try to answer how this translation could be emerged and survive.
The evolution of movement imitation
Moore calls attention to the highly probable assumption that just as species
evolve from other species, also biological processes (like learning) typically
evolve from similar, simpler processes. He made a branching, hierarchical
evolutionary tree of learning (1996, Fig. 1).
Root of the tree is the reflex repertoire. Conditional learning evolved
from sensitisation. Interestingly, according to the conception, movement
imitation (non-reinforced copying of novel responses) has evolved at least
twice; once in mammals from instrumental learning, and once in birds from
song learning.
Moore presents his conception about birds' movement imitation by the
example of his own African grey parrot, Okíchoro. This parrot imitated
at least sixteen human movement (Moore, 1992). Whenever he left the bird's
room, waved good-bye and said "Ciao." In Fig. 2A the bird is
waving and saying "Ciao.". 
In
Fig 2B he is doing the same, but waving his wings instead of a foot.
The bird sometimes synchronised imitative movements with vocal mimicry,
e.g. by making knocking movements in mid air with a foot while vocalising
appropriate sounds. (The author of this essay knew a magpie that kicked
off the telephone handset and started to screech into it whenever the
telephone was ringing).
Okíchoro also showed cross-modal imitation; copied movements that
he could not see himself perform, such as "nod" and "shake"
(cross-modal imitation).
Grey parrots are famous for their conspicuous ability to imitate sounds.
If movement imitation did evolve from vocal mimicry, it had to do so in
two steps: first it was necessary to copy sounds with non-vocal muscles
(percussive mimicry). Moore's parrot sometimes copied the sound of a knocking
by banging on things with the top of his beak or head. Then, a change
from auditory to visual models would produce movement imitation.
True, that no species shows any of these processes without also showing
its hypothesised precursor. However, the proposed sequence needs more
comparative data to be confirmed - birds and primates have been studied
much more intensively than others, therefore there was a bigger chance
for finding any kind of imitation in these taxa.
Perceptual-motor translating in movement imitation
Computational theories suggest that perceptual-motor translation is achived
by selection processes in which input from the model is compared with
the observer's motor output, and/or with predictions of what that output
would be if each of a set of motor primitives were activated. These theories
are not adequate for explaining imitation of perceptually opaque movements
such as facial gestures (Schaal, 1999).
Two theories were formed to address this problem. The first one proposes
that there is an innate imitation mechanism that transforms visual input
into a 'supramodel' representation. Then a 'goal-directed' selection process
compares this representation with proprioceptive feedback from the observer's
motor output. Matched pairs are favoured for future production. This hypothesis
is - among others - inconsistent with the experimental data that imitation
is experience-dependent in primates.
The second hypothesis suggests that development of the imitation mechanism
is highly experience-dependent. It consists of a set of bidirectional
excitatory links between sensory and motor representations (Heyes, 2000).
In the case of perceptually opaque movements, co-activation of sensory
and motor representations occurs whenever the individual observes their
own motor output through experience with mirrors, of being imitated, and
of socially synchronous movement in response to a common stimulus. Concerning
our topic, this theory is consistent with the finding that avian species
can imitate foraging behaviours they have performed in flocks. Moreover,
it is also consistent with recent data on neural mechanisms. It suggests
that imitation of sequences of meaningless or novel movements is associated
with direct activation of cortical and subcortical movement preparation
areas via the dorsal visual pathway. Indirect vertical associations may
be represented by the activation of the left inferior frontal gyrus. Although
recent studies suggest that the left inferior frontal gyrus appears to
mediate movement recognition rather than imitation, this region is thought
to be the human homologue of the 'mirror neurons' containing area in monkeys.
A mirror neuron is a neuron which fires both when performing an action
and when observing the same action performed by another (possibly conspecific)
creature. It fires when a monkey grasps a nut and when it sees a human
grasp a nut (Rizzolatti et al, 1999). The discovery of mirror neurons
has important implications for the evolution of language, suggesting pre-existing
brain structure which could have provided a basis for human language.
Little is known about mirror neurons in birds, probably because the experimental field is rather new, and the structure of the bird-brain is rather different from that of the mammals, first of all there is no cortex in birds. In general, mammalian neocortex is argued to be homologue with the striatum (Karten et al 1973), so mirror neurons possibly could be find somewhere in the ecto-, neo- or archistriatum.
It is also now known that complex cognitive behaviours in birds, i.e. vocal learning, not even found in many mammals, involve both basal ganglia-like and pallial (above the basal ganglia) brain structures (Nottebohm 1972).
The top of the avian cognition (Zachar, 2002): Alex, the talking bird
The world-famous African grey parrot, Alex could thank the top-capacities
clearly to his special training system that is based on social learning.
After 12 years of training Alex names more than 40 different objects (including
paper, key, banana, chain, shoulder, chair, wool), labels seven colours,
functionally uses the word "no" and "Come here", "I
want X", "Wanna go Y" and distinguish quantities of objects
up to six. Moreover, Alex earned the comprehension of "category".
He can answer for both "What colour?" and "What shape?"
questions.
Alex
has also learned the abstract concepts of "same" and "different".
He responds with "None" to the absence of information about
these concepts. Importantly, he can also respond to questions involving
objects, colours, shapes and materials not used in training.
One feature common to all training procedures is the consistent and exclusive
use of intrinsic rewards. If Alex correctly labels an object, the trainers
give him the object and not a food item.
The primary training system, called the model/rival (M/R) technique involves
three-ways interactions between two humans and the parrot. The latter
watches one human act as a trainer of the second human, who acts as a
model for Alex's responses - and as his rival for the trainer's attention.
This protocol involves repeating the interaction while reversing the roles
of the human trainer and model, and occasionally includes the bird in
the interactions. Due to this protocol, Alex responds to, interact with
and learns from all the trainers with whom he comes in contact.
Despite his doubtless success, Alex cannot tell what he did yesterday
or what he would like to do tomorrow. But he can perform tasks that were
once thought beyond the capability of all beings except humans or possibly
certain nonhuman primates (Pepperberg, 1990). Therefore this phylogenetically
distant species is an eminent model for the developing of human language
use.
Enikõ Kubinyi, 2003.
References:
Akins, C.K., & Zentall, T.R. (1996). Imitative learning in male Japanese
quail (Coturnix japonica) involving the two-action method. Journal of
Comparative Psychology, 110, 316-320.
Baptista, L. F. and Petrinovich, L. (1986) Song development in the white-crowned
sparrow:social factors and sex differences. Animal Behaviour, 34:359-1371.
Barresi, J. & Moore, C. (1996) Intentional relations and social understanding.
Behav. Brain Sci. 19, 107-154.
Bugnyar, T. & Kotrschal, K. (2002) Observational learning and the
raiding of food caches in ravens, Corvus corax: is it a 'tactical' deception?
Animal Behaviour, 64:185-195.
Byrne, R.W., & Russon, A.E. (1998). Learning by imitation: a hierarchical
approach. Behavioral Brain Sciences, 21, 667-721.
Fisher, J. & Hinde, R. A. (1949) Furthr observations on the opening
of milk bottles by birds. British Birds, 42:347-357.
Fyday, S. L. & Greigsmith, P. W. (1994) The effect of social-learning
on the food choice of the house sparrow (Passer domesticus). Behaviour,
128:281-300.
Galef, B. G. (1988) Imitation in animals: history, definition, and interpretation
of data from the psychobiological laboratory In: Social Learning, ed.
T.R. Zentall and B. G. Galef (p. 1-28.), Hillsdale, NJ: Lawrence Erlbaum
pp. 3-28.
Heyes, C, (2001) Causes and consequences of imitation. Trends in Cogn.
Sci., 5:253-261.
Heyes, C. M & Ray, E. D. (2000) What is the significance of imitation
in animals? Adv. Study Behav. 29, 215-245.
Karten, H. J., Hodos, W., Nauta, W. J. H. & Revzin, A. M. (1973) Neural
connections of the "visual wulst" of the avian telencephalon.
Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia).
J. Comp. Neurol. 150:253-277.
Meltzoff, A. N. & Moore, M. K. (1988) Infant intersubjectivity: broadening
the dialogue to include imitation, identity and intention. In Intersubjective
Communication and Emotion in Early Ontogeny (Braten, S., ed.) pp. 47-62,
Cambridge University Press.
Moore, B. R. (1992) Avian movement imitation and a new form of mimicry:
Tracing the evolution of a complex form of learning. Behavior, 122:231-263.
Moore, B. R. (1996) The evolution of imitative learning. In C. M. Heyes
& B. G. Galef, Jr. (Eds.), Social learning in animals: The roots of
culture (pp. 245-265). London: Academic Press
Nottebohm, F (1972) The origins of vocal learning. The American Naturalist
106:116-140.
Palameta, B. & Lefebvre, L. (1985) The social transmission of a food-finding
technique in pigeons: What is learned? Animal Behaviour, 33:892-896.
Pepperberg, I & Bright, R. J. (1990) Alex the talking bird. Birds
USA 1990 Annual. on-line. http://www.vdnent.com/html/articles/part_train:alex.html
Rizzolatti, G. et al. (1999) Resonance behaviors and mirror neurons. Arch.
Ital. Biol. 137, 85-100.
Sasvári, L. (1979) Observational learning in great, blue and marsh
tits. Animal Behaviour 27. 767-771.
Schaal, S. (1999) Is imitation learning the route to humanoid robots?
Trends Cogmit. Sci. 3, 233-242.
Sherry, D. F. & Galef, B. G. (1984) Cultural transmission without
imitation: Milk bottle opening by birds. Animal Behavior, 32:937-938.
Whiten, A. & Ham, R. (1992) On the nature and evolution of imitation
in the Animal Kingdom: Reappraisal of a century of research advances in
the study of animal behavior. Behavior. 21. 239-283.
Zachar, G. (2001) Cognition in birds. In: Brain, Behaviour and Evolution:
Avian Systems (course) personal comm.
Zentall, T. & Akins, C. (2001) Imitation in animals: evidence, function,
and mechanisms. In R. G. Cook (ed.) Avian Visual Cognition {on line: www.pigeon.psy.tufts.edu/avc/zentall}