Elsevier

Brain Research Bulletin

Volume 76, Issue 3, 15 June 2008, Pages 264-271
Brain Research Bulletin

Research report
Socially acquired predator avoidance: Is it just classical conditioning?

https://doi.org/10.1016/j.brainresbull.2008.02.005Get rights and content

Abstract

Associative learning theories presume the existence of a general purpose learning process, the structure of which does not mirror the demands of any particular learning problem. In contrast, learning scientists working within an Evolutionary Biology tradition believe that learning processes have been shaped by ecological demands. One potential means of exploring how ecology may have modified properties of acquisition is to use associative learning theory as a framework within which to analyse a particular learning phenomenon. Recent work has used this approach to examine whether socially transmitted predator avoidance can be conceptualised as a classical conditioning process in which a novel predator stimulus acts as a conditioned stimulus (CS) and acquires control over an avoidance response after it has become associated with alarm signals of social companions, the unconditioned stimulus (US). I review here a series of studies examining the effect of CS/US presentation timing on the likelihood of acquisition. Results suggest that socially acquired predator avoidance may be less sensitive to forward relationships than traditional classical conditioning paradigms. I make the case that socially acquired predator avoidance is an exciting novel one-trial learning paradigm that could be studied along side fear conditioning. Comparisons between social and non-social learning of danger at both the behavioural and neural level may yield a better understanding of how ecology might shape properties and mechanisms of learning.

Section snippets

Classical conditioning: general process theory and adaptive specialization

In classical conditioning, also termed Pavlovian conditioning, animals acquire a response to a previously neutral stimulus (conditioned stimulus: CS; e.g. simple tone), if that stimulus predicts a biologically important event (unconditioned stimulus: US; e.g. food) [59]. The mechanism underpinning learning is considered to be the formation of an association between CS and US [60]. Over 100 years of behavioural research has lead to a good understanding of the parameters that affect the

Social learning

Social learning refers to instances of learning in which the behaviour of a ‘demonstrator’, or its by-products (e.g. scent marks), modify the subsequent behaviour of an ‘observer’. Several varieties of social learning have been identified according to the role of the demonstrator [19], [34]. For example, social companions may alter the probability of an observer interacting with a given stimulus (e.g. a stick), a phenomenon referred to as local enhancement [73]. Alternatively, they may alter

Socially acquired predator avoidance

Socially acquired predator avoidance is a taxonomically widespread phenomenon. It has been found in fish, birds and both eutherian and marsupial mammals. The pattern of acquisition is similar across groups. Although animals show initially little or no avoidance of a novel predator stimulus, once it has been presented together with the alarm signals of social companions, it evokes a fear response [24].

Efforts to understand whether socially acquired predator avoidance engages classical

General discussion

Socially acquired predator avoidance is a learning paradigm in which animals acquire an avoidance response towards a novel predator stimulus that initially evokes a low or no response, after it has been experienced together with a social alarm signal. The work reviewed above aimed to explore the long held view that such learning engages a classical conditioning mechanism in which the predator stimulus acts as a CS and the social alarm signal as a US [34], [52], [69]. Specifically, I aimed to

General conclusions

I argue that socially acquired predator avoidance presents an exciting and novel opportunity to explore mechanisms of learning and memory. By considering the function such learning plays in nature, one can formulate testable hypotheses regarding the way in which properties of acquisition may be evolutionarily tailored to solve this particular ecological problem, an approach I have illustrated above. Socially acquired predator avoidance learning is also a one-trial learning phenomenon, a feature

Conflict of interest

The material contained in the manuscript does not raise any conflict of interest.

Acknowledgements

A.S. Griffin was supported by a Swiss National Foundation Postdoctoral Fellowship during work on Carib grackles. The research was supported by an NSERC grant to Louis Lefebvre. Indian mynah research is supported by an Australian Research Council (ARC) Postdoctoral Fellowship to A.S. Griffin. The author wishes to thank the staff of Bellairs Research Station of McGill University, as well as staff of the Central Animal Facility of the University of Newcastle. The author also thanks S. Marlin for

References (79)

  • S.L. Lima et al.

    Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack?

    Anim. Behav.

    (1999)
  • C. Martinoya et al.

    Comparing frontal and lateral viewing in the pigeon. II. Velocity thresholds for movement discrimination

    Behav. Brain Res.

    (1983)
  • L.D. Matzel et al.

    Information and expression of simultaneous and backward associations: implications for contiguity theory

    Learn. Motiv.

    (1988)
  • R. McKenzie et al.

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

    Neuropsychologia

    (1998)
  • A.S. Pell et al.

    The impact of two exotic hollow-nesting birds on two native parrots in savannah and woodland in eastern Australia

    Biol. Conserv.

    (1997)
  • J.A. Soha et al.

    A species-specific acoustic cue for selective song learning in the white-crowned sparrow

    Anim. Behav.

    (2000)
  • W. Vieth et al.

    The adaptive significance of avian mobbing. III. Cultural transmission of enemy recognition in blackbirds: cross-species tutoring and properties of learning

    Anim. Behav.

    (1980)
  • K. Zuberbühler et al.

    Diana monkey long-distance calls: messages for conspecifics and predators

    Anim. Behav.

    (1997)
  • R.J. Andrew

    Use of head position by birds to determine mode of analysis of what is seen

    Acta Zool. Sin.

    (2006)
  • J. Archer

    Behavioural aspects of fear

  • M.C. Baker et al.

    Mobbing calls of black-capped Chickadees: effects of urgency on call production

    Wilson Bull.

    (2002)
  • P. Bateson

    Models of memory: the case of imprinting

  • D.T. Blumstein

    Golden-marmot alarm calls. I. The production of situationally specific vocalisations

    Ethology

    (1995)
  • P.A. Brennan et al.

    Neural mechanisms of olfactory recognition memory

  • D.L. Cheney et al.

    How Monkeys See the World

    (1990)
  • N.S. Clayton et al.

    Episodic-like memory during cache recovery by scrub jays

    Nature

    (1998)
  • M. Cook et al.

    Observational conditioning of snake fear in unrelated rhesus monkeys

    J. Abnorm. Psychol.

    (1985)
  • E. Curio et al.

    The adaptive significance of avian mobbing. II. Cultural transmission of enemy recognition in blackbirds: effectiveness and some constraints

    Z. Tierpsychol.

    (1978)
  • M.S. Dawkins

    What are birds looking at? Head movements and eye use in chickens

    Anim. Behav.

    (2002)
  • M. Domjan et al.

    Learning with arbitrary versus ecological conditioned stimuli: evidence from sexual conditioning

    Psychon. Bull. Rev.

    (2004)
  • N.J. Emery et al.

    The mentality of crows: convergent evolution of intelligence in corvids and apes

    Science

    (2004)
  • C.S. Evans

    Referential signals

    Perspect. Ethol.

    (1997)
  • M.S. Fanselow

    Neural organization of the defensive behavior system responsible for fear

    Psychon. Bull. Rev.

    (1994)
  • B.G. Galef

    Imitation in animals: history, definition, and interpretation of data from the psychological laboratory

  • B.G. Galef et al.

    Absence of blocking, overshadowing, and latent inhibition in social enhancement of food preferences

    Anim. Learn. Behav.

    (1993)
  • C.R. Gallistel et al.

    Computational versus associative models of simple conditioning

    Curr. Dir. Psychol. Sci.

    (2001)
  • J. Garcia et al.

    Relation of cue to consequence in avoidance learning

    Psychon. Sci.

    (1966)
  • A.S. Griffin

    Social learning about predators: a review and prospectus

    Learn. Behav.

    (2004)
  • S. Grossberg

    A neural network architecture for Pavlovian conditioning: reinforcement, attention, forgetting, timing

  • Cited by (0)

    View full text