Nonassociative Learning
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Kirchkamp, Oliver et al. “Nonassociative Learning.” Encyclopedia
of the Sciences of Learning. Ed. Norbert M. Seel. Boston, MA:
Springer US, 2012. 2475-2477. Web. 16 Feb. 2012.
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http://dx.doi.org/10.1007/978-1-4419-1428-6_1849
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Springer-Verlag
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Author's final manuscript
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Thu May 26 23:41:37 EDT 2016
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http://hdl.handle.net/1721.1/69128
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Detailed Terms
In: Encyclopedia of the Sciences of Learning (Seel NM, ed). New York: Springer, 2012, pp. 24752477
Nonassociative Learning
Chi-Sang Poon
Harvard-MIT Division of Health Sciences
and Technology
Massachusetts Institute of Technology
Cambridge, MA
United States
cpoon@mit.edu
Susanne Schmid
Anatomy and Cell Biology
Schulich School of Medicine & Dentistry
London, Ontario
Canada
susanne.schmid@schulich.uwo.ca
Synonyms
None
Definition
Nonassociative learning is an implicit (non-declarative) or procedural form of learning that
systematically attenuates (habituates) or augments (sensitizes) an animal’s sensory percept or
behavioral response to a sensory stimulus upon repeated or continual presentation of the
stimulus. It differs from associative learning in that it does not require the temporal pairing
between two different sensory stimuli or between a sensory stimulus and corresponding response
feedback. It is considered a fundamental form of learning that can be observed across all animal
phyla and most sensory modalities. It may also be regarded as one of the simplest forms of
unsupervised learning in animals, in that it automatically classifies the valence of a sensory input
based upon its temporal pattern without the need for a supervisory signal. In most animal species
including humans, habituation and sensitization take place in sensory and sensorimotor pathways
and provide an important central adaptation and gating mechanism for selective suppression or
amplification of sensory information reaching higher centers of the brain or their effector organs.
Theoretical Background
Early theories about nonassociative learning include the dual-process theory of Groves and
Thompson (1970). This theory is based on the assumption that every sensory stimulus could
induce habituation and sensitization at the same time depending on stimulus strength and
temporal pattern. The dual process theory was revisited and refined by Prescott (1998), who
proposed a model of serial induction of habituation and sensitization, with the depressing locus
preceding the modulatory systems responsible for response facilitation. This causes the
facilitation to wane in the final behavioral response that culminates from these opposing
mechanisms.
The neural correlates of nonassociative learning in lower animals were revealed by Eric Kandel
and co-workers through their work in the sea hare Aplysia. The distinct neuronal pathways
mediating the gill and siphon withdrawal reflex in this invertebrate model enabled them to record
corresponding synaptic and neuronal activities in the behaving animal, directly linking synaptic
plasticity to behavioral plasticity. This work led to the discovery of various cellular and
molecular mechanisms underlying homosynaptic depression mediating short-term and long-term
habituation and heterosynaptic facilitation causing sensitization. Eric Kandel was awarded the
Nobel Prize in Physiology and Medicine in 2000 for his pioneering work.
A comprehensive and more detailed concept of nonassociative learning and its cellular basis has
been developed by Poon and co-workers (Poon & Young, 2006). Poon’s model differentiates
between intrinsic or primary mechanisms that are localized in the sensorimotor pathway of
interest (habituation and primary sensitization), and extrinsic or secondary mechanisms located
in other pathways that modulate the primary pathway (desensitization and secondary
sensitization); see Fig. 1. Behaviorally, desensitization and secondary sensitization are
distinguished from habituation and primary sensitization by a corresponding heterosynapticallyinduced memory trace (engram) in the secondary pathway. The manifestation of the adaptation
effects independent from the primary stimulus is the clearest marker of desensitization and
secondary sensitization. In contrast, the memory trace of habituation and primary sensitization is
latent and is not observable until the next presentation of the primary stimulus. Such an extension
of nonassociative learning to secondary pathways unifies some higher-order forms of
nonassociative learning, such as generalization (transfer, referral or remapping) of habituation
and sensitization from one sensory site (or modality) to another. Poon also emphasizes the
dependence of nonassociative learning on stimulus frequency by contrasting it with a
nonassociative temporal gating mechanism that together prioritizes or filters sensory information
for transmittal to higher processing structures based upon the frequency of occurrence of the
stimulus (use dependence) or its timing (time dependence). Failure of this sensory “firewall”
may result in distortions in the sensory percept or resultant behavioral response. Indeed, many
mental, neurophysiologic and neurodegenerative disorders are associated with nonassociative
learning abnormalities.
Figure 1. Schematic illustration of habituation (H) and primary sensitization (S1) mediated by
homosynaptic depression (filled inner triangle, blue) or facilitation (open inner triangle, red) in
primary pathway, and secondary sensitization (S2) mediated by heterosynaptic facilitation in
secondary pathway. By analogy, heterosynaptic depression of excitatory transmission (or
facilitation of inhibitory transmission) in the secondary pathway may result in desensitization
(secondary habituation, not shown). Alternatively, nonassociative learning may result from
changes in neuronal excitability instead of synaptic efficacy. Adapted from Poon & Young
(2006).
Important Scientific Research and Open Questions
Nonassociative learning mechanisms are studied in a wide variety of organisms and reflex
pathways, including: the Hering-Breuer lung inflation reflex and autonomic responses to odors in
rats, the taste-mediated proboscis extension reflex in bees and Drosophila, and different forms of
escape or startle responses, such as the gill and siphon withdrawal reflex in Aplysia, startle
responses in rodents, swim reversal in C. elegans, the bending reflex in leech, the swim response
in Tritonia, the tentacle withdrawal reflex in Helix aspersa, and others. However, studies on
nonassociative learning mechanisms are not restricted to reflex pathways and may also include
cognitive processes such as modulation of aggressive behavior in bullfrogs as well as orienting
responses, visual attention, and pain perception in humans.
Screens of mutant animals (mice, zebrafish, Drosophila and the nematode C. elegans) for
nonassociative learning deficits or overexpression are starting to reveal various genes and
molecules specifically implicated in habituation and sensitization. An emerging view is that a
variety of cellular, molecular and neural network mechanisms may contribute to nonassociative
learning depending on the behavioral model studied, the modality of the stimulus and the
timescale of stimulus presentation. On the other hand, many nonassociative learning mechanisms
may be highly conserved among species (Schmid et al, 2010; Glanzman 2010).
Important roles for nonassociative learning deficiencies or overexpression have been implicated
in certain mental disorders such as schizophrenia, autism and attention deficit/hyperactivity
disorder. Nonassociative learning deficiencies seem to also contribute to the cognitive deficits in
neurodegenerative disorders, such as Alzheimer’s and Parkinson’s disease. Many patients
suffering from these disorders show impaired habituation to an acoustic (or tactile) startle
stimulus, indicating disrupted sensory gating. Another measure of sensory gating commonly
used in humans and animal models is prepulse inhibition, i.e., the inhibition of a startle response
by a preceding sensory stimulus. Although prepulse inhibition was historically not considered a
form of learning, it perfectly fits into Poon’s definition of desensitization and might therefore
represent a form of nonassociative short-term memory. It may be noted, however, that the
nonassociative nature of desensitization and secondary sensitization has been occasionally
questioned, since environmental context has been shown to play a role in these forms of learning
in some models, indicating that they can at least be modulated by associative processes.
Given the implications of nonassociative learning in higher cognitive function in health and
disease and in light of the recent efforts in trying to understand more complex forms of learning,
it is astonishing how little is known about the mechanisms underlying this most basic form of
learning in humans and mammalian models. Studies of the current models combined with newly
developed investigative tools such as refined imaging and multi-neuronal recording techniques,
genetic and optogenetic approaches etc. will help to further unravel the cellular, molecular and
neural network correlates of nonassociative learning and their roles in mediating the sensory or
sensorimotor integration dysfunctions in various neurologic and neurophysiologic diseases in
future.
Cross References
→ Habituation
→ Habituation & Sensitization
→ Sensitization
→ Explicit versus Implicit Learning
→ Procedural Learning
→ Supervised Learning
→ Unsupervised Learning
References
Groves, P.M. & Thompson, R.F. (1970) Habituation: a dual-process theory. Psychological
Review, 77 (5): 419-450.
Prescott, S.A. (1998) Interactions between Depression and Facilitation within Neural Networks:
Updating the Dual-Process Theory of Plasticity. Learning & Memory, 5: 446-466.
Kandel, E. R. (2001) The molecular biology of memory storage: A dialogue between genes and
synapses. Science 294: 1030-38.
Poon, C.S. & Young, D.L. (2006) Nonassociative learning as gated neural integrator and
differentiator in stimulus-response pathways. Behavioral and Brain Function, 2: 29.
Schmid, S., Brown, T., Simons-Weidenmaier, N., Weber, M., Fendt, M. (2010) Group III
metabotropic glutamate receptors inhibit giant neurons in the caudal pontine reticular nucleus but
do not mediate synaptic depression/short-term habituation of startle. J. Neuroscience, 30(31):
10422-30.
Glanzman, D.L. (2010) Common mechanisms of synaptic plasticity in vertebrates and
invertebrates. Curr Biol. 20(1): R31-36.