Nonassociative Learning
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1 Nonassociative Learning The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation As Published Publisher Kirchkamp, Oliver et al. Nonassociative Learning. Encyclopedia of the Sciences of Learning. Ed. Norbert M. Seel. Boston, MA: Springer US, Web. 16 Feb Springer-Verlag Version Author's final manuscript Accessed Sun Apr 22 18:34:53 EDT 2018 Citable Link Terms of Use Detailed Terms Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use.
2 In: Encyclopedia of the Sciences of Learning (Seel NM, ed). New York: Springer, 2012, pp Nonassociative Learning Chi-Sang Poon Harvard-MIT Division of Health Sciences and Technology Massachusetts Institute of Technology Cambridge, MA United States Susanne Schmid Anatomy and Cell Biology Schulich School of Medicine & Dentistry London, Ontario Canada 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
3 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.
4 Figure 1. Schematic illustration of habituation (H) and primary sensitization (S 1 ) mediated by homosynaptic depression (filled inner triangle, blue) or facilitation (open inner triangle, red) in primary pathway, and secondary sensitization (S 2 ) 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
5 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
6 References Groves, P.M. & Thompson, R.F. (1970) Habituation: a dual-process theory. Psychological Review, 77 (5): Prescott, S.A. (1998) Interactions between Depression and Facilitation within Neural Networks: Updating the Dual-Process Theory of Plasticity. Learning & Memory, 5: Kandel, E. R. (2001) The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 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): Glanzman, D.L. (2010) Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Curr Biol. 20(1): R31-36.
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