Aversive Learning Enhances Perceptual and Cortical Discrimination of Indiscriminable Odor Cues

Cognitive Neurology and Alzheimer's Disease Center, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
Science (Impact Factor: 33.61). 04/2008; 319(5871):1842-5. DOI: 10.1126/science.1152837
Source: PubMed


Learning to associate sensory cues with threats is critical for minimizing aversive experience. The ecological benefit of associative learning relies on accurate perception of predictive cues, but how aversive learning enhances perceptual acuity of sensory signals, particularly in humans, is unclear. We combined multivariate functional magnetic resonance imaging with olfactory psychophysics to show that initially indistinguishable odor enantiomers (mirror-image molecules) become discriminable after aversive conditioning, paralleling the spatial divergence of ensemble activity patterns in primary olfactory (piriform) cortex. Our findings indicate that aversive learning induces piriform plasticity with corresponding gains in odor enantiomer discrimination, underscoring the capacity of fear conditioning to update perceptual representation of predictive cues, over and above its well-recognized role in the acquisition of conditioned responses. That completely indiscriminable sensations can be transformed into discriminable percepts further accentuates the potency of associative learning to enhance sensory cue perception and support adaptive behavior.

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    • "Pairing of odors with unconditioned stimuli has been shown to lead to augmented processing of these olfactory stimulants (Li et al. 2008; Åhs et al. 2013; Krusemark et al. 2013) in cue conditioning paradigms. However, due to their special nature, that is, being able to evoke affective states in a very direct way and often being rather vaguely present in the environment, odors seem to be perfectly suited for context conditioning. "
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    ABSTRACT: Perception and evaluation of objects are highly dependent on surrounding contexts. Threatening contexts enhance processing of faces. Because odors are assumed to deliver strong contextual information, the present study aimed at demonstrating 1) that odors can constitute threat and safety contexts, and 2) consequently modulate the processing of faces presented in these contexts. Therefore, previously neutral odors were used as contextual stimuli in a context conditioning paradigm, resulting in an olfactory anxiety and a safety context. Then, faces showing angry, neutral, or fearful expressions were presented within both contexts during a test phase to investigate the effects of threat versus safety contexts on face perception. The late positive potential (LPP) from the EEG, skin conductance level, and subjective ratings were recorded. Results reveal successful olfactory context conditioning as reflected in enhanced processing of the anxiety context, indicated by enhanced LPP after conditioning, increased skin conductance level, and marginally respectively increased ratings. Moreover, faces presented within the threat context were rated as more unpleasant and marginally more arousing than faces presented in the safety context. Thus, olfactory stimuli can serve as context in fear conditioning, and a threatening olfactory context seems to enhance processing of stimuli perceived within this context.
    Chemical Senses 11/2015; DOI:10.1093/chemse/bjv067 · 3.16 Impact Factor
    • "In addition to single cell responses, overall dynamics in olfactory structures are also strongly modulated by discrimination learning (Beshel et al., 2007; Kay and Beshel, 2010; Kay and Lazzara, 2010; Martin, et al., 2007). In invertebrates, neural correlates of olfactory discrimination learning have been reported in both the antennal lobe and mushroom body structures (Silbering and Galizia, 2007; Silbering et al., 2008; Szyszka et al., 2005). In summary, discrimination learning is a distributed process across many brain structures and is modulated by stimulus and task parameters, previous experience with odorants, and manipulations of specific neurotransmitter and neuromodulator systems. "
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    ABSTRACT: Olfactory memory plays an important role in the everyday lives of both animals and humans, even if people generally attend much less than animals to incoming olfactory information. This chapter focuses on recognition memory and learning paradigms useful in characterizing the olfactory memory system. Recent studies on odour recognition memory have exploited findings from cognitive science and neuroscience that employ signal detection analysis. Receiver operating characteristic (ROC) studies provide a strong foundation for examining the role of the hippocampus in episodic recollection. In the ROC studies memory cues were composed of a large pool of ordinary household odours (e.g., lemon, thyme) mixed in sand within small plastic cups. Olfactory learning and memory result from brain activity in multiple memory pathways that contribute to different strategies of memory performance.
    Handbook of Olfaction and Gustation, Third edited by R.L. Doty, 06/2015: chapter 15: pages 337-351; John Wiley & Sons., ISBN: ISBN: 978-1-118-13922-6
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    • "Following pairing of a visual cue with a painful stimulus applied to the abdomen, IBS patients had higher skin conductance responses during extinction compared to controls (Labus et al., 2013). Further support for altered fear learning and extinction comes from studies on anxiety disorders which often co-occur with chronic pain (Bouton et al., 2001; Lissek et al., 2005; Mineka and Oehlberg, 2008). 1.3. "
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    ABSTRACT: Recent neuropsychological theories emphasize the influence of maladaptive learning and memory processes on pain perception. However, the precise relationship between these processes as well as the underlying mechanisms remain poorly understood; especially the role of perceptual discrimination and its modulation by associative fear learning has received little attention so far. Experimental work with exteroceptive stimuli consistently points to effects of fear learning on perceptual discrimination acuity. In addition, clinical observations have revealed that in individuals with chronic pain perceptual discrimination is impaired, and that tactile discrimination training reduces pain. Based on these findings, we present a theoretical model of which the central tenet is that associative fear learning contributes to the development of chronic pain through impaired interoceptive and proprioceptive discrimination acuity.
    Neuroscience & Biobehavioral Reviews 01/2015; in press. DOI:10.1016/j.neubiorev.2015.01.009 · 8.80 Impact Factor
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