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: 31.48). 04/2008; 319(5871):1842-5. DOI: 10.1126/science.1152837
Source: PubMed

ABSTRACT 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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Available from: Wen Li, Aug 14, 2015
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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
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    • "This might be advantageous in allowing a quicker responding to a stimulus that has been predictive of danger in the past. It has been suggested that a network of extinction resistant neurons within the sensory cortex (Armony et al., 1998; Li et al., 2008) and lateral nucleus of the amygdala (Repa et al., 2001) act together to reengage the amygdala when threat reappears. This is based on evidence that, following extinction, the memory of the emotional event is persistent in the amygdala, as evident by neurons in the lateral nucleus that remain responsive to the CS+ even after extinction (Repa et al., 2001). "
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    ABSTRACT: Research in humans has highlighted the importance of the amygdala for transient modulation of cortical areas for enhanced processing of emotional stimuli. However, non-human animal data has shown that amygdala dependent threat (fear) learning can also lead to long lasting changes in cortical sensitivity, persisting even after extinction of fear responses. The neural mechanisms of long-lasting traces of such conditioning in humans have not yet been explored. We used functional magnetic resonance imaging (fMRI) and assessed skin conductance responses (SCR) during threat acquisition, extinction learning and extinction retrieval. We provide evidence of lasting cortical plasticity in the human brain following threat extinction and show that enhanced blood oxygen level–dependent (BOLD) signal to the learned threat stimulus in the auditory association cortex is resistant to extinction. These findings point to a parallel avenue by which cortical processing of potentially dangerous stimuli can be long lasting, even when immediate threat and the associated amygdala modulation have subsided.
    Neurobiology of Learning and Memory 09/2014; 113. DOI:10.1016/j.nlm.2014.01.016
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    • "In sum, the explicit behavioral measure demonstrated that the conditioning effect of the CS+ is generalized to its similar version, whereas the physiological and implicit behavioral measure showed a specific effect of conditioning which influences selectively the CS+ but not its similar version. Consistent with Li et al. (2008), our findings showed that emotional learning can enhance the discrimination between similar stimuli at both behavioral (reaction time) and physiological levels (inspiration and skin conductance); however by contrast Li et al. (2008) found an increase of the accuracy of the behavioral choices in the triangular test induced by aversive conditioning, while participants' explicit discrimination was not increased in our study after the appetitive conditioning. Many factors could explain this absence of effect (e.g., number of trials, number of participants, odor choice). "
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    ABSTRACT: Stimuli associated with emotional events signal the presence of potentially relevant situations, thus learning to rapidly identify this kind of stimuli can be highly beneficial. It has been demonstrated that individuals acquire a better perceptual representation of stimuli associated with negative and threatening emotional events. Here we investigated whether the same process occurs for stimuli associated with positive and rewarding emotional events. We used an appetitive Pavlovian conditioning paradigm during which one of two perceptually non-distinguishable odors was associated with a rewarding taste (i.e., chocolate). We investigated whether appetitive conditioning could improve the recognition of the odor associated with the reward, rendering it discriminable from its similar version that was never associated with the reward. Results revealed a dissociation between explicit perception and physiological reactions. Although participants were not able to explicitly perceive a difference, they reacted faster, inhaled more and had higher skin conductance responses when confronted with the reward-associated odor compared to its similar version that was never associated with the reward. Our findings have demonstrated that positive emotional associations can improve the implicit perceptual representation of odors, by triggering different physiological responses to odors that do not seem to be otherwise distinguishable.
    Frontiers in Behavioral Neuroscience 05/2014; 8:158. DOI:10.3389/fnbeh.2014.00158
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