No two roses smell exactly alike, but our brain accurately bundles these variations into a single percept `rose'. We found that ensembles of rat olfactory bulb neurons decorrelate complex mixtures that vary by as little as a single missing component, whereas olfactory (piriform) cortical neural ensembles perform pattern completion in response to an absent component, essentially filling in the missing information and allowing perceptual stability. This piriform cortical ensemble activity predicts olfactory perception.The need for perceptual discrimination must be balanced with the need for perceptual stability. Without an ability to ignore some differences between input patterns, nearly all experiences would be unique, with each presentation of a similar stimulus being devoid of previously acquired associations and meaning. Computational modeling and experimental data suggest that some cortical circuits balance discrimination and stability through the network emergent functions of pattern separation and pattern completion 1-5 . Simply put, pattern separation allows partially overlapping input patterns to be decorrelated and processed as being distinct. Pattern completion is a memory-based phenomenon 6 that allows degraded input patterns to be compared to existing templates and, if they are sufficiently close to those templates, `completed' and processed as a match. These processes have been examined in some detail in the hippocampal formation, where slight changes in the spatial distribution of visual cues can be completed to promote stability in hippocampal neuronal place fields and presumably stability in spatial maps and perception. With further change or degradation in the visual spatial patterns, hippocampal place fields shift, presumably along with spatial perception. In olfaction, the need for pattern separation and completion is particularly intense, as most natural odors derive from odorant mixtures, evoking complex spatiotemporal patterns of olfactory sensory neuron and olfactory bulb activity 7 . Given this complexity, it is rare for a given stimulus to always have the exact same components in the exact same proportions, yet it is possible for a noisy or degraded stimulus to reliably evoke a stable percept. On the other hand, if the component makeup changes sufficiently, discrimination ensues. Evidence for pattern completion would be consistent with the view of olfactory perception as an object-oriented sense, where sensation , from which components were removed (for example, 10c-1 (10 components with 1 removed), 10c-2 (10 components with 2 removed), etc.) or replaced (10cR1, 10cR2, etc). This core mixture and its subsets were repeatedly presented during testing, and, given the speed at which cortical units become familiarized to odor mixtures even under anesthesia 13 , it was assumed they were familiar to the rats. We examined aPCX single units responding to the odorant mixtures (two typical examples are shown in Fig. 1a). These units responded to several different mixture combinations, and a...

Chen CF, Barnes DC, Wilson DA. Generalized vs. stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats. J Neurophysiol 106: 3136 -3144, 2011. First published September 14, 2011 doi:10.1152/jn.00721.2011.-Experience shapes both central olfactory system function and odor perception. In piriform cortex, odor experience appears critical for synthetic processing of odor mixtures, which contributes to perceptual learning and perceptual acuity, as well as contributing to memory for events and/or rewards associated with odors. Here, we examined the effect of odor fear conditioning on piriform cortical single-unit responses to the learned aversive odor, as well as its effects on similar (overlapping mixtures) in freely moving rats. We found that odor-evoked fear responses were training paradigm dependent. Simple association of a condition stimulus positive (CSϩ) odor with foot shock (unconditioned stimulus) led to generalized fear (cue-evoked freezing) to similar odors. However, after differential conditioning, which included trials where a CSϪ odor (a mixture overlapping with the CSϩ) was not paired with shock, freezing responses were CSϩ odor specific and less generalized. Pseudoconditioning led to no odor-evoked freezing. These differential levels of stimulus control over freezing were associated with different training-induced changes in single-unit odor responses in anterior piriform cortex (aPCX). Both simple and differential conditioning induced a significant decrease in aPCX single-unit spontaneous activity compared with pretraining levels while pseudoconditioning did not. Simple conditioning enhanced mean receptive field size (breadth of tuning) of the aPCX units, while differential conditioning reduced mean receptive field size. These results suggest that generalized fear is associated with an impairment of olfactory cortical discrimination. Furthermore, changes in sensory processing are dependent on the nature of training and can predict the stimuluscontrolled behavioral outcome of the training. piriform cortex; fear conditioning; learning-induced plasticity THE OLFACTORY SYSTEM INVOLVES a memory-based odor processing function that allows its acuity to be constantly shaped by experience (Wilson and Stevenson 2006). This function enables animals to not only identify myriad novel odors and odor combinations in the environment but also to associate odors with their ecological significance, which is critical for adaptive behavior. Experience-dependent perceptual changes (perceptual learning) and their underlying neural plasticity have been reported across phylogeny from the first to third order neurons in the olfactory system (Davis 2004).

Odor perception is hypothesized to be an experience-dependent process involving the encoding of odor objects by distributed olfactory cortical ensembles. Olfactory cortical neurons coactivated by a specific pattern of odorant evoked input become linked through association fiber synaptic plasticity, creating a template of the familiar odor. In this way, experience and memory play an important role in odor perception and discrimination. In other systems, memory consolidation occurs partially via slow-wave sleep (SWS)-dependent replay of activity patterns originally evoked during waking. SWS is ideal for replay given hyporesponsive sensory systems, and thus reduced interference. Here, using artificial patterns of olfactory bulb stimulation in a fear conditioning procedure in the rat, we tested the effects of imposed post-training replay during SWS and waking on strength and precision of pattern memory. The results show that imposed replay during post-training SWS enhanced the subsequent strength of memory, whereas the identical replay during waking induced extinction. The magnitude of this enhancement was dependent on the timing of imposed replay relative to cortical sharp-waves. Imposed SWS replay of stimuli, which differed from the conditioned stimulus, did not affect conditioned stimulus memory strength but induced generalization of the fear memory to novel artificial patterns. Finally, post-training disruption of piriform cortex intracortical association fiber synapses, hypothesized to be critical for experience-dependent odor coding, also impaired subsequent memory precision but not strength. These results suggest that SWS replay in the olfactory cortex enhances memory consolidation, and that memory precision is dependent on the fidelity of that replay.