The distributed circuit within the piriform cortex makes odor discrimination robust

Recent work in the anterior piriform cortex (aPCX) has demonstrated that cortical odor receptive fields are highly dynamic, showing rapid changes of both firing rate and temporal patterning within relatively few inhalations of an odor, despite relatively maintained, patterned input from olfactory bulb mitral/tufted cells. The present experiment examined the precision (odor-specificity) of this receptive field plasticity and compared it with the primary cortical afferent, olfactory bulb mitral/tufted cells. Adult Long-Evans hooded rats, urethan anesthetized and freely breathing, were used for single-unit recording from mitral/tufted and aPCX layer II/III neurons. Partial mapping of receptive fields to alkane odors (pentane, heptane, and nonane) was performed before and immediately after habituation (50-s exposure) to one of the alkanes. The results demonstrated that odor habituation of aPCX responses was odor specific, with minimal cross-habituation between alkanes differing by as few as two carbons. Mitral/tufted cells, however, showed strong cross-habituation within the odor set with the most profound cross effects to carbon chains shorter than the habituating stimulus. The results suggest that although mitral/tufted cells and aPCX neurons have roughly similar odor receptive fields, aPCX neurons have significantly better odor discrimination within their receptive field. The results have important implications for understanding the underlying bases of receptive fields in olfactory system neurons and the mechanisms of odor discrimination and memory.

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Locus Coeruleus Activation Patterns Differentially Modulate Odor Discrimination Learning and Odor Valence in Rats

Cerebral Cortex Communications ◽

10.1093/texcom/tgab026 ◽

2021 ◽

Author(s):

Abhinaba Ghosh ◽

Faghihe Massaeli ◽

Kyron D Power ◽

Tamunotonye Omoluabi ◽

Sarah E Torraville ◽

...

Keyword(s):

Locus Coeruleus ◽

Discrimination Learning ◽

Basolateral Amygdala ◽

Piriform Cortex ◽

Sensory Information ◽

Odor Discrimination ◽

Mediated Learning ◽

Odor Aversion ◽

Activation Patterns ◽

Tonic Stimulation

Abstract The locus coeruleus (LC) produces phasic and tonic firing patterns that are theorized to have distinct functional consequences. However, how different firing modes affect learning and valence encoding of sensory information are unknown. Here we show bilateral optogenetic activation of rat LC neurons using 10-Hz phasic trains of either 300 msec or 10 sec accelerated acquisition of a similar odor discrimination. Similar odor discrimination learning was impaired by noradrenergic blockade in the piriform cortex (PC). However, 10-Hz phasic light-mediated learning facilitation was prevented by a dopaminergic antagonist in the PC, or by ventral tegmental area (VTA) silencing with lidocaine, suggesting a LC-VTA-PC dopamine circuitry involvement. Ten hertz tonic stimulation did not alter odor discrimination acquisition, and was ineffective in activating VTA DA neurons. For valence encoding, tonic stimulation at 25 Hz induced conditioned odor aversion, while 10-Hz phasic stimulations produced an odor preference. Both conditionings were prevented by noradrenergic blockade in the basolateral amygdala (BLA). Cholera Toxin B retro-labeling showed larger engagement of nucleus accumbens-projecting neurons in the BLA with 10-Hz phasic activation, and larger engagement of central amygdala projecting cells with 25-Hz tonic light. These outcomes argue that the LC activation patterns differentially influence both target networks and behavior.

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Decoding Odor Mixtures in the Dog Brain: An Awake fMRI Study

10.1101/754374 ◽

2019 ◽

Cited By ~ 2

Author(s):

Ashley Prichard ◽

Raveena Chhibber ◽

Jon King ◽

Kate Athanassiades ◽

Mark Spivak ◽

...

Keyword(s):

Piriform Cortex ◽

Brain Regions ◽

Odor Discrimination ◽

Neural Representation ◽

Neural Activation ◽

Sensory Stimuli ◽

High Performing ◽

Odor Processing ◽

Dog Brain ◽

Odor Mixtures

AbstractIn working and practical contexts, dogs rely upon their ability to discriminate a target odor from distracting odors and other sensory stimuli. Few studies have examined odor discrimination using non-behavioral methods or have approached odor discrimination from the dog’s perspective. Using awake fMRI in 18 dogs, we examined the neural mechanisms underlying odor discrimination between two odors and a mixture of the odors. Neural activation was measured during the presentation of a target odor (A) associated with a food reward, a distractor odor (B) associated with nothing, and a mixture of the two odors (A+B). Changes in neural activation during the presentations of the odor stimuli in individual dogs were measured over time within three regions known to be involved with odor processing: the caudate nucleus, the amygdala, and the olfactory bulbs. Average activation within the amygdala showed that dogs maximally differentiated between odor stimuli based on the stimulus-reward associations by the first run, while activation to the mixture (A+B) was most similar to the no-reward (B) stimulus. To identify the neural representation of odor mixtures in the dog brain, we used a random forest classifier to compare multilabel (elemental) vs. multiclass (configural) models. The multiclass model performed much better than the multilabel (weighted-F1 0.44 vs. 0.14), suggesting the odor mixture was processed configurally. Analysis of the subset of high-performing dogs based on their brain classification metrics revealed a network of olfactory information-carrying brain regions that included the amygdala, piriform cortex, and posterior cingulate. These results add further evidence for the configural processing of odor mixtures in dogs and suggest a novel way to identify high-performers based on brain classification metrics.

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Odor discrimination learning is correlated with reduced after-hyperpolarization in piriform cortex pyramidal cells

Neuroscience Letters ◽

10.1016/s0304-3940(97)90175-0 ◽

1997 ◽

Vol 237 ◽

pp. S43

Author(s):

D. Saar ◽

Y. Grossman ◽

E. Barkai

Keyword(s):

Discrimination Learning ◽

Piriform Cortex ◽

Pyramidal Cells ◽

Odor Discrimination

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Rapid, Experience-Induced Enhancement in Odorant Discrimination by Anterior Piriform Cortex Neurons

Journal of Neurophysiology ◽

10.1152/jn.00133.2003 ◽

2003 ◽

Vol 90 (1) ◽

pp. 65-72 ◽

Cited By ~ 85

Author(s):

Donald A. Wilson

Keyword(s):

Single Unit ◽

Piriform Cortex ◽

Receptive Fields ◽

Odor Discrimination ◽

Minimum Duration ◽

Anterior Piriform Cortex ◽

Single Unit Recordings ◽

Tufted Cells ◽

A Site ◽

Enormous Number

Current views of odorant discrimination by the mammalian olfactory system suggest that the piriform cortex serves as a site of odor object synthesis. Given the enormous number of odorant feature combinations possible in nature, however, it seems unlikely that cortical synthetic receptive fields (RFs) are innate but rather require experience for their formation. The present experiment addressed two issues. First, we made a direct comparison of mitral/tufted cell and anterior piriform cortex (aPCX) neuron abilities to discriminate odorant mixtures from their components to further test whether aPCX neurons can treat collections of features different from the features themselves (synthetic coding). Second, we attempted to determine the minimum duration of experience necessary for formation of cortical synthetic RFs. Single-unit recordings were made from mitral/tufted cells and aPCX layer II/III neurons in urethan-anesthetized rats. Cross-habituation between novel binary mixtures and their novel components was used to determine odor discrimination abilities. The results suggest that after ≥50 s of experience with a binary mixture, aPCX neurons can discriminate the mixture from its components, whereas mitral/tufted cells cannot. However, when limited to 10 s of experience with the mixture, aPCX neurons appear similar to mitral/tufted cells and do not discriminate mixtures from components. These results suggest experience-dependent synthetic processing in aPCX and suggest an important role for perceptual learning in normal odor discrimination.

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The Human Brain Representation of Odor Identification in Amnestic Mild Cognitive Impairment and Alzheimer's Dementia of Mild Degree

Frontiers in Neurology ◽

10.3389/fneur.2020.607566 ◽

2021 ◽

Vol 11 ◽

Author(s):

Grete Kjelvik ◽

Hallvard R. Evensmoen ◽

Thomas Hummel ◽

Knut Engedal ◽

Geir Selbæk ◽

...

Keyword(s):

Alzheimer’S Disease ◽

Alzheimer's Disease ◽

Cognitive Impairment ◽

Mild Cognitive Impairment ◽

Brain Activity ◽

Piriform Cortex ◽

Anterior Insula ◽

Amnestic Mild Cognitive Impairment ◽

Odor Discrimination ◽

The Right

Background: Odor identification (OI) ability is a suggested early biomarker of Alzheimer's disease. In this study, we investigated brain activity within the brain's olfactory network associated with OI in patients with amnestic mild cognitive impairment (aMCI) and mild Alzheimer's dementia (mAD) to uncover the neuronal basis of this impairment.Materials and Methods: Patients with aMCI (n = 11) or mAD (n = 6) and 28 healthy older adults underwent OI functional MRI (fMRI) at 3T, OI, odor discrimination, and cognitive tests and apolipoprotein-e4 (APOE4) genotyping. Eleven patients had cerebrospinal fluid (CSF) analyzed. Those with aMCI were followed for 2 years to examine conversion to dementia.Results: The aMCI/mAD group performed significantly worse on all OI tests and the odor discrimination test compared to controls. The aMCI/mAD group had reduced activation in the right anterior piriform cortex compared to the controls during OI fMRI [Gaussian random field (GRF) corrected cluster threshold, p < 0.05]. This group difference remained after correcting for age, sex education, and brain parenchymal fraction. This difference in piriform activity was driven primarily by differences in odor discrimination ability and to a lesser extent by OI ability. There was no group by odor discrimination/identification score interaction on brain activity. Across both groups, only odor discrimination score was significantly associated with brain activity located to the right piriform cortex. Brain activity during OI was not associated with Mini Mental Status Examination scores. At the group level, the aMCI/mAD group activated only the anterior insula, while the control group had significant activation within all regions of the olfactory network during OI fMRI. There was no association between brain activity during OI fMRI and total beta-amyloid levels in the CSF in the aMCI/mAD group.Conclusion: The OI impairment in aMCI/mAD patients is associated with significantly reduced activity in the piriform cortex compared to controls. Activation of downstream regions within the olfactory network is also significantly affected in the aMCI/mAD group, except the anterior insula, which is impinged late in the course of Alzheimer's disease. OI tests thus reflect Alzheimer's disease pathology in olfactory brain structures.

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