Cannabinoids Regulate Sensory Processing in Early Olfactory and Visual Neural Circuits

Heinbockel, Thomas; Straiker, Alex

doi:10.3389/fncir.2021.662349

Cited by 7 publications

(4 citation statements)

References 175 publications

(285 reference statements)

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“…Both AEA and 2-AG amplify the response of primary chemosensory cells, such as the sweet-taste cells in the tongue (Yoshida et al, 2010, 2013), which may help to explain increased consumption of sweet foods and liquids. Cannabinoids can also increase the sensitivity of the mammalian olfactory system as measured during food-odor exploration (Heinbockel & Straiker, 2021; Nogi et al, 2020; Soria-Gómez et al, 2014). We observed an analogous effect in C. elegans , in that AEA alters the sensitivity of a primary chemosensory neuron, AWC.…”

Section: Discussionmentioning

confidence: 99%

The conserved endocannabinoid anandamide modulates olfactory sensitivity to induce hedonic feeding in C. elegans

Levichev

Faumont

et al. 2021

Preprint

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The mammalian endocannabinoid system, comprised of the endocannabinoids AEA (N-arachidonoyl-ethanolamine) and 2-AG (2-Arachidonoylglycerol), their receptors, CB1 and CB2, and their metabolic enzymes, is believed to integrate internal energy state and external food cues to modulate feeding. For example, cannabinoids can increase preference for more palatable, calorically dense food: a response called hedonic amplification, colloquially known as "the munchies." In mammals, cannabinoids can increase sensitivity to odors and sweet tastes, which may underlie amplification. We use C. elegans, an omnivorous bacterivore, as a model in which to investigate the neurophysiology of hedonic amplification. We found that exposure to AEA increases the worms' preference for strongly preferred (more palatable) bacteria over weakly preferred (less palatable) bacteria, mimicking hedonic amplification in mammals. Furthermore, AEA acts bidirectionally, increasing consumption of strongly preferred bacteria while decreasing consumption of weakly preferred bacteria. We also found that deletion of the putative CB1 homolog, npr-19, eliminates hedonic amplification, which can be rescued by expression of wild type npr-19 or human CB1, establishing a humanized worm for cannabinoid signaling studies. Deletion of the olfactory neuron AWC, which directs chemotaxis to food, abolishes hedonic amplification. Consistent with this finding, calcium imaging revealed that AEA bidirectionally modulates AWC activity, increasing its responses to strongly preferred food and decreasing its response for weakly preferred food. In a GFP expression analysis, we found that npr-19 is expressed in approximately 21 neuron classes but, surprisingly, not in AWC. Although AEA's effect could be mediated by NPR-19-expressing neurons presynaptic to AWC, nearly complete elimination of fast synaptic transmission, via the mutation unc-13(e51), had no effect on modulation. Instead, it appears that AEA modulates AWC by activating one or more npr-19-expressing neurons that release a diffusible neuromodulator to which AWC is sensitive.

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Section: Discussionmentioning

confidence: 99%

The conserved endocannabinoid anandamide modulates olfactory sensitivity to induce hedonic feeding in C. elegans

Levichev

Faumont

et al. 2021

Preprint

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“…Neuronal oscillations play fundamental roles in olfactory circuits, with oscillations in the beta and gamma range being strongly linked to sensory perception and attentive states [48][49][50] . We examined the effect of CB1R blockade on aPC local field potential (LFP) oscillations in the theta (4-12 Hz), beta (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30), and gamma (30-80 Hz) frequency bands. Systemic injections of Rim increased the power of the signal in all frequency bands but mainly in the frequency range corresponding to low gamma (Fig.…”

Section: Systemic Cb1r Blockade Promotes Gamma Oscillations In the Apcmentioning

confidence: 99%

“…For instance, it was established more than 50 years ago that cannabis consumption is associated with altered sensory perception 29 . Yet, besides this effect induced by exogenous CB1R ligands, little is known about the physiological actions of endocannabinoids in sensory processing, including in olfaction 25,30 .…”

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confidence: 99%

Endogenous cannabinoids in the piriform cortex tune olfactory perception

Terral,

Harrell,

Lepousez

et al. 2024

Nat Commun

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Sensory perception depends on interactions between external inputs transduced by peripheral sensory organs and internal network dynamics generated by central neuronal circuits. In the sensory cortex, desynchronized network states associate with high signal-to-noise ratio stimulus-evoked responses and heightened perception. Cannabinoid-type-1-receptors (CB1Rs) - which influence network coordination in the hippocampus - are present in anterior piriform cortex (aPC), a sensory paleocortex supporting olfactory perception. Yet, how CB1Rs shape aPC network activity and affect odor perception is unknown. Using pharmacological manipulations coupled with multi-electrode recordings or fiber photometry in the aPC of freely moving male mice, we show that systemic CB1R blockade as well as local drug infusion increases the amplitude of gamma oscillations in aPC, while simultaneously reducing the occurrence of synchronized population events involving aPC excitatory neurons. In animals exposed to odor sources, blockade of CB1Rs reduces correlation among aPC excitatory units and lowers behavioral olfactory detection thresholds. These results suggest that endogenous endocannabinoid signaling promotes synchronized population events and dampen gamma oscillations in the aPC which results in a reduced sensitivity to external sensory inputs.

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“…This plays a critical role in physiological as well as emotional homeostasis as it relates to reproductive and neuroendocrine regulation. In humans, the olfactory pathway starts in nasal olfactory structures that detect odorants in the air (reviewed in Heinbockel and Straiker, 2021 ). In the nasal cavity, the olfactory epithelium houses a large population of olfactory sensory neurons (OSNs) with odorant receptor proteins in the membranes of their dendritic cilia.…”

Section: Olfactory Neuroscience and Anosmia/hyposmiamentioning

confidence: 99%

Chemical Constituents of Essential Oils Used in Olfactory Training: Focus on COVID-19 Induced Olfactory Dysfunction

Koyama

Heinbockel

2022

Front. Pharmacol.

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The recent increase in the number of patients with post-viral olfactory dysfunction (PVOD) following the outbreak of COVID-19 has raised the general interest in and concern about olfactory dysfunction. At present, no clear method of treatment for PVOD has been established. Currently the most well-known method to improve the symptoms of olfactory dysfunction is “olfactory training” using essential oils. The essential oils used in olfactory training typically include rose, lemon, clove, and eucalyptus, which were selected based on the odor prism hypothesis proposed by Hans Henning in 1916. He classified odors based on six primary categories or dimensions and suggested that any olfactory stimulus fits into his smell prism, a three-dimensional space. The term “olfactory training” has been used based on the concept of training olfactory sensory neurons to relearn and distinguish olfactory stimuli. However, other mechanisms might contribute to how olfactory training can improve the recovery of the olfactory sense. Possibly, the essential oils contain chemical constituents with bioactive properties that facilitate the recovery of the olfactory sense by suppressing inflammation and enhancing regeneration. In this review, we summarize the chemical constituents of the essential oils of rose, lemon, clove, and eucalyptus and raise the possibility that the chemical constituents with bioactive properties are involved in improving the symptoms of olfactory dysfunction. We also propose that other essential oils that contain chemical constituents with anti-inflammatory effects and have binding affinity with SARS-CoV-2 can be new candidates to test their efficiencies in facilitating the recovery.

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Cannabinoids Regulate Sensory Processing in Early Olfactory and Visual Neural Circuits

Cited by 7 publications

References 175 publications

The conserved endocannabinoid anandamide modulates olfactory sensitivity to induce hedonic feeding in C. elegans

The conserved endocannabinoid anandamide modulates olfactory sensitivity to induce hedonic feeding in C. elegans

Endogenous cannabinoids in the piriform cortex tune olfactory perception

Chemical Constituents of Essential Oils Used in Olfactory Training: Focus on COVID-19 Induced Olfactory Dysfunction

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