Terminal Nerve-Derived Neuropeptide Y Modulates Physiological Responses in the Olfactory Epithelium of Hungry Axolotls (Ambystoma mexicanum)

Abstract

The vertebrate brain actively regulates incoming sensory information, effectively filtering input and focusing attention toward environmental stimuli that are most relevant to the animal's behavioral context or physiological state. Such centrifugal modulation has been shown to play an important role in processing in the retina and cochlea, but has received relatively little attention in olfaction. The terminal nerve, a cranial nerve that extends underneath the lamina propria surrounding the olfactory epithelium, displays anatomical and neurochemical characteristics that suggest that it modulates activity in the olfactory epithelium. Using immunocytochemical techniques, we demonstrate that neuropeptide Y (NPY) is abundantly present in the terminal nerve in the axolotl (Ambystoma mexicanum), an aquatic salamander. Because NPY plays an important role in regulating appetite and hunger in many vertebrates, we investigated the possibility that NPY modulates activity in the olfactory epithelium in relation to the animal's hunger level. We therefore characterized the full-length NPY gene from axolotls to enable synthesis of authentic axolotl NPY for use in electrophysiological experiments. We find that axolotl NPY modulates olfactory epithelial responses evoked by L-glutamic acid, a food-related odorant, but only in hungry animals. Similarly, whole-cell patch-clamp recordings demonstrate that bath application of axolotl NPY enhances the magnitude of a tetrodotoxin-sensitive inward current, but only in hungry animals. These results suggest that expression or activity of NPY receptors in the olfactory epithelium may change with hunger level, and that terminal nerve-derived peptides modulate activity in the olfactory epithelium in response to an animal's changing behavioral and physiological circumstances.

Cannabinoid action in the olfactory epithelium

“…First steps in this direction would be a quantification of endocannabinoid levels in the OE combined with a detailed characterization of the involved mechanisms regarding re-uptake and enzymatic hydrolysis. Our finding that the ECS influences olfactory sensory input adds to a growing knowledge showing that the activity of ORNs is modulated by numerous compounds, including acetylcholine, adrenaline, ATP, dopamine, GnRH, and s-neuropeptide Y (4,(30)(31)(32)(33)(34)(35)(36).…”

The Endocannabinoid 2-Arachidonoyl-Glycerol Controls Odor Sensitivity in Larvae of Xenopus laevis

“…In agreement with this hypothesis, we found here that the expression of the 2-AG synthesis enzyme DAG lipase ␣ in SCs was increased, causing enhanced levels of 2-AG in the olfactory epithelium after food deprivation. Several studies have indeed been published dealing with the influence of the nutritious state on the neurophysiology of olfactory information processing, whereby an altered sensitivity of ORNs could indirectly be attributed to the effects of modulators such as neuropeptide Y, leptin, or orexin (Caillol et al, 2003;Getchell et al, 2006;Mousley et al, 2006). In the present study, we investigated detection thresholds to arginine, lysine, and methionine.…”

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

“…In addition, there are examples of peptidergic modulation in the olfactory system by efferent neurons. Centrifugal peptidergic modulation has been demonstrated in the olfactory epithelia of a salamander, where neuropeptide Y was shown to enhance responses evoked by a food-related odor in hungry animals (42). The peptide FMRFamide has been shown to modulate the activity of ORNs in the olfactory epithelium of the mouse and the salamander, but the circuitry is not clear (17,43).…”