Learning-induced sensory plasticity of mouse olfactory epithelium
https://doi.org/10.18699/VJ18.452
Abstract
Traditionally, studies of the neurobiology of learning and memory focus on the circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulusspecifc changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. In this study, we investigated the effect of olfactory associative training on the functional activity of olfactory epithelium neurons in response to an indifferent stimulus (orange oil). It was found that such a peripheral structure of the olfactory system of adult mice as the olfactory epithelium (OE) demonstrates experiencedependent plasticity. In our experiment, associative learning led to changes in the patterns of OE cell activation in response to orange oil in comparison with the control group and animals that were given odor without reinforcement. To interpret the results obtained, we compared the distribution of MRI contrast across the zones of OE in response to a conditioned odor in trained animals and in control animals that were given orange oil at three concentrations: original (used for conditioning), 4fold higher and 4fold lower. Since the OE activation patterns obtained coincided in the group of trained animals and controls, which were stimulated with orange oil at the 4fold higher concentration, it can be concluded that associative conditioning increased the sensitivity of the OE to the conditioned stimulus. The observed increase in OE response to orange oil may be the result of neurogenesis, i. e. the maturation of new olfactory neurons responsive to this stimulus, or the consequence of an increase in individual sensitivity of each OE neuron. Based on data of MRI contrast accumulation in mouse OE, the sensory plasticity way in learninginduced increase in sensitivity of OE to conditioned stimulus is more possible. Thus, the sensory plasticity of the OE plays a signifcant role in the formation of the neuronal response to the provision of an initially indifferent odor and is part of the adaptive responses to the environmental changing.
About the Authors
A. V. RomashchenkoRussian Federation
Novosibirsk
Р. Е. Kireeva
Russian Federation
Novosibirsk
M. В. Sharapova
Russian Federation
Novosibirsk
Т. A. Zapara
Russian Federation
Novosibirsk
A. S. Ratushnyak
Russian Federation
Novosibirsk
References
1. Abraham N.M., Vincis R., Lagier S., Rodriguez I., Carleton A. Long term functional plasticity of sensory inputs mediated by olfactory learning. Elife. 2014;(3):e02109. DOI 10.7554/eLife.02109.
2. Aoki I., Wu Y.J.L., Silva A.C., Lynch R.M., Koretsky A.P. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage. 2004;22(3):1046-1059. DOI 10.1016/j.neuroimage.2004.03.031.
3. Bieszczad K.M., Weinberger N.M. Extinction reveals that primary sensory cortex predicts reinforcement outcome. Eur. J. Neurosci. 2012; 35(4):598¬613. DOI 10.1111/j.1460-9568.2011.07974.x.
4. Carey R.M., Verhagen J.V., Wesson D.W., Pírez N., Wachowiak M. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J. Neurophysiol. 2009;101(2):1073-1088. DOI 10.1152/jn.90902.2008.
5. Gao E., Suga N. Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc. Natl. Acad. Sci. USA. 2000;97(14):8081-8086. DOI 10.1073/pnas.97.14.8081.
6. Getchell T.V. Functional properties of vertebrate olfactory receptor neurons. Physiol. Rev. 1986;66(3):772-818. DOI 10.1152/physrev.1986.66.3.772.
7. Headley D.B., Weinberger N.M. Relational associative learning induces cross-modal plasticity in early visual cortex. Cerebral Cortex. 2013;25(5):1306-1318. DOI 10.1093/cercor/bht325.
8. Jones S.V., Choi D.C., Davis M., Ressler K.J. Learning-dependent structural plasticity in the adult olfactory pathway. J. Neurosci. 2008; 28(49):13106-13111. DOI 10.1523/JNEUROSCI.4465-08.2008.
9. Kass M.D., Rosenthal M.C., Pottackal J., McGann J.P. Fear learning enhances neural responses to threat-predictive sensory stimuli. Science. 2013;342(6164):1389-1392. DOI 10.1126/science.1244916.
10. McGann J.P. Associative learning and sensory neuroplasticity: how does it happen and what is it good for? Learn. Mem. 2015;22(11):567- 576. DOI 10.1101/lm.039636.115.
11. Moulton D.G., Beidler L.M. Structure and function in the peripheral olfactory system. Physiol. Rev. 1967;47(1):1-52. DOI 10.1152/physrev.1967.47.1.1.
12. Pautler R.G. In vivo, trans-synaptic tract¬tracing utilizing manganeseenhanced magnetic resonance imaging (MEMRI). NMR Biomed. 2004;17(8):595-601. DOI 10.1002/nbm.942.
13. Pautler R.G., Koretsky A.P. Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage. 2002;16(2):441-448.
14. Polley D.B., Heiser M.A., Blake D.T., Schreine C.E., Merzenich M.M. Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proc. Natl. Acad. Sci. USA. 2004; 101(46):16351-16356. DOI 10.1073/pnas.0407586101.
15. Schwob J.E., Youngentob S.L., Mezza R.C. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 1995;359(1):15-37. DOI 10.1002/cne.903590103.
16. Smith K.D.B., Kallhoff V., Zheng H., Pautler R.G. In vivo axonal transport rates decrease in a mouse model of Alzheimer’s disease. Neuroimage. 2007;35(4):1401-1408. DOI 10.1016/j.neuroimage.2007. 01.046.
17. Weinberger N.M. Reconceptualizing the Primary Auditory Cortex: Learning, Memory and Specifc Plasticity. In: Winer J.A., Schreiner C.E. (Eds.). The Auditory Cortex. N. Y.: Springer, 2011;465-491. DOI 10.1007/978-1-4419-0074-6_22.
18. Zhang X., Firestein S. The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 2002;5(2):124-133. DOI 10.1038/nn800.
19. Zhang Y., Zhao Y., Zhu X., Sun X., Zhou X. Refning cortical representation of sound azimuths by auditory discrimination training. J. Neurosci. 2013;33(23):9693-9698. DOI 10.1523/JNEUROSCI.0158-13.2013.