Nonassociative Plasticity Alters Competitive Interactions Among Mixture Components in Early Olfactory Processing

Overview

Journal Eur J Neurosci

Specialty Neurology

Date 2012 Nov 22

PMID 23167675

Citations 27

Authors

Fernando F Locatelli

Patricia C Fernandez

Francis Villareal

Kerem Muezzinoglu

Ramon Huerta

C Giovanni Galizia

Brian H Smith

Affiliations

Soon will be listed here.

Abstract

Experience-related plasticity is an essential component of networks involved in early olfactory processing. However, the mechanisms and functions of plasticity in these neural networks are not well understood. We studied nonassociative plasticity by evaluating responses to two pure odors (A and X) and their binary mixture using calcium imaging of odor-elicited activity in output neurons of the honey bee antennal lobe. Unreinforced exposure to A or X produced no change in the neural response elicited by the pure odors. However, exposure to one odor (e.g. A) caused the response to the mixture to become more similar to that of the other component (X). We also show in behavioral analyses that unreinforced exposure to A caused the mixture to become perceptually more similar to X. These results suggest that nonassociative plasticity modifies neural networks in such a way that it affects local competitive interactions among mixture components. We used a computational model to evaluate the most likely targets for modification. Hebbian modification of synapses from inhibitory local interneurons to projection neurons most reliably produced the observed shift in response to the mixture. These results are consistent with a model in which the antennal lobe acts to filter olfactory information according to its relevance for performing a particular task.

Citing Articles

Reinforcement expectation in the honeybee (): Can downshifts in reinforcement show conditioned inhibition?.

Mahoney S, Hosler J, Smith B Learn Mem. 2024; 31(5).

PMID: 38862176 PMC: 11199939. DOI: 10.1101/lm.053915.124.

Tyramine and its receptor modulate attention in honey bees ().

Latshaw J, Mazade R, Petersen M, Mustard J, Sinakevitch I, Wissler L Elife. 2023; 12.

PMID: 37814951 PMC: 10564449. DOI: 10.7554/eLife.83348.

Granger Causality Analysis of Transient Calcium Dynamics in the Honey Bee Antennal Lobe Network.

Paoli M, Antonacci Y, Albi A, Faes L, Haase A Insects. 2023; 14(6).

PMID: 37367355 PMC: 10299490. DOI: 10.3390/insects14060539.

Gain modulation and odor concentration invariance in early olfactory networks.

Marachlian E, Huerta R, Locatelli F PLoS Comput Biol. 2023; 19(6):e1011176.

PMID: 37343029 PMC: 10317235. DOI: 10.1371/journal.pcbi.1011176.

Novelty detection in early olfactory processing of the honey bee, Apis mellifera.

Lei H, Haney S, Jernigan C, Guo X, Cook C, Bazhenov M PLoS One. 2022; 17(3):e0265009.

PMID: 35353837 PMC: 8967009. DOI: 10.1371/journal.pone.0265009.

References

Yu D, Ponomarev A, Davis R . Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron. 2004; 42(3):437-49. DOI: 10.1016/s0896-6273(04)00217-x. View

Peele P, Ditzen M, Menzel R, Galizia C . Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2006; 192(10):1083-103. DOI: 10.1007/s00359-006-0152-3. View

Bitterman M, Menzel R, Fietz A, Schafer S . Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol. 1983; 97(2):107-19. View

Huerta R, Sanchez-Montanes M, Corbacho F, Siguenza J . A central pattern generator to control a pyloric-based system. Biol Cybern. 2000; 82(1):85-94. DOI: 10.1007/PL00007963. View

Cleland T, Morse A, Yue E, Linster C . Behavioral models of odor similarity. Behav Neurosci. 2002; 116(2):222-31. DOI: 10.1037//0735-7044.116.2.222. View

Rath L, Galizia C, Szyszka P . Multiple memory traces after associative learning in the honey bee antennal lobe. Eur J Neurosci. 2011; 34(2):352-60. DOI: 10.1111/j.1460-9568.2011.07753.x. View

Wilson D, Linster C . Neurobiology of a simple memory. J Neurophysiol. 2008; 100(1):2-7. DOI: 10.1152/jn.90479.2008. View

Smith B . Analysis of interaction in binary odorant mixtures. Physiol Behav. 1999; 65(3):397-407. DOI: 10.1016/s0031-9384(98)00142-5. View

Lubow R . Latent inhibition. Psychol Bull. 1973; 79(6):398-407. DOI: 10.1037/h0034425. View

10.

Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M . Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci. 2003; 23(33):10495-502. PMC: 6740930. View

11.

Hammer M . The neural basis of associative reward learning in honeybees. Trends Neurosci. 1997; 20(6):245-52. DOI: 10.1016/s0166-2236(96)01019-3. View

12.

Hu A, Zhang W, Wang Z . Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway. Proc Natl Acad Sci U S A. 2010; 107(22):10262-7. PMC: 2890443. DOI: 10.1073/pnas.0914912107. View

13.

Wilson R, Turner G, Laurent G . Transformation of olfactory representations in the Drosophila antennal lobe. Science. 2003; 303(5656):366-70. DOI: 10.1126/science.1090782. View

14.

Winnington A, Napper R, Mercer A . Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J Comp Neurol. 1996; 365(3):479-90. DOI: 10.1002/(SICI)1096-9861(19960212)365:3<479::AID-CNE10>3.0.CO;2-M. View

15.

Muller U, Hildebrandt H . Nitric oxide/cGMP-mediated protein kinase A activation in the antennal lobes plays an important role in appetitive reflex habituation in the honeybee. J Neurosci. 2002; 22(19):8739-47. PMC: 6757786. View

16.

Grunbaum L, Muller U . Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J Neurosci. 1998; 18(11):4384-92. PMC: 6792810. View

17.

Smith B . The role of attention in learning about odorants. Biol Bull. 1996; 191(1):76-83. DOI: 10.2307/1543065. View

18.

Sachse S, Rappert A, Galizia C . The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci. 1999; 11(11):3970-82. DOI: 10.1046/j.1460-9568.1999.00826.x. View

19.

Ashraf S, McLoon A, Sclarsic S, Kunes S . Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell. 2006; 124(1):191-205. DOI: 10.1016/j.cell.2005.12.017. View

20.

Strausfeld N, Hildebrand J . Olfactory systems: common design, uncommon origins?. Curr Opin Neurobiol. 1999; 9(5):634-9. DOI: 10.1016/S0959-4388(99)00019-7. View