The differential requirement of mushroom body α/β subdivisions in long-term memory retrieval in Drosophila

Cheng Huang1,3, Pengzhi Wang1,4, Zhiyong Xie1, Lianzhang Wang1, Yi Zhong1,2()

PDF(693 KB)
PDF(693 KB)
Protein Cell ›› 2013, Vol. 4 ›› Issue (7) : 512-519. DOI: 10.1007/s13238-013-3035-8
RESEARCH ARTICLE

The differential requirement of mushroom body α/β subdivisions in long-term memory retrieval in Drosophila

  • Cheng Huang1,3, Pengzhi Wang1,4, Zhiyong Xie1, Lianzhang Wang1, Yi Zhong1,2()
Author information +
History +

Abstract

The mushroom body (MB), a bilateral brain structure possessing about 2000-2500 neurons per hemisphere, plays a central role in olfactory learning and memory in Drosophila melanogaster. Extensive studies have demonstrated that three major types of MB neurons (α/β, α’/β’ and γ) exhibit distinct functions in memory processing, including the critical role of approximately 1000 MB α/β neurons in retrieving long-term memory. Inspired by recent findings that MB α/β neurons can be further divided into three subdivisions (surface, posterior and core) and wherein the α/β core neurons play an permissive role in long-term memory consolidation, we examined the functional differences of all the three morphological subdivisions of MB α/β by temporally precise manipulation of their synaptic outputs during long-term memory retrieval. We found the normal neurotransmission from a combination of MB α/β surface and posterior neurons is necessary for retrieving both aversive and appetitive long-term memory, whereas output from MB α/β posterior or core subdivision alone is dispensable. These results imply a specific requirement of about 500 MB α/β neurons in supporting long-term memory retrieval and a further functional partitioning for memory processing within the MB α/β region.

Keywords

memory retrieval / neural circuits / aversive olfactory conditioning / appetitive olfactory conditioning / mushroom body

Cite this article

Download citation ▾
Cheng Huang, Pengzhi Wang, Zhiyong Xie, Lianzhang Wang, Yi Zhong. The differential requirement of mushroom body α/β subdivisions in long-term memory retrieval in Drosophila. Prot Cell, 2013, 4(7): 512‒519 https://doi.org/10.1007/s13238-013-3035-8

References

[1] Aso, Y., Grubel, K., Busch, S., Friedrich, A.B., Siwanowicz, I., and Tanimoto, H. (2009). The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23, 156-172 .10.1080/01677060802471718
[2] Blum, A.L., Li, W., Cressy, M., and Dubnau, J. (2009). Short- and longterm memory in Drosophila require cAMP signaling in distinct neuron types. Curr Biol 19, 1-10 .10.1016/j.cub.2009.07.016
[3] Chen, C.C., Wu, J.K., Lin, H.W., Pai, T.P., Fu, T.F., Wu, C.L., Tully, T., and Chiang, A.S. (2012). Visualizing long-term memory formation in two neurons of the Drosophila brain. Science 335, 678-685 .10.1126/science.1212735
[4] Christiansen, F., Zube, C., Andlauer, T.F., Wichmann, C., Fouquet, W., Owald, D., Mertel, S., Leiss, F., Tavosanis, G., Luna, A.F., . (2011). Presynapses in Kenyon cell dendrites in the mushroom body calyx of Drosophila. J Neurosci 31, 9696-9707 .10.1523/JNEUROSCI.6542-10.2011
[5] Crittenden, J.R., Skoulakis, E.M., Han, K.A., Kalderon, D., and Davis, R.L. (1998). Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5, 38-51 .
[6] de Belle, J.S., and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695 .10.1126/science.8303280
[7] Dubnau, J. and Chiang, A.S. (2013). System memory consolidation in Drosophila. Curr Opin Neurobiol 23, 84-91 .10.1016/j.conb.2012.09.006
[8] Dubnau, J., Grady, L., Kitamoto, T., and Tully, T. (2001). Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411, 476-480 .10.1038/35078077
[9] Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat Rev Neurosci 4, 266-275 .10.1038/nrn1074
[10] Huang, C., Zheng, X., Zhao, H., Li, M., Wang, P., Xie, Z., Wang, L., and Zhong, Y. (2012). A permissive role of mushroom body α/β core neurons in long-term memory consolidation in Drosophila. Curr Biol 22, 1981-1989 .10.1016/j.cub.2012.08.048
[11] Isabel, G., Pascual, A., and Preat, T. (2004). Exclusive consolidated memory phases in Drosophila. Science 304, 1024-1027 .10.1126/science.1094932
[12] Johard, H.A., Enell, L.E., Gustafsson, E., Trifilieff, P., Veenstra, J.A. and N?ssel, D.R. (2008). Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J Comp Neurol 507, 1479-1496 .10.1002/cne.21636
[13] Keene, A.C., Krashes, M.J., Leung, B., Bernard, J.A. and Waddell, S. (2006). Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr Biol 16, 1524-1530 .10.1016/j.cub.2006.06.022
[14] Kim, Y., Lee, H., and Han, K. (2007). D1 Dopamine Receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila, J Neurosci 27, 7640-7647 .10.1523/JNEUROSCI.1167-07.2007
[15] Kitamoto, T. (2001). Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47, 81-92 .10.1002/neu.1018
[16] Krashes, M.J., DasGupta, S, Vreede, A., White, B., Armstrong, J.D. and Waddell, S. (2009). A neural circuit mechanism integrating motivational state with memory expression in Drosophila . Cell 139, 416-427 .10.1016/j.cell.2009.08.035
[17] Krashes, M.J., Keene, A.C., Leung, B., Armstrong, J.D., and Waddell, S. (2007). Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53, 103-115 .10.1016/j.neuron.2006.11.021
[18] Krashes, M.J., and Waddell, S. (2008). Rapid consolidation to a radish and protein synthesis-dependent long-term memory after singlesession appetitive olfactory conditioning in Drosophila. J Neurosci 28, 3103-3113 .10.1523/JNEUROSCI.5333-07.2008
[19] Lee, T., Lee, A., and Luo, L. (1999). Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065-4076 .
[20] Pai, T.P., Chen, C.C., Lin H.H., Chin A.L., Lai, J.S.Y., Lee, P.T., Tully, T. & ChiangA.S. (2013). Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation. Proc Natl Acad Sci U S A 110, 7898-7903 .10.1073/pnas.1216336110
[21] Perrat, P.N., DasGupta, S., Wang, J., Theurkauf, W., Weng, Z., Rosbash, M. and Waddell, S. (2013). Transposition-Driven genomic heterogeneity in the Drosophila brain. Science 340, 91-95 .10.1126/science.1231965
[22] Pitman, J.L., Huetteroth, W., Burke, C.J., Krashes, M.J., Lai, S.L., Lee, T. and Waddell, S. (2011). A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body. Curr Biol 21, 855-861 .10.1016/j.cub.2011.03.069
[23] Qin, H., Cressy, M., Li, W., Coravos, J.S., Izzi, S.A., and Dubnau, J. (2012). Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Curr Biol 22, 608-614 .10.1016/j.cub.2012.02.014
[24] Séjourné, J., Pla?ais, P.Y., Aso, Y., Siwanowicz, I., Trannoy, S, Thoma, V., Tedjakumala, S.R., Rubin, G.M., Tchénio, P., Ito, K., . (2011). Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat Neurosci 14, 903-910 .10.1038/nn.2846
[25] Silva, A.J., Zhou, Y., Rogerson, T., Shobe, J. and Balaji, J. (2009). Molecular and cellular approaches to memory allocation in neural circuits. Science 326, 391-395 .10.1126/science.1174519
[26] Sinakevitch, I., Grau, Y., Strausfeld, N.J., and Birman, S. (2010). Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila. Neural Dev 5, 10-30 .10.1186/1749-8104-5-10
[27] Small, S.A., Schobel, S.A., Buxton, R.B., Witter, M.P. and Barnes, C.A. (2011). A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12, 585-601 .10.1038/nrn3085
[28] Tanaka, N.K., Tanimoto, H., and Ito, K. (2008). Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508, 711-755 .10.1002/cne.21692
[29] Trannoy, S., Redt-Clouet, C., Dura, J.M., and Preat, T. (2011). Parallel processing of appetitive short- and long-term memories in Drosophila. Curr Biol 21, 1647-1653 .10.1016/j.cub.2011.08.032
[30] Tully, T., Preat, T., Boynton, S.C., and Del Vecchio, M. (1994). Genetic dissection of consolidated memory in Drosophila. Cell 79, 35-47 .10.1016/0092-8674(94)90398-0
[31] Tully, T., and Quinn, W.G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157, 263-277 .10.1007/BF01350033
[32] Tye, K.M. and Deisseroth, K. (2012). Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci 13, 251-266 .10.1038/nrn3171
[33] van Strien, N.M., Cappaert, N.L. and Witter, M.P. (2009). The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10, 272-282 .10.1038/nrn2614
[34] Wang, Y., Mamiya, A., Chiang, A., and Zhong, Y. (2008). Imaging of an Early Memory Trace in the Drosophila Mushroom Body. J Neurosci 28, 4368-4376 .10.1523/JNEUROSCI.2958-07.2008
[35] Wu, C.L., Shih, M.F., Lai, J.S., Yang, H.T., Turner, G.C., Chen, L. and Chiang, A.S. (2011). Heterotypic gap junctions between two neurons in the drosophila brain are critical for memory. Curr Biol 21, 848-854 .10.1016/j.cub.2011.02.041
[36] Wu, C.L., Xia, S., Fu, T.F., Wang, H., Chen, Y.H., Leong, D., Chiang, A.S. and Tully, T. (2007). Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10, 1578-1586 .10.1038/nn2005
AI Summary AI Mindmap
PDF(693 KB)

Accesses

Citations

Detail

Sections
Recommended

/