在快速變化的環境中，動物必須獲取足夠的周圍信息以執行適當的行為。動物也會發展屬於自己物種的交流模式來傳達及傳達與接收資訊。透過“社交學習”模式使完全未知的動物得以向有經驗的同伴來學習正確的資訊。即使社交學習比起自我學習更有效率且容易獲得，但由於動物間信息傳遞相當複雜，其分子與機制還沒得到詳細解答。恐懼是誘導動物進行聯想學習的動機之一，我們利用後天性恐懼作為社交學習的研究模式。我們初步研究已證實受過厭惡性嗅覺制約訓練的老師果蠅能夠將對於特定氣味恐懼訊息傳遞給未被訓練過的學生果蠅。進一步研究確立特定的嗅覺受體以及腦中特定區域在調控後天恐懼的社交學習行為。此外處理社交行為和進行躲避行為以迴避受壓力的果蠅的神經元位於同一大腦區域，表示果蠅的腦部存在著一個中心，將外部的刺激與內部狀態進行整合以產生逃避危險的行為。果蠅模式上，原先只有相同物種間才能進行社交學習來傳遞恐懼資訊。然而近期我們發現，兩相異物種若經過先前交流經驗，就可以進行跨物種之間的社交行為。我們也進一步的確立了跨物種間交流的神經機制與同物種間社交學習機制是有相異之處。
最後，我們探討與社交障礙相關的病症與社交學習之關係。經過社交隔離狀態無法進行社交學習，更嚴重的是長期隔離狀態引發類憂鬱症行為。然而社交學習的障礙可以藉由生活環境改變或是藥物達到某種程度的改善；長時間隔離誘導類憂鬱症特定症狀能經特定藥物達到改善。
總而言之，我的研究表明了動物可以藉由社交學習行為習得正確訊息以做出適當的行為，且其中的機制與傳統的學習和記憶是不同的。重要的是，我的研究有機會更深入研究動物間複雜且的社會行為。

Animals communicate with each other through social activities. Social learning enables animals to learn from the experienced animals. In Drosophila, fruit flies transmit the environmental information to direct proper behaviors. Although social learning is more efficient than self-learning, the detailed cellular mechanism remains unknown. Previous studies from our lab have shown that socially-isolated condition disable social learning ability and cause depressive-like behaviors. Here, my research aims to explore the neural mechanism of social learning and isolation-induced depressive-like behaviors.
My preliminary results showed that trained flies (referred to as teachers) could transmit learned aversive information to the naïve flies (students), and this learned-fear information is species dependent. The neural circuit used to process learned social learning information is Or88a >VA1d> MBs >MBONs. Moreover, neurons used to process social learning and conduct avoidance behavior to escape from stressed flies are in the same brain region.
My results also suggested that socially-isolated flies cannot perceive learned-fear information through social learning. In addition to social learning deficit, solitary flies develop depressive-like behaviors, such as abnormal circadian rhythm, more ethanol consumption, and lower preference to sugar. However, isolation-induced depressive-like behaviors is reversible by keeping isolated flies back to the group. Simultaneously activating dopamine and serotonin receptors through drug treatment during isolation prevents isolation-induced social learning deficit. Taken together, my study provides an opportunity to study how isolated environment affect animal’s social learning.

Akalal, D.-B.G., Wilson, C.F., Zong, L., Tanaka, N.K., Ito, K., and Davis, R.L. (2006). Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learning & memory 13, 659-668.
Aso, Y., Hattori, D., Yu, Y., Johnston, R.M., Iyer, N.A., Ngo, T.-T., Dionne, H., Abbott, L., Axel, R., and Tanimoto, H. (2014a). The neuronal architecture of the mushroom body provides a logic for associative learning. elife 3, e04577.
Aso, Y., Sitaraman, D., Ichinose, T., Kaun, K.R., Vogt, K., Belliart-Guérin, G., Plaçais, P.-Y., Robie, A.A., Yamagata, N., and Schnaitmann, C. (2014b). Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. Elife 3, e04580.
Aso Y, Herb A, Ogueta M, Siwanowicz I, Templier T, Friedrich AB, Ito K, Scholz H, Tanimoto H (2012) Three dopamine pathways induce aversive odor memories with different stability. PLoS genetics 8:e1002768.
Bartelt RJ, Schaner AM, Jackson LL (1985) cis-Vaccenyl acetate as an aggregation pheromone inDrosophila melanogaster. Journal of chemical ecology 11:1747-1756.
Battesti M, Moreno C, Joly D, Mery F (2012) Spread of social information and dynamics of social transmission within Drosophila groups. Current biology : CB 22:309-313.
Bates AS, Schlegel P, Roberts RJV, Drummond N, Tamimi IFM, Turnbull R, Zhao X, Marin EC, Popovici PD, Dhawan S, Jamasb A, Javier A, Serratosa Capdevila L, Li F, Rubin GM, Waddell S, Bock DD, Costa M, Jefferis G (2020) Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain. Current biology : CB 30:3183-3199.e3186.
Bertolio, R., et al., Sterol regulatory element binding protein 1 couples mechanical cues and lipid metabolism. Nat. Commun. 10(1): 1326. (2019)
Blum MS (1969) Alarm Pheromones. Annual Review of Entomology 14:57-80.
Butterworth FM (1969) Lipids of Drosophila: a newly detected lipid in the male. Science (New York, NY) 163:1356-1357.
Bruchey, A. K., Jones, C. E. & Monfils, M. H. Fear conditioning by-proxy: social transmission of fear during memory retrieval. Behavioural brain research, 214(1), 80–84. (2010)
Chakraborty, T.S., et al., Sensory perception of dead conspecifics induces aversive cues and modulates lifespan through serotonin in Drosophila. Nat. Commun. 10(1): 2365. (2019)
Crossley S, Zuill E (1970) Courtship behaviour of some Drosophila melanogaster mutants. Nature 225:1064-1065.
Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Current biology : CB 15:1535-1547.
Dawson, E. H. et al. Social environment mediates cancer progression in Drosophila.
Nat. Commun. 9 (2018).
Dolan MJ, Belliart-Guérin G, Bates AS, Frechter S, Lampin-Saint-Amaux A, Aso Y, Roberts RJV, Schlegel P, Wong A, Hammad A, Bock D, Rubin GM, Preat T, Plaçais PY, Jefferis G (2018) Communication from Learned to Innate Olfactory Processing Centers Is Required for Memory Retrieval in Drosophila. Neuron 100:651-668.e658.
Dweck HKM, Ebrahim SAM, Thoma M, Mohamed AAM, Keesey IW, Trona F, Lavista-Llanos S, Svatoš A, Sachse S, Knaden M, Hansson BS (2015) Pheromones mediating copulation and attraction in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 112:E2829-E2835.
Depetris-Chauvin A, Galagovsky D, Grosjean Y (2015) Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila. Frontiers in Ecology and Evolution 3.
Fathinezhad Z, Sewell RDE, Lorigooini Z, Rafieian-Kopaei M (2019) Depression and Treatment with Effective Herbs. Current pharmaceutical design 25:738-745.
Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Current biology : CB 15:1548-1553.
Folkers E, Drain P, Quinn WG (1993) Radish, a Drosophila mutant deficient in consolidated memory. Proceedings of the National Academy of Sciences of the United States of America 90:8123-8127.
Ganguly-Fitzgerald, I., Donlea, J. & Shaw, P. J. Waking experience affects sleep need in Drosophila. Science 313, 1775–1781 (2006).
Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:217-220.
Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T, Benzer S (2007) Prandiology of Drosophila and the CAFE assay. Proceedings of the National Academy of Sciences 104:8253-8256.
Kacsoh BZ, Bozler J, Bosco G (2018) Drosophila species learn dialects through communal living. PLoS genetics 14:e1007430.
Kacsoh BZ, Lynch ZR, Mortimer NT, Schlenke TA (2013) Fruit flies medicate offspring after seeing parasites. Science (New York, NY) 339:947-950.
Kacsoh BZ, Bozler J, Ramaswami M, Bosco G (2015a) Social communication of predator-induced changes in Drosophila behavior and germ line physiology. eLife 4.
Kacsoh BZ, Bozler J, Hodge S, Bosco G (2019) Neural circuitry of social learning in Drosophila requires multiple inputs to facilitate inter-species communication. Communications biology 2:309.
Karlson P, LÜScher M (1959) ‘Pheromones’: a New Term for a Class of Biologically Active Substances. Nature 183:55-56.
Kandel E, Abel T (1995) Neuropeptides, adenylyl cyclase, and memory storage. Science (New York, NY) 268:825-826.
Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nature Reviews Neuroscience 8:341-354.
Keene AC, Krashes MJ, Leung B, Bernard JA, Waddell S (2006) Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr Biol 16:1524-1530.
Krstic D, Boll W, Noll M (2009) Sensory Integration Regulating Male Courtship Behavior in Drosophila. PLOS ONE 4:e4457.
LeDoux J (2003) The emotional brain, fear, and the amygdala. Cellular and molecular neurobiology 23:727-738.
LeDoux JE (2014) Coming to terms with fear. Proceedings of the National Academy of Sciences of the United States of America 111:2871-2878.
Lee P-T, Lin H-W, Chang Y-H, Fu T-F, Dubnau J, Hirsh J, Lee T, Chiang A-S (2011) Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila. Proceedings of the National Academy of Sciences 108:13794-13799.
Li, W. H. et al. Chronic social isolation signals starvation and reduces sleep in Drosophila. Nature 597, 239–244 (2021).
Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Current biology : CB 15:R700-713.
Masek P, Worden K, Aso Y, Rubin GM, Keene AC (2015) A dopamine-modulated neural circuit regulating aversive taste memory in Drosophila. Current biology : CB 25:1535-1541.
Masse NY, Turner GC, Jefferis GSXE (2009) Olfactory Information Processing in Drosophila. Current Biology 19:R700-R713.
McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science (New York, NY) 293:1330-1333.
O.Malkesman, R.Maay, A.Weizm, A.Weller. (2006). Aggressive behavior and HPA axis hormones after social isolation in adult rats of two different genetic animal models for depression. Behavioural Brain Research. Volume 175, Issue 2.
Quinn WG, Dudai Y (1976) Memory phases in Drosophila. Nature 262:576-577.
Quinn WG, Harris WA, Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 71:708-712.
Sarin S, Dukas R (2009) Social learning about egg-laying substrates in fruit flies. Proceedings Biological sciences 276:4323-4328.
Shohat-Ophir G, Kaun KR, Azanchi R, Mohammed H, Heberlein U (2012) Sexual deprivation increases ethanol intake in Drosophila. Science (New York, NY) 335:1351-1355.
Sivolap YP (2017) [Serotonin neurotrasmission and treatment options for depression]. Zhurnal nevrologii i psikhiatrii imeni SS Korsakova 117:174-177.
Sumpter D, Buhl J, Biro D, Couzin I (2008) Information transfer in moving animal groups. Theory in biosciences 127:177-186.
Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. The Journal of comparative neurology 508:711-755.
Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263-277.
Vogt K, Schnaitmann C, Dylla KV, Knapek S, Aso Y, Rubin GM, Tanimoto H (2014) Shared mushroom body circuits underlie visual and olfactory memories in Drosophila. eLife 3:e02395.
Vyacheslav A. Ryabov (2016) The study of acoustic signals and the supposed dolphins’ spoken language. St Petersburg State Polytechnical University Journal Physics and Mathematics 248(3):88-101.
Wicker-Thomas C, Guenachi I, Keita YF (2009) Contribution of oenocytes and pheromones to courtship behaviour in Drosophila. BMC biochemistry 10:21.
Xie Z, Huang C, Ci B, Wang L, Zhong Y (2013) Requirement of the combination of mushroom body γ lobe and α/β lobes for the retrieval of both aversive and appetitive early memories in Drosophila. Learning ＆ memory (Cold Spring Harbor, NY) 20:474-481.
Yuan Q, Lin F, Zheng X, Sehgal A (2005) Serotonin modulates circadian entrainment in Drosophila. Neuron 47:115-127.
Zuberbühler K (2001) Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli. Behavioral Ecology and Sociobiology 50:414-422.