c-Fos expression predicts long-term social memory retrieval in mice.

Amygdala/metabolism; Animals; Hippocampus/metabolism; Male; Memory/physiology; Memory, Long-Term/physiology; Mice; Mice, Inbred C57BL; Olfactory Bulb/physiology; Prefrontal Cortex/physiology; Proto-Oncogene Proteins c-fos/metabolism; Smell/physiology; Social Behavior; Contextual integration; Long-term social memory; Random Forest; Top-down modulation; c-Fos

Abstract :

[en] The way the rodent brain generally processes socially relevant information is rather well understood. How social information is stored into long-term social memory, however, is still under debate. Here, brain c-Fos expression was measured after adult mice were exposed to familiar or novel juveniles and expression was compared in several memory and socially relevant brain areas. Machine Learning algorithm Random Forest was then used to predict the social interaction category of adult mice based on c-Fos expression in these areas. Interaction with a familiar co-specific altered brain activation in the olfactory bulb, amygdala, hippocampus, lateral septum and medial prefrontal cortex. Remarkably, Random Forest was able to predict interaction with a familiar juvenile with 100% accuracy. Activity in the olfactory bulb, amygdala, hippocampus and the medial prefrontal cortex were crucial to this prediction. From our results, we suggest long-term social memory depends on initial social olfactory processing in the medial amygdala and its output connections synergistically with non-social contextual integration by the hippocampus and medial prefrontal cortex top-down modulation of primary olfactory structures.

Disciplines :

Life sciences: Multidisciplinary, general & others

Author, co-author :

Lüscher Dias, Thomaz

Fernandes Golino, Hudson

De Moura Oliveira, Vinicius Elias ; Université de Liège - ULiège > Neurosciences-Neuroendocrinology

Dutra Moraes, Márcio Flávio

Schenatto Pereira, Grace

Language :

English

Title :

c-Fos expression predicts long-term social memory retrieval in mice.

Publication date :

2016

Journal title :

Behavioural Brain Research

ISSN :

0166-4328

eISSN :

1872-7549

Publisher :

Elsevier, Netherlands

Volume :

313

Pages :

260-271

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 31 May 2021

Statistics

Number of views

32 (1 by ULiège)

Number of downloads

2 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

[1] Bluthé, R.M., Dantzer, R., Role of the vomeronasal system in vasopressinergic modulation of social recognition in rats. Brain Res. 604 (1993), 205–210 http://www.ncbi.nlm.nih.gov/pubmed/8457849.
[2] Brennan, P.a., Zufall, F., Pheromonal communication in vertebrates. Nature 444 (2006), 308–315, 10.1038/nature05404.
[3] Brennan, P.a., Kendrick, K.M., Mammalian social odours: attraction and individual recognition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 (2006), 2061–2078, 10.1098/rstb.2006.1931.
[4] Thor, D., Holloway, W., Social memory of the male laboratory rat. J. Comp. Physiol. 96 (1982), 1000–1006 http://psycnet.apa.org/psycinfo/1983-20411-001 (accessed 8.01.13).
[5] Hurst, J.L., Payne, C.E., Nevison, C.M., Marie, A.D., Humphries, R.E., Robertson, D.H., Cavaggioni, A., Beynon, R.J., Individual recognition in mice mediated by major urinary proteins. Nature 414 (2001), 631–634.
[6] Overath, P., Sturm, T., Rammensee, H.-G., Of volatiles and peptides: in search for MHC-dependent olfactory signals in social communication. Cell. Mol. Life Sci. 71 (2014), 2429–2442, 10.1007/s00018-014-1559-6.
[7] Ferguson, J.N., Young, L.J., Insel, T.R., The neuroendocrine basis of social recognition. Front. Neuroendocr. 23 (2002), 200–224, 10.1006/frne.2002.0229.
[8] Bielsky, I.F., Young, L.J., Oxytocin, vasopressin, and social recognition in mammals. Peptides 25 (2004), 1565–1574, 10.1016/j.peptides.2004.05.019.
[9] Scalia, F., Winans, S.S., The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161 (1975), 31–55, 10.1002/cne.901610105.
[10] Knobloch, H.S., Charlet, A., Hoffmann, L., Eliava, M., Khrulev, S., Cetin, A., Osten, P., Schwarz, M., Seeburg, P., Stoop, R., Grinevich, V., Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73 (2012), 553–566, 10.1016/j.neuron.2011.11.030.
[11] Risold, P.Y., Swanson, L.W., Connections of the rat lateral septal complex. Brain Res. Rev. 24 (1997), 115–195, 10.1016/S0165-0173(97)00009-X.
[12] Sekiguchi, R., Wolterink, G., van Ree, J.M., Analysis of the influence of vasopressin neuropeptides on social recognition of rats. Eur. Neuropsychopharmacol. 1 (1991), 123–126 http://www.ncbi.nlm.nih.gov/pubmed/1821701.
[13] Maaswinkel, H., Baars, a M., Gispen, W.H., Spruijt, B.M., Roles of the basolateral amygdala and hippocampus in social recognition in rats. Physiol. Behav. 60 (1996), 55–63 http://www.ncbi.nlm.nih.gov/pubmed/8804643.
[14] van Wimersma Greidanus, T.B., Maigret, C., The role of limbic vasopressin and oxytocin in social recognition. Brain Res. 713 (1996), 153–159 http://www.ncbi.nlm.nih.gov/pubmed/8724986.
[15] Samuelsen, C.L., Meredith, M., Oxytocin antagonist disrupts male mouse medial amygdala response to chemical-communication signals. Neuroscience 180 (2011), 96–104, 10.1016/j.neuroscience.2011.02.030.
[16] Gur, R., Tendler, A., Wagner, S., Long-term social recognition memory is mediated by oxytocin-dependent synaptic plasticity in the medial amygdala. Biol. Psychiatry. 76 (2014), 377–386, 10.1016/j.biopsych.2014.03.022.
[17] Noack, J., Murau, R., Engelmann, M., Consequences of temporary inhibition of the medial amygdala on social recognition memory performance in mice. Front. Neurosci. 9 (2015), 1–6, 10.3389/fnins.2015.00152.
[18] Maroun, M., Wagner, S., Oxytocin and memory of emotional stimuli: some dance to remember, some dance to forget. Biol. Psychiatry. 79 (2015), 203–212, 10.1016/j.biopsych.2015.07.016.
[19] Pena, R.R., Pereira-Caixeta, R.a., Moraes, M.F.D., Pereira, G.S., Anisomycin administered in the olfactory bulb and dorsal hippocampus impaired social recognition memory consolidation in different time-points. Brain Res. Bull. 109C (2014), 151–157, 10.1016/j.brainresbull.2014.10.009.
[20] Hitti, F.L., Siegelbaum, S.a., The hippocampal CA2 region is essential for social memory. Nature 508 (2014), 88–92, 10.1038/nature13028.
[21] Stevenson, E.L., Caldwell, H.K., Lesions to the CA2 region of the hippocampus impair social memory in mice. Eur. J. Neurosci. 40 (2014), 3294–3301, 10.1111/ejn.12689.
[22] Kogan, J.H., Frankland, P.W., Silva, a.J., Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10 (2000), 47–56, 10.1002/(SICI)1098-1063(2000)10:1<47:AID-HIPO5>3.0.CO;2-6.
[23] Belluscio, L., Koentges, G., Axel, R., Dulac, C., A map of pheromone receptor activation in the mammalian brain. Cell 97 (1999), 209–220.
[24] Lin, S.D.Y., Block, E., Katz, L., Encoding social signals in the mouse main olfactory bulb. Nature, 434, 2005 htt://www.nature.com/nature/journal/v434/n7032/abs/nature03414.html (accessed 17.11.14).
[25] Kim, Y., Venkataraju, K.U., Pradhan, K., Mende, C., Taranda, J., Turaga, S.C., Arganda-Carreras, I., Ng, L., Hawrylycz, M.J., Rockland, K.S., Seung, H.S., Osten, P., Mapping social behavior-induced brain activation at cellular resolution in the mouse. Cell Rep. 10 (2015), 292–305, 10.1016/j.celrep.2014.12.014.
[26] Mourao, F.A.G., Lockmann, A.L.V., Castro, G.P., de Castro Medeiros, D., Reis, M.P., Pereira, G.S., Massensini, A.R., Moraes, M.F.D., Triggering different brain states using asynchronous serial communication to the rat amygdala. Cereb. Cortex, 2015, 10.1093/cercor/bhu313.
[27] Molapour, T., Golkar, A., Navarrete, C.D., Haaker, J., Olsson, A., Neural correlates of biased social fear learning and interaction in an intergroup context. Neuroimage 121 (2015), 171–183, 10.1016/j.neuroimage.2015.07.015.
[28] Laubach, M., Wessberg, J., Nicolelis, M.a., Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405 (2000), 567–571, 10.1038/35014604.
[29] Saleh, M., Reimer, J., Penn, R., Ojakangas, C.L., Hatsopoulos, N.G., Fast and slow oscillations in human primary motor cortex predict oncoming behaviorally relevant cues. Neuron 65 (2010), 461–471, 10.1016/j.neuron.2010.02.001.
[30] Borelli, K.G., Blanchard, D.C., Javier, L.K., Defensor, E.B., Brandão, M.L., Blanchard, R.J., Neural correlates of scent marking behavior in C57BL/6 J mice: detection and recognition of a social stimulus. Neuroscience 162 (2009), 914–923, 10.1016/j.neuroscience.2009.05.047.
[31] Dudai, Y., The neurobiology of consolidations, or, how stable is the Engram?. Annu. Rev. Psychol. 55 (2004), 51–86, 10.1146/annurev.psych.55.090902.142050.
[32] Gusmão, I.D., Monteiro, B.M.M., Cornélio, G.O.S., Fonseca, C.S., Moraes, M.F.D., Pereira, G.S., Odor-enriched environment rescues long-term social memory, but does not improve olfaction in social isolated adult mice. Behav. Brain Res. 228 (2012), 440–446, 10.1016/j.bbr.2011.12.040.
[33] Monteiro, B.M.M., Moreira, F.a., Massensini, A.R., Moraes, M.F.D., Pereira, G.S., Enriched environment increases neurogenesis and improves social memory persistence in socially isolated adult mice. Hippocampus 24 (2014), 239–248, 10.1002/hipo.22218.
[34] Rice, M.C., O'Brien, S.J., Genetic variance of laboratory outbred Swiss mice. Nature 283 (1980), 157–161.
[35] Cui, S., Chesson, C., Hope, R., Genetic variation within and between strains of outbred Swiss mice. Lab. Anim. 27 (1993), 116–123, 10.1258/002367793780810397.
[36] M. Dragunow, P. Bag, The use of c-fos as a metabolic marker in neuronal pathway tracing, 29 (1989) 261–265.
[37] Kee, N., Teixeira, C.M., Wang, A.H., Frankland, P.W., Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10 (2007), 355–362, 10.1038/nn1847.
[38] Paxinos, G., Franklin, K., The Mouse Brain in Stereotaxic Coordinates. 4th ed., 2011, Academic Press, San Diego.
[39] Lein, E.S., Hawrylycz, M.J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A.F., Boguski, M.S., Brockway, K.S., Byrnes, E.J., Chen, L., Chen, L., Chen, T.-M., Chin, M.C., Chong, J., Crook, B.E., Czaplinska, A., Dang, C.N., Datta, S., Dee, N.R., Desaki, A.L., Desta, T., Diep, E., Dolbeare, T.a., Donelan, M.J., Dong, H.-W., Dougherty, J.G., Duncan, B.J., Ebbert, A.J., Eichele, G., Estin, L.K., Faber, C., Facer, B.a., Fields, R., Fischer, S.R., Fliss, T.P., Frensley, C., Gates, S.N., Glattfelder, K.J., Halverson, K.R., Hart, M.R., Hohmann, J.G., Howell, M.P., Jeung, D.P., Johnson, R.a., Karr, P.T., Kawal, R., Kidney, J.M., Knapik, R.H., Kuan, C.L., Lake, J.H., Laramee, A.R., Larsen, K.D., Lau, C., Lemon, T.a., Liang, A.J., Liu, Y., Luong, L.T., Michaels, J., Morgan, J.J., Morgan, R.J., Mortrud, M.T., Mosqueda, N.F., Ng, L.L., Ng, R., Orta, G.J., Overly, C.C., Pak, T.H., Parry, S.E., Pathak, S.D., Pearson, O.C., Puchalski, R.B., Riley, Z.L., Rockett, H.R., Rowland, S.a., Royall, J.J., Ruiz, M.J., Sarno, N.R., Schaffnit, K., Shapovalova, N.V., Sivisay, T., Slaughterbeck, C.R., Smith, S.C., Smith, K.a., Smith, B.I., Sodt, A.J., Stewart, N.N., Stumpf, K.-R., Sunkin, S.M., Sutram, M., Tam, A., Teemer, C.D., Thaller, C., Thompson, C.L., Varnam, L.R., Visel, A., Whitlock, R.M., Wohnoutka, P.E., Wolkey, C.K., Wong, V.Y., Wood, M., Yaylaoglu, M.B., Young, R.C., Youngstrom, B.L., Yuan, X.F., Zhang, B., Zwingman, T.a., Jones, A.R., Genome-wide atlas of gene expression in the adult mouse brain. Nature 445 (2007), 168–176, 10.1038/nature05453.
[40] Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682, 10.1038/nmeth.2019.
[41] Golino, H.F., Gomes, C.M.A., Four machine learning methods to predict academic achievement of college students: a comparison study. Rev. E-Psi 4 (2014), 68–101.
[42] Golino, H.F., Gomes, C.M.A., Visualizing Random Forest's prediction results. Psychology 05 (2014), 2084–2098, 10.4236/psych.2014.519211.
[43] Geurts, P., Irrthum, A., Wehenkel, L., Supervised learning with decision tree-based methods in computational and systems biology. Mol. Biosyst. 5 (2009), 1593–1605, 10.1039/b907946g.
[44] Breiman, L., Random Forests. Mach. Learn. 45 (2001), 5–32, 10.1023/A:1010933404324.
[45] James, G., Witten, D., Hastie, T., Tibshirani, R., An Introduction to Statistical Learning with Applications in R. 2013, Springer-Verlag, New York, 10.1007/978-1-4614-7138-7.
[46] Liaw, A., Wiener, M., Classification and regression by randomForest. R News 2 (2002), 18–22.
[47] Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J.-C., Müller, M., pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinf., 12, 2011, 77, 10.1186/1471-2105-12-77.
[48] DeLong, E.R., DeLong, D.M., Clarke-Pearson, D.L., Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics, 44, 1988, 837, 10.2307/2531595.
[49] Archer, K.J., Kimes, R.V., Empirical characterization of random forest variable importance measures. Comput. Stat. Data Anal. 52 (2008), 2249–2260, 10.1016/j.csda.2007.08.015.
[50] Richter, K., Wolf, G., Engelmann, M., Social recognition memory requires two stages of protein synthesis in mice. Learn. Mem. 12 (2005), 407–413, 10.1101/lm.97505.
[51] Gowin, J.L., Ball, T.M., Wittmann, M., Tapert, S.F., Paulus, M.P., Individualized relapse prediction: personality measures and striatal and insular activity during reward-processing robustly predict relapse. Drug Alcohol Depend. 152 (2015), 93–101, 10.1016/j.drugalcdep.2015.04.018.
[52] Ferris, C.F., Delville, Y., Vasopressin and serotonin interactions in the control of agonistic behavior. Psychoneuroendocrinology 19 (1994), 593–601.
[53] Kang, N., Baum, M.J., Cherry, J.A., Different profiles of main and accessory olfactory bulb mitral/tufted cell projections revealed in mice using an anterograde tracer and a whole-mount, flattened cortex preparation. Chem. Senses 36 (2011), 251–260, 10.1093/chemse/bjq120.
[54] Root, C.M., Denny, C.A., Hen, R., Axel, R., The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515 (2014), 269–273, 10.1038/nature13897.
[55] J.N. Ferguson, J.M. Aldag, T.R. Insel, L.J. Young, Oxytocin in the medial amygdala is essential for social recognition in the mouse, 21 (2001) 8278–8285.
[56] Kim, Y., Venkataraju, K.U., Pradhan, K., Mende, C., Taranda, J., Turaga, S.C., Arganda-Carreras, I., Ng, L., Hawrylycz, M.J., Rockland, K.S., Seung, H.S., Osten, P., Mapping social behavior-induced brain activation at cellular resolution in the mouse. Cell Rep. 10 (2015), 292–305, 10.1016/j.celrep.2014.12.014.
[57] von Heimendahl, M., Rao, R.P., Brecht, M., Weak and nondiscriminative responses to conspecifics in the rat hippocampus. J. Neurosci. 32 (2012), 2129–2141, 10.1523/JNEUROSCI.3812-11.2012.
[58] Guzmán, Y.F., Tronson, N.C., Sato, K., Mesic, I., Guedea, A.L., Nishimori, K., Radulovic, J., Role of oxytocin receptors in modulation of fear by social memory. Psychopharmacology (Berl.) 231 (2014), 2097–2105, 10.1007/s00213-013-3356-6.
[59] Wong, L.C., Wang, L., D'Amour, J.A., Yumita, T., Chen, G., Yamaguchi, T., Chang, B.C., Bernstein, H., You, X., Feng, J.E., Froemke, R.C., Lin, D., Effective modulation of male aggression through lateral septum to medial hypothalamus projection. Curr. Biol. 26 (2016), 593–604, 10.1016/j.cub.2015.12.065.
[60] Procaccini, C., Aitta-aho, T., Jaako-Movits, K., Zharkovsky, A., Panhelainen, A., Sprengel, R., Linden, A.-M., Korpi, E.R., Excessive novelty-induced c-Fos expression and altered neurogenesis in the hippocampus of GluA1 knockout mice. Eur. J. Neurosci. 33 (2011), 161–174, 10.1111/j.1460-9568.2010.07485.x.
[61] Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149 (2012), 188–201.
[62] Zheng, D.-J., Foley, L., Rehman, A., Ophir, A.G., Social recognition is context dependent in single male prairie voles. Anim. Behav. 86 (2013), 1085–1095, 10.1016/j.anbehav.2013.09.015.
[63] Burman, O.H.P., Mendl, M., The effects of environmental context on laboratory rat social recognition. Anim. Behav. 58 (1999), 629–634 (10.1006/anbe.1999.1170\n http://libproxy.lib.csusb.edu/login?url=http://search.ebscohost.com/login.aspx?direct=true&db=psyh&AN=1999-01745-017&site=ehost-live).
[64] Burman, O.H., Mendl, M., Recognition of conspecific odors by laboratory rats (Rattus norvegicus) does not show context specificity. J. Comp. Psychol. 116 (2002), 247–252, 10.1037/0735-7036.116.3.247.
[65] Alvarez, P., Wendelken, L., Eichenbaum, H., Hippocampal formation lesions impair performance in an odor–odor association task independently of spatial context. Neurobiol. Learn. Mem. 78 (2002), 470–476, 10.1006/nlme.2002.4068.
[66] Bunsey, M., Eichenbaum, H., Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulus–stimulus association. Hippocampus 5 (1995), 546–556, 10.1002/hipo.450050606.
[67] Burton, S., Murphy, D., Qureshi, U., Sutton, P., O'Keefe, J., Combined lesions of hippocampus and subiculum Do not produce deficits in a nonspatial social olfactory memory task. J. Neurosci. 20 (2000), 5468–5475 http://www.ncbi.nlm.nih.gov/pubmed/10884330.
[68] Petrulis, A., Eichenbaum, H., The perirhinal-entorhinal cortex, but not the hippocampus, is critical for expression of individual recognition in the context of the Coolidge effect. Neuroscience 122 (2003), 599–607, 10.1016/j.neuroscience.2003.08.009.
[69] Squires, A.S., Peddle, R., Milway, S.J., Harley, C.W., Cytotoxic lesions of the hippocampus do not impair social recognition memory in socially housed rats. Neurobiol. Learn. Mem. 85 (2006), 95–101, 10.1016/j.nlm.2005.08.012.
[70] Leser, N., Wagner, S., The effects of acute social isolation on long-term social recognition memory. Neurobiol. Learn. Mem. 124 (2015), 97–103, 10.1016/j.nlm.2015.07.002.
[71] Lieberwirth, C., Liu, Y., Jia, X., Wang, Z., Social isolation impairs adult neurogenesis in the limbic system and alters behaviors in female prairie voles. Hormones Behav. 62 (2012), 357–366, 10.1016/j.yhbeh.2012.03.005.
[72] Westenbroek, C., Den Boer, J.a, Veenhuis, M., Ter Horst, G.J., Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res. Bull. 64 (2004), 303–308, 10.1016/j.brainresbull.2004.08.006.
[73] Lu, L., Modification of hippocampal neurogenesis and neuroplasticity by social environments. Exp. Neurol. 183 (2003), 600–609, 10.1016/S0014-4886(03)00248-6.
[74] Kamal, A., Ramakers, G.M.J., Altinbilek, B., Kas, M.J.H., Social isolation stress reduces hippocampal long-term potentiation: effect of animal strain and involvement of glucocorticoid receptors. Neuroscience 256 (2014), 262–270, 10.1016/j.neuroscience.2013.10.016.
[75] Pereira-Caixeta, A.R., Guarnieri, L.O., Pena, R.R., Dias, T.L., Pereira, G.S., Neurogenesis inhibition prevents enriched environment to prolong and strengthen social recognition memory, but not to increase BDNF expression. Mol. Neurobiol., 2016, 10.1007/s12035-016-9922-2.
[76] Marín-Burgin, A., Schinder, A.F., Requirement of adult-born neurons for hippocampus-dependent learning. Behav. Brain Res. 227 (2012), 391–399, 10.1016/j.bbr.2011.07.001.
[77] Kropff, E., Yang, S.M., Schinder, A.F., Dynamic role of adult-born dentate granule cells in memory processing. Curr. Opin. Neurobiol. 35 (2015), 21–26, 10.1016/j.conb.2015.06.002.
[78] Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat. Neurosci. 15 (2012), 1700–1706.
[79] Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70 (2011), 582–588.
[80] O'Keefe, J., Nadel, L., The Hippocampus as a Cognitive Map. 1978, Oxford.
[81] Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I., Microstructure of a spatial map in the entorhinal cortex. Nature 436 (2005), 801–806, 10.1038/nature03721.
[82] Larkin, M.C., Lykken, C., Tye, L.D., Wickelgren, J.G., Frank, L.M., Hippocampal output area CA1 broadcasts a generalized novelty signal during an object-place recognition task. Hippocampus 24 (2014), 773–783, 10.1002/hipo.22268.
[83] Young, W.S., Li, J., Wersinger, S.R., Palkovits, M., The vasopressin 1b receptor is prominent in the hippocampal area CA2 where it is unaffected by restraint stress or adrenalectomy. Neuroscience 143 (2006), 1031–1039, 10.1016/j.neuroscience.2006.08.040.
[84] Cui, Z., Gerfen, C.R., Young, W.S. 3rd., Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus. J. Comp. Neurol. 521 (2013), 1844–1866, 10.1002/cne.23263.
[85] Rowland, D.C., Weible, A.P., Wickersham, I.R., Wu, H., Mayford, M., Witter, M.P., Kentros, C.G., Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 33 (2013), 14889–14898, 10.1523/JNEUROSCI.1046-13.2013.
[86] Gnatkovsky, V., Uva, L., de Curtis, M., Topographic distribution of direct and hippocampus- mediated entorhinal cortex activity evoked by olfactory tract stimulation. Eur. J. Neurosci. 20 (2004), 1897–1905, 10.1111/j.1460-9568.2004.03627.x.
[87] Boisselier, L., Ferry, B., Gervais, R., Involvement of the lateral entorhinal cortex for the formation of cross-modal olfactory-tactile associations in the rat. Hippocampus 24 (2014), 877–891, 10.1002/hipo.22277.
[88] Rajasethupathy, P., Sankaran, S., Marshel, J.H., Kim, C.K., Ferenczi, E., Lee, S.Y., Berndt, A., Ramakrishnan, C., Jaffe, A., Lo, M., Liston, C., Deisseroth, K., Projections from neocortex mediate top-down control of memory retrieval. Nature 526 (2015), 653–659, 10.1038/nature15389.
[89] Bonnavion, P., Mickelsen, L., Fujita, A., de Lecea, L., Jackson, A.C., Hubs and spokes of the lateral hypothalamus: cell types, circuits and behaviour. J. Physiol. 1 (2016), 1–34, 10.1113/JP271946.
[90] Yang, L., Zou, B., Xiong, X., Pascual, C., Xie, J., Malik, A., Xie, J., Sakurai, T., Xie, X., Hypocretin/orexin neurons contribute to hippocampus-dependent social memory and synaptic plasticity in mice. J. Neurosci. 33 (2013), 5275–5284, 10.1523/JNEUROSCI.3200-12.2013.
[91] Nieh, E.H., Vander Weele, C.M., Matthews, G.A., Presbrey, K.N., Wichmann, R., Leppla, C.A., Izadmehr, E.M., Tye, K.M., Inhibitory input from the lateral hypothalamus to the ventral tegmental area disinhibits dopamine neurons and promotes behavioral activation. Neuron 90 (2016), 1286–1298, 10.1016/j.neuron.2016.04.035.
[92] Kádár, E., Vico-Varela, E., Aldavert-Vera, L., Huguet, G., Morgado-Bernal, I., Segura-Torres, P., Increase in c-Fos and Arc protein in retrosplenial cortex after memory-improving lateral hypothalamic electrical stimulation treatment. Neurobiol. Learn. Mem. 128 (2016), 117–124, 10.1016/j.nlm.2015.12.012.
[93] Altman, J., Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137 (1969), 433–457, 10.1002/cne.901370404.
[94] Song, H., Kempermann, G., Overstreet Wadiche, L., Zhao, C., Schinder, A.F., Bischofberger, J., New neurons in the adult mammalian brain: synaptogenesis and functional integration. J. Neurosci. 25 (2005), 10366–10368, 10.1523/JNEUROSCI.3452-05.2005.
[95] Feierstein, C.E., Linking adult olfactory neurogenesis to social behavior. Front. Neurosci., 6, 2012, 173, 10.3389/fnins.2012.00173.
[96] Kageyama, R., Imayoshi, I., Sakamoto, M., The role of neurogenesis in olfaction-dependent behaviors. Behav. Brain Res. 227 (2012), 459–463, 10.1016/j.bbr.2011.04.038.
[97] Carey, R.M., Wachowiak, M., Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J. Neurosci. 31 (2011), 10615–10626, 10.1523/JNEUROSCI.1805-11.2011.
[98] Oettl, L.-L., Ravi, N., Schneider, M., Scheller, M.F., Schneider, P., Mitre, M., da Silva Gouveia, M., Froemke, R.C., Chao, M.V., Young, W.S., Meyer-Lindenberg, A., Grinevich, V., Shusterman, R., Kelsch, W., Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron 90 (2016), 609–621, 10.1016/j.neuron.2016.03.033.
[99] Nagayama, S., Homma, R., Imamura, F., Neuronal organization of olfactory bulb circuits. Front. Neural Circuits. 8 (2014), 1–19, 10.3389/fncir.2014.00098.
[100] Takagishi, M., Chiba, T., Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res. 566 (1991), 26–39, 10.1016/0006-8993(91)91677-S.
[101] Sesack, S.R., Deutch, A.Y., Roth, R.H., Bunney, B.S., Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290 (1989), 213–242, 10.1002/cne.902900205.
[102] Bicks, L.K., Koike, H., Akbarian, S., Morishita, H., Prefrontal cortex and social cognition in mouse and man. Front. Psychol. 6 (2015), 1–15, 10.3389/fpsyg.2015.01805.
[103] El Rawas, R., Klement, S., Kummer, K.K., Fritz, M., Dechant, G., Saria, A., Zernig, G., Brain regions associated with the acquisition of conditioned place preference for cocaine vs. social interaction. Front. Behav. Neurosci. 6 (2012), 1–14, 10.3389/fnbeh.2012.00063.
[104] van Kerkhof, L.W., Damsteegt, R., Trezza, V., Voorn, P., Vanderschuren, L.J., Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum. Neuropsychopharmacology 38 (2013), 1899–1909, 10.1038/npp.2013.83.
[105] Cooper, M.A., Clinard, C.T., Morrison, K.E., Neurobiological mechanisms supporting experience-dependent resistance to social stress. Neuroscience 291 (2015), 1–14, 10.1016/j.neuroscience.2015.01.072.
[106] Sharpe, M.J., Killcross, S., The prelimbic cortex uses higher-order cues to modulate both the acquisition and expression of conditioned fear. Front. Syst. Neurosci., 8, 2014, 235, 10.3389/fnsys.2014.00235.
[107] Harvey, P.-O., Fossati, P., Lepage, M., Modulation of memory formation by stimulus content: specific role of the medial prefrontal cortex in the successful encoding of social pictures. J. Cogn. Neurosci. 19 (2007), 351–362, 10.1162/jocn.2007.19.2.351.