Mapping social behavior-induced brain activation at cellular resolution in the mouse

Cell Reports

Volumn 10, Issue 2, 2015, Pages 292-305

  Kim, Yongsoo ^a   Venkataraju, Kannan Umadevi ^a   Pradhan, Kith ^a   Mende, Carolin ^a   Taranda, Julian ^a   Turaga, Srinivas C ^b   Arganda Carreras, Ignacio ^b   Ng, Lydia ^c   Hawrylycz, Michael J ^c   Rockland, Kathleen S ^a,d   Seung, H Sebastian ^b   Osten, Pavel ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; BRAIN REGION; CELL DENSITY; CONTROLLED STUDY; EVOKED RESPONSE; EXPLORATORY BEHAVIOR; FEMALE; HYPOTHALAMUS; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; ONCOGENE C FOS; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL RECOGNITION TEST; ANIMAL; ANIMAL BEHAVIOR; BRAIN; C57BL MOUSE; GENETICS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; RADIOGRAPHY; THREE DIMENSIONAL IMAGING; TOMOGRAPHY; TRANSGENIC MOUSE; VETERINARY;

GREEN FLUORESCENT PROTEIN; PROTEIN C FOS;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; BRAIN MAPPING; FEMALE; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-FOS; TOMOGRAPHY;

EID: 84920886188     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.12.014     Document Type: Article

References (58)

1. Anderson D.J. Optogenetics, sex, and violence in the brain: implications for psychiatry. Biol. Psychiatry 2012, 71:1081-1089.
2. Baum M.J., Kelliher K.R. Complementary roles of the main and accessory olfactory systems in mammalian mate recognition. Annu. Rev. Physiol. 2009, 71:141-160.
3. Bean N.J. Olfactory and vomeronasal mediation of ultrasonic vocalizations in male mice. Physiol. Behav. 1982, 28:31-37.
4. Biały M., Kaczmarek L. c-Fos expression as a tool to search for the neurobiological base of the sexual behaviour of males. Acta Neurobiol. Exp. (Warsz.) 1996, 56:567-577.
5. Brennan P.A., Zufall F. Pheromonal communication in vertebrates. Nature 2006, 444:308-315.
6. Buzsáki G. Large-scale recording of neuronal ensembles. Nat. Neurosci. 2004, 7:446-451.
7. Clayton D.F. The genomic action potential. Neurobiol. Learn. Mem. 2000, 74:185-216.
8. Coolen L.M., Peters H.J., Veening J.G. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res. 1996, 738:67-82.
9. Dölen G., Darvishzadeh A., Huang K.W., Malenka R.C. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013, 501:179-184.
10. Dong H.W., Swanson L.W. Projections from bed nuclei of thestria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J.Comp. Neurol. 2004, 471:396-433.
11. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, magnocellular nucleus: implications for cerebral hemisphere regulation of micturition, defecation, and penile erection. J.Comp. Neurol. 2006, 494:108-141.
12. Dragunow M., Robertson H.A. Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 1987, 329:441-442.
13. Fenno L., Yizhar O., Deisseroth K. The development and application of optogenetics. Annu. Rev. Neurosci. 2011, 34:389-412.
14. Ferguson J.N., Young L.J., Hearn E.F., Matzuk M.M., Insel T.R., Winslow J.T. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 2000, 25:284-288.
15. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J.Neurosci. 2001, 21:8278-8285.
16. Garner A.R., Rowland D.C., Hwang S.Y., Baumgaertel K., Roth B.L., Kentros C., Mayford M. Generation of a synthetic memory trace. Science 2012, 335:1513-1516.
17. Ghosh S., Larson S.D., Hefzi H., Marnoy Z., Cutforth T., Dokka K., Baldwin K.K. Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 2011, 472:217-220.
18. Grewe B.F., Helmchen F. Optical probing of neuronal ensemble activity. Curr. Opin. Neurobiol. 2009, 19:520-529.
19. Guzowski J.F., Timlin J.A., Roysam B., McNaughton B.L., Worley P.F., Barnes C.A. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr. Opin. Neurobiol. 2005, 15:599-606.
20. Herculano-Houzel S., Mota B., Lent R. Cellular scaling rules for rodent brains. Proc. Natl. Acad. Sci. USA 2006, 103:12138-12143.
21. Hitti F.L., Siegelbaum S.A. The hippocampal CA2 region is essential for social memory. Nature 2014, 508:88-92.
22. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Brain Res. Rev. 2007, 56:27-78.
23. Keller A., Carlson G.C. Neonatal whisker clipping alters intracortical, but not thalamocortical projections, in rat barrel cortex. J.Comp. Neurol. 1999, 412:83-94.
24. Keller M., Douhard Q., Baum M.J., Bakker J. Sexual experience does not compensate for the disruptive effects of zinc sulfate-lesioning of the main olfactory epithelium on sexual behavior in male mice. Chem. Senses 2006, 31:753-762.
25. Kelley A.E., Stinus L. The distribution of the projection from the parataenial nucleus of the thalamus to the nucleus accumbens in the rat: an autoradiographic study. Exp. Brain Res. 1984, 54:499-512.
26. Kopec C.D., Bowers A.C., Pai S., Brody C.D. Semi-automated atlas-based analysis of brain histological sections. J.Neurosci. Methods 2011, 196:12-19.
27. Lee H.M., Giguere P.M., Roth B.L. DREADDs: novel tools for drug discovery and development. Drug Discov. Today 2014, 19:469-473.
28. Lin D., Boyle M.P., Dollar P., Lee H., Lein E.S., Perona P., Anderson D.J. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011, 470:221-226.
29. Liu X., Ramirez S., Pang P.T., Puryear C.B., Govindarajan A., Deisseroth K., Tonegawa S. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484:381-385.
30. Mandiyan V.S., Coats J.K., Shah N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 2005, 8:1660-1662.
31. Matsuo N., Reijmers L., Mayford M. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 2008, 319:1104-1107.
32. Mattes D., Haynor D.R., Vesselle H., Lewellen T.K., Eubank W. PET-CT image registration in the chest using free-form deformations. IEEE Trans. Med. Imaging 2003, 22:120-128.
33. Meyer H.S., Wimmer V.C., Oberlaender M., de Kock C.P., Sakmann B., Helmstaedter M. Number and laminar distribution of neurons in a thalamocortical projection column of rat vibrissal cortex. Cereb. Cortex 2010, 20:2277-2286.
34. Morgan J.I., Cohen D.R., Hempstead J.L., Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 1987, 237:192-197.
35. Olshausen B.A., Field D.J. Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 2004, 14:481-487.
36. Pankevich D.E., Baum M.J., Cherry J.A. Olfactory sex discrimination persists, whereas the preference for urinary odorants from estrous females disappears in male mice after vomeronasal organ removal. J.Neurosci. 2004, 24:9451-9457.
37. Pfaus J.G., Heeb M.M. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res. Bull. 1997, 44:397-407.
38. Pitkänen A., Savander V., LeDoux J.E. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci. 1997, 20:517-523.
39. Ragan T., Kadiri L.R., Venkataraju K.U., Bahlmann K., Sutin J., Taranda J., Arganda-Carreras I., Kim Y., Seung H.S., Osten P. Serial two-photon tomography for automated exvivo mouse brain imaging. Nat. Methods 2012, 9:255-258.
40. Reijmers L.G., Perkins B.L., Matsuo N., Mayford M. Localization of a stable neural correlate of associative memory. Science 2007, 317:1230-1233.
41. Saper C.B., Lu J., Chou T.C., Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci. 2005, 28:152-157.
42. Sesack S.R., Grace A.A. Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 2010, 35:27-47.
43. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 2002, 25:507-536.
44. Smith P.M., Ferguson A.V. Circulating signals as critical regulators of autonomic state-central roles for the subfornical organ. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R405-R415.
45. Sokolowski K., Corbin J.G. Wired for behaviors: from development to function of innate limbic system circuitry. Front. Mol. Neurosci. 2012, 5:55.
46. Sosulski D.L., Bloom M.L., Cutforth T., Axel R., Datta S.R. Distinct representations of olfactory information in different cortical centres. Nature 2011, 472:213-216.
47. Sternson S.M. Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 2013, 77:810-824.
48. Stowers L., Holy T.E., Meister M., Dulac C., Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 2002, 295:1493-1500.
49. Sunkin S.M., Ng L., Lau C., Dolbeare T., Gilbert T.L., Thompson C.L., Hawrylycz M., Dang C. Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system. Nucleic Acids Res. 2013, 41:D996-D1008.
50. Swanson L.W. Cerebral hemisphere regulation of motivated behavior. Brain Res. 2000, 886:113-164.
51. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
52. Turaga S.C., Murray J.F., Jain V., Roth F., Helmstaedter M., Briggman K., Denk W., Seung H.S. Convolutional networks can learn to generate affinity graphs for image segmentation. Neural Comput. 2010, 22:511-538.
53. Veening J.G., Coolen L.M., de Jong T.R., Joosten H.W., de Boer S.F., Koolhaas J.M., Olivier B. Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur. J. Pharmacol. 2005, 526:226-239.
54. Vousden D.A., Epp J., Okuno H., Nieman B.J., van Eede M., Dazai J., Ragan T., Bito H., Frankland P.W., Lerch J.P., Henkelman R.M. Whole-brain mapping of behaviourally induced neural activation in mice. Brain Struct. Funct. 2014.
55. Williams R.W., Rakic P. Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J.Comp. Neurol. 1988, 278:344-352.
56. Winslow J.T. Mouse social recognition and preference. Curr. Protoc. Neurosci. 2003, Chapter 8:16.
57. Yang C.F., Chiang M.C., Gray D.C., Prabhakaran M., Alvarado M., Juntti S.A., Unger E.K., Wells J.A., Shah N.M. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 2013, 153:896-909.
58. Yang C.F., Shah N.M. Representing sex in the brain, one module at a time. Neuron 2014, 82:261-278.