Afferent projections to the different medial amygdala subdivisions: a retrograde tracing study in the mouse

Brain Structure and Function

Volumn 221, Issue 2, 2016, Pages 1033-1065

  Cádiz Moretti, Bernardita ^a   Otero García, Marcos ^a   Martínez García, Fernando ^a,b   Lanuza, Enrique ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITAT JAUME I   (Spain)

Author keywords

Fluorogold; Olfactory system; Retrograde tracing; Socio sexual behaviour; Vomeronasal

Indexed keywords

FLUOROGOLD;

ADULT; ALLOCORTEX; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CLAUSTRUM; CONTROLLED STUDY; DENSITY; FEMALE; FRONTAL CORTEX; INFRALIMBIC CORTEX; MEDIAL AMYGDALA; MEDIAL AMYGDALOID NUCLEUS ANTERIOR; MEDIAL AMYGDALOID NUCLEUS POSTERODORSAL; MEDIAL AMYGDALOID NUCLEUS POSTEROVENTRAL; MEDIAL ORBITOFRONTAL CORTEX; MOUSE; NONHUMAN; OLFACTORY BULB; PRELIMBIC CORTEX; PRIORITY JOURNAL; PYRIFORM CORTEX; SEPTUM PELLUCIDUM; STRIA TERMINALIS; THALAMUS; VENTRAL HIPPOCAMPUS; VENTRAL STRIATUM; AMYGDALA; ANIMAL; BRAIN CORTEX; BRAIN MAPPING; FRONTAL LOBE; HIPPOCAMPUS; HYPOTHALAMUS; NERVE TRACT; OLFACTORY SYSTEM; PATHOLOGY; PHYSIOLOGY; SEXUAL BEHAVIOR; VOMERONASAL ORGAN;

AMYGDALA; ANIMALS; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; HYPOTHALAMUS; MICE; NEURAL PATHWAYS; OLFACTORY BULB; OLFACTORY PATHWAYS; SEXUAL BEHAVIOR, ANIMAL; THALAMUS; VOMERONASAL ORGAN;

EID: 84959319934     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0954-y     Document Type: Article

References (139)

1. Arakawa H, Arakawa K, Deak T (2010) Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor. Neuroscience 171:1141–1151
2. Bader A, Breer H, Strotmann J (2012) Untypical connectivity from olfactory sensory neurons expressing OR37 into higher brain centers visualized by genetic tracing. Histochem Cell Biol 137:615–628
3. Bautze V, Bar R, Fissler B, Trapp M, Schmidt D, Beifuss U, Bufe B, Zufall F, Breer H, Strotmann J (2012) Mammalian-specific OR37 receptors are differentially activated by distinct odorous fatty aldehydes. Chem Senses 37:479–493
4. Bautze V, Schwack W, Breer H, Strotmann J (2014) Identification of a natural source for the OR37B ligand. Chem Senses 39:27–38
5. Bergan JF, Ben-Shaul Y, Dulac C (2014) Sex-specific processing of social cues in the medial amygdala. Elife 3:e02743. doi:10.7554/eLife02743
6. Bordi F, LeDoux JE (1994) Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdala stimulation. Exp Brain Res 98:275–286
7. Bourgeais L, Gauriau C, Bernard JF (2001) Projections from the nociceptive area of the central nucleus of the amygdala to the forebrain: a PHA-L study in the rat. Eur J Neurosci 14:229–255
8. Bupesh M, Legaz I, Abellan A, Medina L (2011) Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol 519:1505–1525
9. Cadiz-Moretti B, Martinez-Garcia F, Lanuza E (2013) Neural substrate to associate odorants and pheromones: convergence of projections from the main and accessory olfactory bulbs in mice. In: East ML, Dehnhard M (eds) Chemical signals in vertebrates 12. Springer Science, New York, pp 3–16
10. Cahill L, McGaugh JL (1990) Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav Neurosci 104:532–543
11. Calu DJ, Roesch MR, Stalnaker TA, Schoenbaum G (2007) Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb Cortex 17:1342–1349
12. Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324:180–194
13. Canteras NS, Simerly RB, Swanson LW (1992a) Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143–179
14. Canteras NS, Simerly RB, Swanson LW (1992b) Projections of the ventral premammillary nucleus. J Comp Neurol 324:195–212
15. Canteras NS, Simerly RB, Swanson LW (1994) Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348:41–79
16. Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213–245
17. Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56:1–26
18. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450:899–902
19. Choi GB, Dong HW, Murphy AJ, Valenzuela DM, Yancopoulos GD, Swanson LW, Anderson DJ (2005) Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46:647–660
20. Christensen MK, Frederickson CJ (1998) Zinc-containing afferent projections to the rat corticomedial amygdaloid complex: a retrograde tracing study. J Comp Neurol 400:375–390
21. Coolen LM, Wood RI (1998) Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: simultaneous anterograde and retrograde tract tracing. J Comp Neurol 399:189–209
22. Cousens G, Otto T (1998) Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning. Behav Neurosci 112:1092–1103
23. Cousens GA, Kearns A, Laterza F, Tundidor J (2012) Excitotoxic lesions of the medial amygdala attenuate olfactory fear-potentiated startle and conditioned freezing behavior. Behav Brain Res 229:427–432
24. de la Rosa-Prieto C, Ubeda-Banon I, Mohedano-Moriano A, Pro-Sistiaga P, Saiz-Sanchez D, Insausti R, Martinez-Marcos A (2009) Subicular and CA1 hippocampal projections to the accessory olfactory bulb. Hippocampus 19:124–129
25. de Olmos JS, Beltramino CA, Alheid GF (2004) Amygdala and extended Amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In: Paxinos G (ed) The rat nervous system. Elsevier Academic Press, San Diego, pp 509–603
26. Dielenberg RA, Hunt GE, McGregor IS (2001) ”When a rat smells a cat”: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104:1085–1097
27. Dong HW, Swanson LW (2004) Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J Comp Neurol 471:396–433
28. Dong HW, Petrovich GD, Swanson LW (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Rev 38:192–246
29. Doron NN, LeDoux JE (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J Comp Neurol 412:383–409
30. Erskine MS (1993) Mating-induced increases in FOS protein in preoptic area and medial amygdala of cycling female rats. Brain Res Bull 32:447–451
31. Falkner AL, Dollar P, Perona P, Anderson DJ, Lin D (2014) Decoding ventromedial hypothalamic neural activity during male mouse aggression. J Neurosci 34:5971–5984
32. Fortes-Marco L, Lanuza E, Martinez-Garcia F (2013) Of pheromones and kairomones: what receptors mediate innate emotional responses? Anat Rec (Hoboken) 296:1346–1363
33. Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319:229–259
34. Gomez DM, Newman SW (1992) Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster. J Comp Neurol 317:195–218
35. Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48:11–22
36. Gu G, Cornea A, Simerly RB (2003) Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J Comp Neurol 460:542–562
37. Guillamon A, Segovia S (1997) Sex differences in the vomeronasal system. Brain Res Bull 44:377–382
38. Gulia KK, Jodo E, Kawauchi A, Miki T, Kayama Y, Mallick HN, Koyama Y (2008) The septal area, site for the central regulation of penile erection during waking and rapid eye movement sleep in rats: a stimulation study. Neuroscience 156:1064–1073
39. Gutiérrez-Castellanos N, Martínez-Marcos A, Martínez-García F, Lanuza E (2010) Chemosensory function of the amygdala. Vitam Horm 83:165–196
40. Gutiérrez-Castellanos N, Pardo-Bellver C, Martínez-García F, Lanuza E (2014) The vomeronasal cortex—afferent and efferent projections of the posteromedial cortical nucleus of the amygdala in mice. Eur J Neurosci 39:141–158
41. Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551–576
42. Halem HA, Cherry JA, Baum MJ (1999) Vomeronasal neuroepithelium and forebrain Fos responses to male pheromones in male and female mice. J Neurobiol 39:249–263
43. Halpern M, Martinez-Marcos A (2003) Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245–318
44. Hari Dass SA, Vyas A (2014) Copulation or sensory cues from the female augment fos expression in arginine vasopressin neurons of the posterodorsal medial amygdala of male rats. Front Zool 11:42
45. Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249–276
46. Isogai Y, Si S, Pont-Lezica L, Tan T, Kapoor V, Murthy VN, Dulac C (2011) Molecular organization of vomeronasal chemoreception. Nature 478:241–245
47. Kang N, Baum MJ, Cherry JA (2009) A direct main olfactory bulb projection to the ‘vomeronasal’ amygdala in female mice selectively responds to volatile pheromones from males. Eur J Neurosci 29:624–634
48. Kang N, Baum MJ, Cherry JA (2011) 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 36:251–260
49. Kishi T, Tsumori T, Yokota S, Yasui Y (2006) Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J Comp Neurol 496:349–368
50. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99:10825–10830
51. Kollack-Walker S, Newman SW (1995) Mating and agonistic behavior produce different patterns of fos immunolabeling in the male Syrian hamster brain. Neurosci 66:721–736
52. Koolhaas JM, van den Brink THC, Roozendaal B, Boorsma F (1990) Medial amygdala and aggressive behavior: interaction between testosterone and vasopressin. Aggr Behav 16:223–229
53. Krieger MS, Conrad LC, Pfaff DW (1979) An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. J Comp Neurol 183:785–815
54. Krieger J, Schmitt A, Lobel D, Gudermann T, Schultz G, Breer H, Boekhoff I (1999) Selective activation of G protein subtypes in the vomeronasal organ upon stimulation with urine-derived compounds. J Biol Chem 274:4655–4662
55. Lanuza E, Nader K, LeDoux JE (2004) Unconditioned stimulus pathways to the amygdala: effects of posterior thalamic and cortical lesions on fear conditioning. Neuroscience 125:305–315
56. Lanuza E, Moncho-Bogani J, LeDoux JE (2008) Unconditioned stimulus pathways to the amygdala: effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala. Neuroscience 155:959–968
57. LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ (1987) Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123–146
58. LeDoux JE, Farb C, Ruggiero DA (1990a) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10:1043–1054
59. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990b) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069
60. Lehman MN, Winans SS, Powers JB (1980) Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science 210:557–560
61. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796
62. Li S, Kirouac GJ (2008) Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 506:263–287
63. Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221–226
64. Linke R, De Lima AD, Schwegler H, Pape HC (1999) Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J Comp Neurol 403:158–170
65. Majak K, Pitkanen A (2003) Projections from the periamygdaloid cortex to the amygdaloid complex, the hippocampal formation, and the parahippocampal region: a PHA-L study in the rat. Hippocampus 13:922–942
66. Maras PM, Petrulis A (2010a) Anatomical connections between the anterior and posterodorsal sub-regions of the medial amygdala: integration of odor and hormone signals. Neuroscience 170:610–622
67. Maras PM, Petrulis A (2010b) The anterior medial amygdala transmits sexual odor information to the posterior medial amygdala and related forebrain nuclei. Eur J Neurosci 32:469–482
68. Maras PM, Petrulis A (2010c) Lesions that functionally disconnect the anterior and posterodorsal sub-regions of the medial amygdala eliminate opposite-sex odor preference in male Syrian hamsters (Mesocricetus auratus). Neuroscience 165:1052–1062
69. Maren S, Fanselow MS (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 15:7548–7564
70. Martínez-García F, Novejarque A, Gutiérrez-Castellanos N, Lanuza E (2012) Piriform cortex and amygdala. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic Press, San Diego, pp 140–172
71. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332
72. McDonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71:55–75
73. Meredith M (1986) Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol Behav 36:737–743
74. Meredith M, Westberry JM (2004) Distinctive responses in the medial amygdala to same-species and different-species pheromones. J Neurosci 24:5719–5725
75. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055–2067
76. Mohedano-Moriano A, Pro-Sistiaga P, Ubeda-Banon I, Crespo C, Insausti R, Martinez-Marcos A (2007) Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur J Neurosci 25:2065–2080
77. Moncho-Bogani J, Martinez-Garcia F, Novejarque A, Lanuza E (2005) Attraction to sexual pheromones and associated odorants in female mice involves activation of the reward system and basolateral amygdala. Eur J Neurosci 21:2186–2198
78. Morgan HD, Watchus JA, Milgram NW, Fleming AS (1999) The long lasting effects of electrical simulation of the medial preoptic area and medial amygdala on maternal behavior in female rats. Behav Brain Res 99:61–73
79. Morris JA, Jordan CL, King ZA, Northcutt KV, Breedlove SM (2008) Sexual dimorphism and steroid responsiveness of the posterodorsal medial amygdala in adult mice. Brain Res 1190:115–121
80. Motta SC, Guimaraes CC, Furigo IC, Sukikara MH, Baldo MV, Lonstein JS, Canteras NS (2013) Ventral premammillary nucleus as a critical sensory relay to the maternal aggression network. Proc Natl Acad Sci USA 110:14438–14443
81. Newman SW (1999) The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 877:242–257
82. Nitecka L (1981) Connections of the hypothalamus and preoptic area with nuclei of the amygdaloid body in the rat; HRP retrograde transport study. Acta Neurobiol Exp 41:53–67
83. Nodari F, Hsu FF, Fu X, Holekamp TF, Kao LF, Turk J, Holy TE (2008) Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J Neurosci 28:6407–6418
84. Olucha-Bordonau FE, Fortes-Marco L, Otero-García M, Lanuza E, Martínez-García F (2015) Amygdala, structure and function. In: Paxinos G (ed) The rat nervous system. Academic Press, New York, pp 441–490
85. Otero-Garcia M, Martin-Sanchez A, Fortes-Marco L, Martínez-Ricós J, Agustin-Pavón C, Lanuza E, Martínez-García F (2014) Extending the socio-sexual brain: arginine-vasopressin immunoreactive circuits in the telencephalon of mice. Brain Struct Funct 219:1055–1081
86. Ottersen OP (1980) Afferent connections of the amygdaloid complex of the rat and cat. II. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol 194:267–289
87. Ottersen OP, Ben-Ari Y (1979) Afferent connections of the amygdaloid complex of the rat and cat. I. Projections from the thalamus. J Comp Neurol 187:401–424
88. Oxley G, Fleming AS (2000) The effects of medial preoptic area and amygdala lesions on maternal behavior in the juvenile rat. Dev Psychobiol 37:253–265
89. Palomero-Gallagher N, Zilles K (2015) Isocortex. In: Paxinos G (ed) The rat nervous system, 4th edn. Academic Press, London, pp 601–625
90. Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692–703
91. Pardo-Bellver C, Cadiz-Moretti B, Novejarque A, Martinez-Garcia F, Lanuza E (2012) Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice. Front Neuroanat 6:33
92. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego
93. Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374:387–420
94. Petrulis A (2013) Chemosignals, hormones and mammalian reproduction. Horm Behav 63:723–741
95. Pezzone MA, Lee W-, Hoffman GE, Rabin BS (1992) Induction of c-Fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res 597:41–50
96. Pfaus JG, Kleopoulos SP, Mobbs CV, Gibbs RB, Pfaff DW (1993) Sexual stimulation activates c-fos within estrogen-concentrating regions of the female rat forebrain. Brain Res 624:253–267
97. Pfaus JG, Marcangione C, Smith WJ, Manitt C, Abillamaa H (1996) Differential induction of Fos in the female rat brain following different amounts of vaginocervical stimulation: modulation by steroid hormones. Brain Res 741:314–330
98. Pitkanen A (2000) Connectivity of the rat amygdaloid complex. In: Aggleton J (ed) The amygdala. A functional analysis, 2nd edn. Oxford University Press, Oxford, pp 31–115
99. Polston EK, Erskine MS (1995) Patterns of induction of the immediate-early genes c-fos and egr-1 in the female rat brain following differential amounts of mating stimulation. Neuroendocrinology 62:370–384
100. Pro-Sistiaga P, Mohedano-Moriano A, Ubeda-Banon I, Del Mar Arroyo-Jimenez M, Marcos P, Artacho-Perula E, Crespo C, Insausti R, Martinez-Marcos A (2007) Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J Comp Neurol 504:346–362
101. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes dlx-2, emx-1, nkx- 2.1, pax-6, and tbr-1. J Comp Neurol 424:409–438
102. Risold PY (2004) The septal region. In: Paxinos G (ed) The rat nervous system, 3rd edn. Academic Press, San Diego, pp 605–632
103. Risold PY, Canteras NS, Swanson LW (1994) Organization of projections from the anterior hypothalamic nucleus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348:1–40
104. Riviere S, Challet L, Fluegge D, Spehr M, Rodriguez I (2009) Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 459:574–577
105. Rood BD, Stott RT, You S, Smith CJ, Woodbury ME, De Vries GJ (2013) Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J Comp Neurol 521:2321–2358
106. Rosen JB, Fanselow MS, Young SL, Sitcoske M, Maren S (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res 796:132–142
107. Salazar I, Brennan PA (2001) Retrograde labelling of mitral/tufted cells in the mouse accessory olfactory bulb following local injections of the lipophilic tracer DiI into the vomeronasal amygdala. Brain Res 896:198–203
108. Samuelsen CL, Meredith M (2009a) Categorization of biologically relevant chemical signals in the medial amygdala. Brain Res 1263:33–42
109. Samuelsen CL, Meredith M (2009b) The vomeronasal organ is required for the male mouse medial amygdala response to chemical-communication signals, as assessed by immediate early gene expression. Neuroscience 164:1468–1476
110. Sano K, Tsuda MC, Musatov S, Sakamoto T, Ogawa S (2013) Differential effects of site-specific knockdown of estrogen receptor alpha in the medial amygdala, medial pre-optic area, and ventromedial nucleus of the hypothalamus on sexual and aggressive behavior of male mice. Eur J Neurosci 37:1308–1319
111. Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161:31–55
112. Shi CJ, Cassell MD (1998) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399:440–468
113. Shi C, Davis M (1999) Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci 19:420–430
114. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–538
115. Simerly RB (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507–536
116. Simerly RB, Chang C, Muramatsu M, Swanson LW (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76–95
117. Swann J, Fabre-Nys C, Barton R (2009) Hormonal and pheromonal modulation of the extended amygdala: implications for social behavior. In: Pfaff DW, Arnold AP, Fahrbach SE, Etgen AM, Rubin RT (eds) Hormones, brain and behavior, 2nd edn. Academic Press, San Diego, pp 441–474
118. Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113–164
119. Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331
120. Tachikawa KS, Yoshihara Y, Kuroda KO (2013) Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J Neurosci 33:5120–5126
121. Takahashi LK (2014) Olfactory systems and neural circuits that modulate predator odor fear. Front Behav Neurosci 8:72
122. Takahashi LK, Hubbard DT, Lee I, Dar Y, Sipes SM (2007) Predator odor-induced conditioned fear involves the basolateral and medial amygdala. Behav Neurosci 121:100–110
123. Tetel MJ, Getzinger MJ, Blaustein JD (1993) Fos expression in the rat brain following vaginal-cervical stimulation by mating and manual probing. J Neuroendocrinol 5:397–404
124. Thompson RH, Canteras NS, Swanson LW (1996) Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J Comp Neurol 376:143–173
125. Thompson JA, Salcedo E, Restrepo D, Finger TE (2012) Second-order input to the medial amygdala from olfactory sensory neurons expressing the transduction channel TRPM5. J Comp Neurol 520:1819–1830
126. Tirindelli R, Dibattista M, Pifferi S, Menini A (2009) From pheromones to behavior. Physiol Rev 89:921–956
127. Tsukahara S, Tsuda MC, Kurihara R, Kato Y, Kuroda Y, Nakata M, Xiao K, Nagata K, Toda K, Ogawa S (2011) Effects of aromatase or estrogen receptor gene deletion on masculinization of the principal nucleus of the bed nucleus of the stria terminalis of mice. Neuroendocrinology 94(2):137–147
128. Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing. J Comp Neurol 313:295–325
129. Usunoff KG, Schmitt O, Itzev DE, Haas SJ, Lazarov NE, Rolfs A, Wree A (2009) Efferent projections of the anterior and posterodorsal regions of the medial nucleus of the amygdala in the mouse. Cells Tissues Organs 190:256–285
130. Veening JG (1978) Subcortical afferents of the amygdaloid complex in the rat: an HRP study. Neurosci Lett 8:197–202
131. Veening JG, Coolen LM (1998) Neural activation following sexual behavior in the male and female rat brain. Behav Brain Res 92:181–193
132. Veening JG, Coolen LM, de Jong TR, Joosten HW, de Boer SF, Koolhaas JM, Olivier B (2005) Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur J Pharmacol 526:226–239
133. Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212–237
134. Vertes RP, Crane AM, Colom LV, Bland BH (1995) Ascending projections of the posterior nucleus of the hypothalamus: PHA-L analysis in the rat. J Comp Neurol 359:90–116
135. von Campenhausen H, Mori K (2000) Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur J Neurosci 12:33–46
136. Wang Y, He Z, Zhao C, Li L (2013) Medial amygdala lesions modify aggressive behavior and immediate early gene expression in oxytocin and vasopressin neurons during intermale exposure. Behav Brain Res 245:42–49
137. Yokosuka M, Matsuoka M, Ohtani-Kaneko R, Iigo M, Hara M, Hirata K, Ichikawa M (1999) Female-soiled bedding induced fos immunoreactivity in the ventral part of the premammillary nucleus (PMv) of the male mouse. Physiol Behav 68:257–261
138. Zhang WN, Bast T, Feldon J (2001) The ventral hippocampus and fear conditioning in rats: different anterograde amnesias of fear after infusion of N-methyl-d-aspartate or its noncompetitive antagonist MK-801 into the ventral hippocampus. Behav Brain Res 126:159–174
139. Zufall F, Leinders-Zufall T (2007) Mammalian pheromone sensing. Curr Opin Neurobiol 17:483–489