Connections of the juxtaventromedial region of the lateral hypothalamic area in the male rat

Frontiers in Systems Neuroscience

Volumn 9, Issue MAY, 2015, Pages 1-53

  Hahn, Joel D ^a   Swanson, Larry W ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Cognitive systems; Fundamental behavior; Hypothalamus; Lateral hypothalamic area; Motor systems

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMIC NUCLEUS; ARTICLE; BRAIN CORTEX; BRAIN REGION; CEREBRAL NUCLEI; CEREBROSPINAL TRUNK; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; JUXTAVENTROMEDIAL REGION; LATERAL HYPOTHALAMUS; MALE; NERVE FIBER; NEUROANATOMICAL TRACT TRACING; NONHUMAN; NUCLEUS ACCUMBENS; PERIAQUEDUCTAL GRAY MATTER; RAT; REPRODUCTIVE BEHAVIOR; STRIA TERMINALIS; SUPERIOR COLLICULUS; SYNAPSE;

EID: 84930505466     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2015.00066     Document Type: Article

References (201)

1. Armstrong, W. E. (1995). "Hypothalamic supraoptic and paraventricular nuclei, " in The Rat Nervous System, ed G. Paxinos (San Diego, CA: Academic Press), 377-390.
2. Atasoy, D., Betley, J. N., Su, H. H., and Sternson, S. M. (2012). Deconstruction of a neural circuit for hunger. Nature 488, 172-177. doi: 10. 1038/nature11270.
3. Baker, B. L., Dermody, W. C., and Reel, J. R. (1975). Distribution of gonadotropin-releasing hormone in the rat brain as observed with immunocytochemistry. Endocrinology 97, 125-135. doi: 10. 1210/endo-97-1-125.
4. Bargmann, W., and Scharrer, E. (1951). The site of origin of the hormones of the posterior pituitary. Am. Sci. 39, 255-259.
5. Barnett, S. A. (1963). The Rat: A Study In Behavior. Chicago, IL: Aldine Publishing Company.
6. Betley, J. N., Cao, Z. F., Ritola, K. D., and Sternson, S. M. (2013). Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell 155, 1337-1350. doi: 10. 1016/j. cell. 2013. 11. 002.
7. Bota, M., Spoorns, O., and Swanson, L. W. (2015). Architecture of the cerebral cortical association connectome underlying cognition. Proc. Natl. Acad. Sci. U. S. A. 112, E2093-E2101. doi: 10. 1073/pnas. 1504394112.
8. Bota, M., Talpalaru, S., Hintiryan, H., Dong, H. W., and Swanson, L. W. (2014). BAMS2 workspace: a comprehensive and versatile neuroinformatic platform for collating and processing neuroanatomical connections. J. Comp. Neurol. 522, 3160-3176. doi: 10. 1002/cne. 23592.
9. Broberger, C. (1999). Hypothalamic cocaine-and amphetamine-regulated transcript (CART) neurons: histochemical relationship to thyrotropin-releasing hormone, melanin-concentrating hormone, orexin/hypocretin and neuropeptide Y. Brain Res. 848, 101-113. doi: 10. 1016/S0006-8993(99)01977-0.
10. Brown, R. A., and Swanson, L. W. (2013). Neural systems language: a formal modeling language for the systematic description, unambiguous communication, and automated digital curation of neural connectivity. J. Comp. Neurol. 521, 2889-2906. doi: 10. 1002/cne. 23348.
11. Buzsaki, G., and Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130-138. doi: 10. 1038/nn. 3304.
12. Cant, N. B., and Benson, C. G. (2003). Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res. Bull. 60, 457-474. doi: 10. 1016/S0361-9230(03)00050-9.
13. Canteras, N. S. (2002). The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol. Biochem. Behav. 71, 481-491. doi: 10. 1016/S0091-3057(01)00685-2.
14. Canteras, N. S., Chiavegatto, S., DoValle, L. E. R., and Swanson, L. W. (1997). Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res. Bull. 44, 297-305. doi: 10. 1016/S0361-9230(97)00141-X.
15. Canteras, N. S., and Graeff, F. G. (2014). Executive and modulatory neural circuits of defensive reactions: implications for panic disorder. Neurosci. Biobehav. Rev. 46(Pt 3), 352-364. doi: 10. 1016/j. neubiorev. 2014. 03. 020.
16. Canteras, N. S., Simerly, R. B., and Swanson, L. W. (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. doi: 10. 1002/cne. 903480103.
17. Carrive, P., Leung, P., Harris, J., and Paxinos, G. (1997). Conditioned fear to context is associated with increased Fos expression in the caudal ventrolateral region of the midbrain periaqueductal gray. Neuroscience 78, 165-177. doi: 10. 1016/S0306-4522(97)83047-3.
18. Cenquizca, L. A., and Swanson, L. W. (2007). Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res. Rev. 56, 1-26. doi: 10. 1016/j. brainresrev. 2007. 05. 002.
19. Choi, G. B., Dong, H. W., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Swanson, L. W., et al. (2005). Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46, 647-660. doi: 10. 1016/j. neuron. 2005. 04. 011.
20. Cole, S., Hobin, M. P., and Petrovich, G. D. (2015). Appetitive associative learning recruits a distinct network with cortical, striatal, and hypothalamic regions. Neuroscience 286, 187-202. doi: 10. 1016/j. neuroscience. 2014. 11. 026.
21. Cole, S., Powell, D. J., and Petrovich, G. D. (2013). Differential recruitment of distinct amygdalar nuclei across appetitive associative learning. Learn. Mem. 20, 295-299. doi: 10. 1101/lm. 031070. 113.
22. Comoli, E., Das Neves Favaro, P., Vautrelle, N., Leriche, M., Overton, P. G., and Redgrave, P. (2012). Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense. Front. Neuroanat. 6: 9. doi: 10. 3389/fnana. 2012. 00009.
23. Coolen, L. M., Peters, H. J., and Veening, J. G. (1996). Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res. 738, 67-82. doi: 10. 1016/0006-8993(96)00763-9.
24. Coolen, L. M., Peters, H. J., and Veening, J. G. (1998). Anatomical interrelationships of the medial preoptic area and other brain regions activated following male sexual behavior: a combined fos and tract-tracing study. J. Comp. Neurol. 397, 421-435.
25. Cowley, D. S., and Arana, G. W. (1990). The diagnostic utility of lactate sensitivity in panic disorder. Arch. Gen. Psychiatry 47, 277-284. doi: 10. 1001/archpsyc. 1990. 01810150077012.
26. Cvetkovic, V., Brischoux, F., Jacquemard, C., Fellmann, D., Griffond, B., and Risold, P. Y. (2004). Characterization of subpopulations of neurons producing melanin-concentrating hormone in the rat ventral diencephalon. J. Neurochem. 91, 911-919. doi: 10. 1111/j. 1471-4159. 2004. 02776. x.
27. Davis, M., Gendelman, D. S., Tischler, M. D., and Gendelman, P. M. (1982). A primary acoustic startle circuit: lesion and stimulation studies. J. Neurosci. 2, 791-805.
28. Dean, P., Redgrave, P., and Westby, G. W. (1989). Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12, 137-147. doi: 10. 1016/0166-2236(89)90052-0.
29. Del Cid-Pellitero, E., and Jones, B. E. (2012). Immunohistochemical evidence for synaptic release of GABA from melanin-concentrating hormone containing varicosities in the locus coeruleus. Neuroscience 223, 269-276. doi: 10. 1016/j. neuroscience. 2012. 07. 072.
30. DesJardin, J. T., Holmes, A. L., Forcelli, P. A., Cole, C. E., Gale, J. T., Wellman, L. L., et al. (2013). Defense-like behaviors evoked by pharmacological disinhibition of the superior colliculus in the primate. J. Neurosci. 33, 150-155. doi: 10. 1523/JNEUROSCI. 2924-12. 2013.
31. DeVries, G. J., Buijs, R. M., Van Leeuwen, F. W., Caffe, A. R., and Swaab, D. F. (1985). The vasopressinergic innervation of the brain in normal and castrated rats. J. Comp. Neurol. 233, 236-254. doi: 10. 1002/cne. 902330206.
32. Dielenberg, R. A., Hunt, G. E., and McGregor, I. S. (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. doi: 10. 1016/S0306-4522(01)00150-6.
33. Dong, H. W., Petrovich, G. D., and Swanson, L. W. (2001a). Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 38, 192-246. doi: 10. 1016/S0165-0173(01)00079-0.
34. Dong, H. W., Petrovich, G. D., Watts, A. G., and Swanson, L. W. (2001b). Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J. Comp. Neurol. 436, 430-455. doi: 10. 1002/cne. 1079.
35. Dong, H. W., and Swanson, L. W. (2003). Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors. J. Comp. Neurol. 463, 434-472. doi: 10. 1002/cne. 10758.
36. Dong, H. W., and Swanson, L. W. (2004a). Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J. Comp. Neurol. 468, 277-298. doi: 10. 1002/cne. 10949.
37. Dong, H. W., and Swanson, L. W. (2004b). 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. doi: 10. 1002/cne. 20002.
38. Dong, H. W., and Swanson, L. W. (2006a). Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J. Comp. Neurol. 494, 142-178. doi: 10. 1002/cne. 20788.
39. Dong, H. W., and Swanson, L. W. (2006b). Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J. Comp. Neurol. 494, 75-107. doi: 10. 1002/cne. 20790.
40. Dong, H. W., and Swanson, L. W. (2006c). Projections from bed nuclei of the stria terminalis, magnocellular nucleus: implications for cerebral hemisphere regulation of micturition, defecation, and penile erection. J. Comp. Neurol. 494, 108-141. doi: 10. 1002/cne. 20789.
41. Dong, H. W., Swanson, L. W., Chen, L., Fanselow, M. S., and Toga, A. W. (2009). Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. U. S. A. 106, 11794-11799. doi: 10. 1073/pnas. 0812608106.
42. Dumas, M., Schwab, M. E., and Thoenen, H. (1979). Retrograde axonal transport of specific macromolecules as a tool for characterizing nerve terminal membranes. J. Neurobiol. 10, 179-197. doi: 10. 1002/neu. 480100207.
43. Elias, C. F., Lee, C. E., Kelly, J. F., Ahima, R. S., Kuhar, M., Saper, C. B., et al. (2001). Characterization of CART neurons in the rat and human hypothalamus. J. Comp. Neurol. 432, 1-19. doi: 10. 1002/cne. 1085.
44. Engelmann, M., Ebner, K., Landgraf, R., Holsboer, F., and Wotjak, C. T (1999). Emotional stress triggers intrahypothalamic but not peripheral release of oxytocin in male rats. J. Neuroendocrinol. 11, 867-872. doi: 10. 1046/j. 1365-2826. 1999. 00403. x.
45. Fanselow, M. S., and Dong, H. W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19. doi: 10. 1016/j. neuron. 2009. 11. 031.
46. Farrell, M. S., and Roth, B. L. (2013). Pharmacosynthetics: reimagining the pharmacogenetic approach. Brain Res. 1511, 6-20. doi: 10. 1016/j. brainres. 2012. 09. 043.
47. Faturi, C. B., Rangel, M. J. Jr. Baldo, M. V., and Canteras, N. S. (2014). Functional mapping of the circuits involved in the expression of contextual fear responses in socially defeated animals. Brain Struct. Funct. 219, 931-946. doi: 10. 1007/s00429-013-0544-4.
48. Fenno, L., Yizhar, O., and Deisseroth, K. (2011). The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389-412. doi: 10. 1146/annurev-neuro-061010-113817.
49. Foo, K. S., Brismar, H., and Broberger, C. (2008). Distribution and neuropeptide coexistence of nucleobindin-2 mRNA/nesfatin-like immunoreactivity in the rat CNS. Neuroscience 156, 563-579. doi: 10. 1016/j. neuroscience. 2008. 07. 054.
50. Fort, P., Salvert, D., Hanriot, L., Jego, S., Shimizu, H., Hashimoto, K., et al. (2008). The satiety molecule nesfatin-1 is co-expressed with melanin concentrating hormone in tuberal hypothalamic neurons of the rat. Neuroscience 155, 174-181. doi: 10. 1016/j. neuroscience. 2008. 05. 035.
51. Fulton, J. F., Ranson, S. W., and Frantz, A. M. (1940). The Hypothalamus and Central Levels of Autonomic Function. Baltimore, MD: The Williams and Wilkins Co.
52. Gerfen, C. R., and Sawchenko, P. E. (1984). An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 290, 219-238. doi: 10. 1016/0006-8993(84)90940-5.
53. Gonzalez-Hernandez, T., Mantolan-Sarmiento, B., Gonzalez-Gonzalez, B., and Perez-Gonzalez, H. (1996). Sources of GABAergic input to the inferior colliculus of the rat. J. Comp. Neurol. 372, 309-326.
54. Goto, M., Canteras, N. S., Burns, G., and Swanson, L. W. (2005). Projections from the subfornical region of the lateral hypothalamic area. J. Comp. Neurol. 493, 412-438. doi: 10. 1002/cne. 20764.
55. Goto, M., Swanson, L. W., and Canteras, N. S. (2001). Connections of the nucleus incertus. J. Comp. Neurol. 438, 86-122. doi: 10. 1002/cne. 1303.
56. Groenewegen, H. J., Vermeulen-Van der Zee, E., te, K. A., and Witter, M. P. (1987). Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience 23, 103-120. doi: 10. 1016/0306-4522(87)90275-2.
57. Gross, C. T., and Canteras, N. S. (2012). The many paths to fear. Nat. Rev. Neurosci. 13, 651-658. doi: 10. 1038/nrn3301.
58. Gu, G. B., and Simerly, R. B. (1997). Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J. Comp. Neurol. 384, 142-164.
59. Gurdjian, E. S. (1927). The diencephalon of the albino rat. Studies on the brain of the rat. No. 2. J. Comp. Neurol. 43, 1-114. doi: 10. 1002/cne. 900430102.
60. Hahn, J. D. (2010). Comparison of melanin-concentrating hormone and hypocretin/orexin peptide expression patterns in a current parceling scheme of the lateral hypothalamic zone. Neurosci. Lett. 468, 12-17. doi: 10. 1016/j. neulet. 2009. 10. 047.
61. Hahn, J. D., and Coen, C. W. (2006). Comparative study of the sources of neuronal projections to the site of gonadotrophin-releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats. J. Comp. Neurol. 494, 190-214. doi: 10. 1002/cne. 20803.
62. Hahn, J. D., and Swanson, L. W. (2010). Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res. Rev. 64, 14-103. doi: 10. 1016/j. brainresrev. 2010. 02. 002.
63. Hahn, J. D., and Swanson, L. W. (2012). Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat. J. Comp. Neurol. 520, 1831-1890. doi: 10. 1002/cne. 23064.
64. Harris, G. W. (1955). Neural Control of the Pituitary Gland. London: Arnold.
65. Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K. W., et al. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol. 497, 326-349. doi: 10. 1002/cne. 20970.
66. Haymaker, W., Anderson, E., and Nauta, W. J. H. (1969). The Hypothalamus. Illinois, IL: Charles C Thomas.
67. Henny, P., Brischoux, F., Mainville, L., Stroh, T., and Jones, B. E. (2010). Immunohistochemical evidence for synaptic release of glutamate from orexin terminals in the locus coeruleus. Neuroscience 169, 1150-1157. doi: 10. 1016/j. neuroscience. 2010. 06. 003.
68. Ho, C. Y., and Berridge, K. C. (2014). Excessive disgust caused by brain lesions or temporary inactivations: mapping hotspots of the nucleus accumbens and ventral pallidum. Eur. J. Neurosci. 40, 3556-3572. doi: 10. 1111/ejn. 12720.
69. Holland, P. C., Petrovich, G. D., and Gallagher, M. (2002). The effects of amygdala lesions on conditioned stimulus-potentiated eating in rats. Physiol. Behav. 76, 117-129. doi: 10. 1016/S0031-9384(02)00688-1.
70. Honda, K., Yanagimoto, M., Negoro, H., Narita, K., Murata, T., and Higuchi, T. (1999). Excitation of oxytocin cells in the hypothalamic supraoptic nucleus by electrical stimulation of the dorsal penile nerve and tactile stimulation of the penis in the rat. Brain Res. Bull. 48, 309-313. doi: 10. 1016/S0361-9230(98)00180-4.
71. Hou-Yu, A., Lamme, A. T., Zimmerman, E. A., and Silverman, A. J. (1986). Comparative distribution of vasopressin and oxytocin neurons in the rat brain using a double-label procedure. Neuroendocrinology 44, 235-246. doi: 10. 1159/000124651.
72. Hrabovszky, E., Halasz, J., Meelis, W., Kruk, M. R., Liposits, Z., and Haller, J. (2005). Neurochemical characterization of hypothalamic neurons involved in attack behavior: glutamatergic dominance and co-expression of thyrotropin-releasing hormone in a subset of glutamatergic neurons. Neuroscience 133, 657-666. doi: 10. 1016/j. neuroscience. 2005. 03. 042.
73. Hsu, T. M., Hahn, J. D., Konanur, V. R., Lam, A., and Kanoski, S. E. (2014). Hippocampal GLP-1 Receptors influence food intake, meal size, and effort-based responding for food through volume transmission. Neuropsychopharmacology 40, 327-337. doi: 10. 1038/npp. 2014. 175.
74. Inglis, W. L., and Winn, P. (1995). The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog. Neurobiol. 47, 1-29. doi: 10. 1016/0301-0082(95)00013-L.
75. Jego, S., Glasgow, S. D., Herrera, C. G., Ekstrand, M., Reed, S. J., Boyce, R., et al. (2013). Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nat. Neurosci. 16, 1637-1643. doi: 10. 1038/nn. 3522.
76. Jhou, T. C., Geisler, S., Marinelli, M., Degarmo, B. A., and Zahm, D. S. (2009). The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J. Comp. Neurol. 513, 566-596. doi: 10. 1002/cne. 21891.
77. Johnson, P., Lowry, C., Truitt, W., and Shekhar, A. (2008). Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. J. Psychopharmacol. 22, 642-652. doi: 10. 1177/0269881107082900.
78. Johnson, P. L., Fitz, S. D., Hollis, J. H., Moratalla, R., Lightman, S. L., Shekhar, A., et al. (2011). Induction of c-Fos in 'panic/defence'-related brain circuits following brief hypercarbic gas exposure. J. Psychopharmacol. 25, 26-36. doi: 10. 1177/0269881109353464.
79. Kanoski, S. E., Hayes, M. R., Greenwald, H. S., Fortin, S. M., Gianessi, C. A., Gilbert, J. R., et al. (2011). Hippocampal leptin signaling reduces food intake and modulates food-related memory processing. Neuropsychopharmacology 36, 1859-1870. doi: 10. 1038/npp. 2011. 70.
80. Karnani, M. M., Szabo, G., Erdelyi, F., and Burdakov, D. (2013). Lateral hypothalamic GAD65 neurons are spontaneously firing and distinct from orexin-and melanin-concentrating hormone neurons. J. Physiol. 591, 933-953. doi: 10. 1113/jphysiol. 2012. 243493.
81. Kasper, E. M., Larkman, A. U., Lubke, J., and Blakemore, C. (1994). Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets. J. Comp. Neurol. 339, 459-474. doi: 10. 1002/cne. 903390402.
82. Kay-Nishiyama, C., and Watts, A. G. (1999). Dehydration modifies somal CRH immunoreactivity in the rat hypothalamus: an immunocytochemical study in the absence of colchicine. Brain Res. 822, 251-255. doi: 10. 1016/S0006-8993(99)01130-0.
83. Keen-Rhinehart, E., Ondek, K., and Schneider, J. E. (2013). Neuroendocrine regulation of appetitive ingestive behavior. Front. Neurosci. 7: 213. doi: 10. 3389/fnins. 2013. 00213.
84. Keim, S. R., and Shekhar, A. (1996). The effects of GABAA receptor blockade in the dorsomedial hypothalamic nucleus on corticotrophin (ACTH) and corticosterone secretion in male rats. Brain Res. 739, 46-51. doi: 10. 1016/S0006-8993(96)00810-4.
85. Kelly, A. B., and Watts, A. G. (1996). Mediation of dehydration-induced peptidergic gene expression in the rat lateral hypothalamic area by forebrain afferent projections. J. Comp. Neurol. 370, 231-246.
86. Kelly, A. B., and Watts, A. G. (1998). The region of the pontine parabrachial nucleus is a major target of dehydration-sensitive CRH neurons in the rat lateral hypothalamic area. J. Comp. Neurol. 394, 48-63.
87. Kelly, J., and Swanson, L. W. (1980). Additional forebrain regions projecting to the posterior pituitary-preoptic region, bed nucleus of the stria terminalis, and zona incerta. Brain Res. 197, 1-9. doi: 10. 1016/0006-8993(80)90430-8.
88. Kita, T., and Kita, H. (2011). Cholinergic and non-cholinergic mesopontine tegmental neurons projecting to the subthalamic nucleus in the rat. Eur. J. Neurosci. 33, 433-443. doi: 10. 1111/j. 1460-9568. 2010. 07537. x.
89. Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H. A., Murison, R., Moser, E. I., and Moser, M. B. (2002). Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. U. S. A. 99, 10825-10830. doi: 10. 1073/pnas. 152112399.
90. Krieg, W. J. S. (1932). The hypothalamus of the albino rat. J. Comp. Neurol. 55, 19-89. doi: 10. 1002/cne. 900550104.
91. Le Gros Clark, W. E. (1938. "The hypothalamus, morphological, functional, clinical and surgical aspects, ") in The Hypothalamus, eds W. E. Le Gros Clark, J. Beattie, G. Riddoch, and N. M. Dott (Edinburgh: Oliver and Boyd), 1-68.
92. Lee, H., Kim, D. W., Remedios, R., Anthony, T. E., Chang, A., Madisen, L., et al. (2014). Scalable control of mounting and attack by Esr1 neurons in the ventromedial hypothalamus. Nature 509, 627-632. doi: 10. 1038/nature13169.
93. Lee, Y., Lopez, D. E., Meloni, E. G., and Davis, M. (1996). A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J. Neurosci. 16, 3775-3789.
94. Lin, D., Boyle, M. P., Dollar, P., Lee, H., Lein, E. S., Perona, P., et al. (2011). Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226. doi: 10. 1038/nature09736.
95. Luppi, P. H., Fort, P., and Jouvet, M. (1990). Iontophoretic application of unconjugated cholera toxin B subunit (CTb) combined with immunohistochemistry of neurochemical substances: a method for transmitter identification of retrogradely labeled neurons. Brain Res. 534, 209-224. doi: 10. 1016/0006-8993(90)90131-T.
96. Luppi, P. H., Sakai, K., Salvert, D., Fort, P., and Jouvet, M. (1987). Peptidergic hypothalamic afferents to the cat nucleus raphe pallidus as revealed by a double immunostaining technique using unconjugated cholera toxin as a retrograde tracer. Brain Res. 402, 339-345. doi: 10. 1016/0006-8993(87)90041-2.
97. Markakis, E. A., and Swanson, L. W. (1997). Spatiotemporal patterns of secretomotor neuron generation in the parvicellular neuroendocrine system. Brain Res. Rev. 24, 255-291. doi: 10. 1016/S0165-0173(97)00006-4.
98. Markham, C. M., Taylor, S. L., and Huhman, K. L. (2010). Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters. Learn. Mem. 17, 109-116. doi: 10. 1101/lm. 1633710.
99. Mason, W. T., Ho, Y. W., and Hatton, G. I. (1984). Axon collaterals of supraoptic neurones: anatomical and electrophysiological evidence for their existence in the lateral hypothalamus. Neuroscience 11, 169-182. doi: 10. 1016/0306-4522(84)90221-5.
100. Matsumoto, J., Urakawa, S., Hori, E., de Araujo, M. F., Sakuma, Y., Ono, T., et al. (2012). Neuronal responses in the nucleus accumbens shell during sexual behavior in male rats. J. Neurosci. 32, 1672-1686. doi: 10. 1523/JNEUROSCI. 5140-11. 2012.
101. McDonald, A. J. (1998). Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55, 257-332. doi: 10. 1016/S0301-0082(98)00003-3.
102. McDowall, L. M., Horiuchi, J., Killinger, S., and Dampney, R. A. (2006). Modulation of the baroreceptor reflex by the dorsomedial hypothalamic nucleus and perifornical area. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1020-R1026. doi: 10. 1152/ajpregu. 00541. 2005.
103. Meister, B. (2007). Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol. Behav. 92, 263-271. doi: 10. 1016/j. physbeh. 2007. 05. 021.
104. Merchenthaler, I., Gorcs, T., Setalo, G., Petrusz, P., and Flerko, B. (1984). Gonadotropin-releasing hormone (GnRH) neurons and pathways in the rat brain. Cell Tissue Res. 237, 15-29. doi: 10. 1007/BF00229195.
105. Meredith, M. A., and Stein, B. E. (1986). Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J. Neurophysiol. 56, 640-662.
106. Millhouse, O. E. (1969). A Golgi study of the desending medial forebrain bundle. Brain Res. 15, 341-363. doi: 10. 1016/0006-8993(69)90161-9.
107. Millhouse, O. E. (1973). The organization of the ventromedial hypothalamic nucleus. Brain Res. 55, 71-87. doi: 10. 1016/0006-8993(73)90489-7.
108. Millhouse, O. E. (1979). "A Golgi anatomy of the rodent hypothalamus, " in Anatomy of the Hypothalamus, Vol. 1, eds P. J. Morgane and J. Panksepp (New York, NY: Dekker), 221-265.
109. Mohedano-Moriano, A., Pro-Sistiaga, P., Ubeda-Banon, I., Crespo, C., Insausti, R., and 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. doi: 10. 1111/j. 1460-9568. 2007. 05472. x.
110. Morgane, P. J., and Panksepp, J. (1979). Anatomy of the Hypothalamus. New York, NY: Dekker.
111. Morin, L. P., and Studholme, K. M. (2014). Retinofugal projections in the mouse. J. Comp. Neurol. 522, 3733-3753. doi: 10. 1002/cne. 23635.
112. Morris, R. (2006). "Theories of hippocampal function, " in The Hippocampus Book, eds P. Andersen, R. Morris, D. Amaral, T. Bliss, and J. O'Keefe (Oxford: Oxford University Press), 581-714.
113. Nauta, W. J. H., and Haymaker, W. (1969). "Hypothalamic nuclei and fiber connections, " in The Hypothalamus, eds W. Haymaker, E. Anderson, and W. J. H. Nauta (Illinois, IL: Charles C Thomas), 136-209.
114. Netzer, F., Bernard, J. F., Verberne, A. J., Hamon, M., Camus, F., Benoliel, J. J., et al. (2011). Brain circuits mediating baroreflex bradycardia inhibition in rats: an anatomical and functional link between the cuneiform nucleus and the periaqueductal grey. J. Physiol. 589, 2079-2091. doi: 10. 1113/jphysiol. 2010. 203737.
115. O'Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map. Oxford: Oxford University Press.
116. Pattij, T., de Jong, T. R., Uitterdijk, A., Waldinger, M. D., Veening, J. G., Cools, A. R., et al. (2005). Individual differences in male rat ejaculatory behaviour: searching for models to study ejaculation disorders. Eur. J. Neurosci. 22, 724-734. doi: 10. 1111/j. 1460-9568. 2005. 04252. x.
117. Pawluski, J. L., and Galea, L. A. (2006). Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 66, 71-81. doi: 10. 1002/neu. 20194.
118. Pentkowski, N. S., Blanchard, D. C., Lever, C., Litvin, Y., and Blanchard, R. J. (2006). Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur. J. Neurosci. 23, 2185-2196. doi: 10. 1111/j. 1460-9568. 2006. 04754. x.
119. Petrovich, G. D., Canteras, N. S., and Swanson, L. W. (2001). Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 38, 247-289. doi: 10. 1016/S0165-0173(01)00080-7.
120. Petrovich, G. D., Holland, P. C., and Gallagher, M. (2005). Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J. Neurosci. 25, 8295-8302. doi: 10. 1523/JNEUROSCI. 2480-05. 2005.
121. Pitkanen, A., Stefanacci, L., Farb, C. R., Go, G. G., LeDoux, J. E., and Amaral, D. G. (1995). Intrinsic connections of the rat amygdaloid complex: projections originating in the lateral nucleus. J. Comp. Neurol. 356, 288-310. doi: 10. 1002/cne. 903560211.
122. Pollak, G. D., Burger, R. M., and Klug, A. (2003). Dissecting the circuitry of the auditory system. Trends Neurosci. 26, 33-39. doi: 10. 1016/S0166-2236(02)00009-7.
123. Pro-Sistiaga, P., Mohedano-Moriano, A., Ubeda-Banon, I., Mar Arroyo-Jimenez, M., Marcos, P., Artacho-Perula, E., et al. (2007). Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J. Comp. Neurol. 504, 346-362. doi: 10. 1002/cne. 21455.
124. Ramon y Cajal, S. (1995). Histology of the Nervous System of Man and Vertebrates. New York, NY: Oxford University Press.
125. Randle, J. C., Bourque, C. W., and Renaud, L. P. (1986). Serial reconstruction of Lucifer yellow-labeled supraoptic nucleus neurons in perfused rat hypothalamic explants. Neuroscience 17, 453-467. doi: 10. 1016/0306-4522(86)90259-9.
126. Richard, J. M., Castro, D. C., Difeliceantonio, A. G., Robinson, M. J., and Berridge, K. C. (2013). Mapping brain circuits of reward and motivation: in the footsteps of Ann Kelley. Neurosci. Biobehav. Rev. 37, 1919-1931. doi: 10. 1016/j. neubiorev. 2012. 12. 008.
127. Risold, P. Y., Canteras, N. S., and Swanson, L. W. (1994). Organization of projections from the anterior hypothalamic nucleus-a Phaseolus-Vulgaris-Leukoagglutinin study in the rat. J. Comp. Neurol. 348, 1-40. doi: 10. 1002/cne. 903480102.
128. Risold, P. Y., and Swanson, L. W. (1996). Structural evidence for functional domains in the rat hippocampus. Science 272, 1484-1486. doi: 10. 1126/science. 272. 5267. 1484.
129. Risold, P. Y., and Swanson, L. W. (1997a). Chemoarchitecture of the rat lateral septal nucleus. Brain Res. Brain Res. Rev. 24, 91-113. doi: 10. 1016/S0165-0173(97)00008-8.
130. Risold, P. Y., and Swanson, L. W. (1997b). Connections of the rat lateral septal complex. Brain Res. Brain Res. Rev. 24, 115-195. doi: 10. 1016/S0165-0173(97)00009-X.
131. Risold, P. Y., Thompson, R. H., and Swanson, L. W. (1997). The structural organization of connections between hypothalamus and cerebral cortex. Brain Res. Brain Res. Rev. 24, 197-254. doi: 10. 1016/S0165-0173(97)00007-6.
132. Rye, D. B., Lee, H. J., Saper, C. B., and Wainer, B. H. (1988). Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J. Comp. Neurol. 269, 315-341. doi: 10. 1002/cne. 902690302.
133. Rye, D. B., Saper, C. B., Lee, H. J., and Wainer, B. H. (1987). Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J. Comp. Neurol. 259, 483-528. doi: 10. 1002/cne. 902590403.
134. Saper, C. B., Swanson, L. W., and Cowan, W. M. (1979). An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J. Comp. Neurol. 183, 689-706. doi: 10. 1002/cne. 901830402.
135. Scalia, F., and Winans, S. S. (1975). The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161, 31-55. doi: 10. 1002/cne. 901610105.
136. Schmued, L. C., and Fallon, J. H. (1986). Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res. 377, 147-154. doi: 10. 1016/0006-8993(86)91199-6.
137. Sharpe, L. G., and Swanson, L. W. (1974). Drinking induced by injections of angiotensin into forebrain and mid-brain sites of monkey. J. Physiol. 239, 595-622. doi: 10. 1113/jphysiol. 1974. sp010584.
138. Shekhar, A. (1993). GABA receptors in the region of the dorsomedial hypothalamus of rats regulate anxiety in the elevated plus-maze test. I. Behavioral measures. Brain Res. 627, 9-16. doi: 10. 1016/0006-8993(93)90742-6.
139. Shekhar, A., Keim, S. R., Simon, J. R., and McBride, W. J. (1996). Dorsomedial hypothalamic GABA dysfunction produces physiological arousal following sodium lactate infusions. Pharmacol. Biochem. Behav. 55, 249-256. doi: 10. 1016/S0091-3057(96)00077-9.
140. Shekhar, A., Sims, L. S., and Bowsher, R. R. (1993). GABA receptors in the region of the dorsomedial hypothalamus of rats regulate anxiety in the elevated plus-maze test. II. Physiological measures. Brain Res. 627, 17-24. doi: 10. 1016/0006-8993(93)90743-7.
141. Shimogawa, Y., Sakuma, Y., and Yamanouchi, K. (2014). Efferent and afferent connections of the ventromedial hypothalamic nucleus determined by neural tracer analysis: implications for lordosis regulation in female rats. Neurosci Res. 91, 19-33. doi: 10. 1016/j. neures. 2014. 10. 016.
142. Shughrue, P. J., Lane, M. V., and Merchenthaler, I. (1997). Comparative distribution of estrogen receptor-alpha and-beta mRNA in the rat central nervous system. J. Comp. Neurol. 388, 507-525.
143. Silverman, A. J., Jhamandas, J., and Renaud, L. P. (1987). Localization of luteinizing hormone-releasing hormone (LHRH) neurons that project to the median eminence. J. Neurosci. 7, 2312-2319.
144. Simerly, R. B. (2002). Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25, 507-536. doi: 10. 1146/annurev. neuro. 25. 112701. 142745.
145. Simerly, R. B., Chang, C., Muramatsu, M., and Swanson, L. W. (1990). Distribution of androgen and estrogen-receptor messenger rna-containing cells in the rat-brain-an Insitu hybridization study. J. Comp. Neurol. 294, 76-95. doi: 10. 1002/cne. 902940107.
146. Simmons, D. M., and Swanson, L. W. (1993). "The nissl stain, " in Neuroscience Protocols, ed F. G. Wouterlood (Amsterdam: Elsevier), 1-7.
147. Simmons, D. M., and Swanson, L. W. (2009). Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: toward a global 3D model. J. Comp. Neurol. 516, 423-441. doi: 10. 1002/cne. 22126.
148. Simon, D. K., and O'Leary, D. D. (1992). Development of topographic order in the mammalian retinocollicular projection. J. Neurosci. 12, 1212-1232.
149. Smithson, K. G., Weiss, M. L., and Hatton, G. I. (1992). Supraoptic nucleus afferents from the accessory olfactory bulb: evidence from anterograde and retrograde tract tracing in the rat. Brain Res. Bull. 29, 209-220. doi: 10. 1016/0361-9230(92)90028-V.
150. Sohn, J. W., Elmquist, J. K., and Williams, K. W. (2013). Neuronal circuits that regulate feeding behavior and metabolism. Trends Neurosci. 36, 504-512. doi: 10. 1016/j. tins. 2013. 05. 003.
151. Squire, L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195-231. doi: 10. 1037/0033-295X. 99. 2. 195.
152. Stein, B. E., Stanford, T. R., and Rowland, B. A. (2009). The neural basis of multisensory integration in the midbrain: its organization and maturation. Hear. Res. 258, 4-15. doi: 10. 1016/j. heares. 2009. 03. 012.
153. Steininger, T. L., Rye, D. B., and Wainer, B. H. (1992). Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. I. Retrograde tracing studies. J. Comp. Neurol. 321, 515-543. doi: 10. 1002/cne. 903210403.
154. Sternson, S. M. (2013). Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 77, 810-824. doi: 10. 1016/j. neuron. 2013. 02. 018.
155. Stoeckel, K., Schwab, M., and Thoenen, H. (1977). Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin. Brain Res. 132, 273-285. doi: 10. 1016/0006-8993(77)90421-8.
156. Stoneham, M. D., Everitt, B. J., Hansen, S., Lightman, S. L., and Todd, K. (1985). Oxytocin and sexual behaviour in the male rat and rabbit. J. Endocrinol. 107, 97-106. doi: 10. 1677/joe. 0. 1070097.
157. Strange, B. A., Witter, M. P., Lein, E. S., and Moser, E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 15, 655-669. doi: 10. 1038/nrn3785.
158. Swanson, L. W. (1981). Tracing central pathways with the autoradiographic method. J. Histochem. Cytochem. 29, 117-124. doi: 10. 1177/29. 1A_Suppl. 7288150.
159. Swanson, L. W. (1986). "Organization of the mammalian neuroendocrine system, " in Handbook of Physiology, The Nervous System, Vol. 4, ed F. E. Bloom (Baltimore: Waverly Press), 169-190.
160. Swanson, L. W. (1987). "The hypothalamus, " in Handbook of Chemical Neuroanatomy, Vol. 5, eds A. Bjorklund, T. Hokfelt and L. W. Swanson (Amsterdam: Elsevier), 1-124.
161. Swanson, L. W. (1999). The neuroanatomy revolution of the 1970s and the hypothalamus. Brain Res. Bull. 50, 397. doi: 10. 1016/S0361-9230(99)00163-X.
162. Swanson, L. W. (2000). Cerebral hemisphere regulation of motivated behavior. Brain Res. 886, 113-164. doi: 10. 1016/S0006-8993(00)02905-X.
163. Swanson, L. W. (2004). Brain Maps: Structure of the Rat Brain, 3rd Edn. Amsterdam: Academic Press.
164. Swanson, L. W. (2007). Quest for the basic plan of nervous system circuitry. Brain Res. Rev. 55, 356-372. doi: 10. 1016/j. brainresrev. 2006. 12. 006.
165. Swanson, L. W., and Bota, M. (2010). Foundational model of structural connectivity in the nervous system with a schema for wiring diagrams, connectome, and basic plan architecture. Proc. Natl. Acad. Sci. U. S. A. 107, 20610-20617. doi: 10. 1073/pnas. 1015128107.
166. Swanson, L. W., and Cowan, W. M. (1976). "Autoradiographic studies of the development and connections of the septal area in the rat, " in The Septal Nuclei: Advances in Behavioral Biology, Vol. 20, ed J. F. DeFrance (New York, NY Springer US), 37-64. doi: 10. 1007/978-1-4684-3084-4_2.
167. Swanson, L. W., and Cowan, W. M. (1977). Autoradiographic study of organization of efferent connections of hippocampal formation in rat. J. Comp. Neurol. 172, 49-84. doi: 10. 1002/cne. 901720104.
168. Swanson, L. W., and Petrovich, G. D. (1998). What is the amygdala? Trends Neurosci. 21, 323-331. doi: 10. 1016/S0166-2236(98)01265-X.
169. Swanson, L. W., Sanchez-Watts, G., and Watts, A. G. (2005). Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci. Lett. 387, 80-84. doi: 10. 1016/j. neulet. 2005. 06. 066.
170. Swanson, L. W., and Sharpe, L. G. (1973). Centrally induced drinking-comparison of angiotensin-Ii-sensitive and carbachol-sensitive sites in rats. Am. J. Physiol. 225, 566-573.
171. Swanson, L. W., Sharpe, L. G., and Griffin, D. (1973). Drinking to intracerebral angiotensin-Ii and Carbachol-Dose-response relationships and ionic involvement. Physiol. Behav. 10, 595-600. doi: 10. 1016/0031-9384(73)90227-8.
172. Thellier, D., Moos, F., Richard, P., and Stoeckel, M. E. (1994a). Evidence for connections between a discrete hypothalamic dorsochiasmatic area and the supraoptic and paraventricular nuclei. Brain Res. Bull. 34, 261-274. doi: 10. 1016/0361-9230(94)90063-9.
173. Thellier, D., Moos, F., Richard, P., and Stoeckel, M. E. (1994b). Evidence for reciprocal connections between the dorsochiasmatic area and the hypothalamo neurohypophyseal system and some related extrahypothalamic structures. Brain Res. Bull. 35, 311-322. doi: 10. 1016/0361-9230(94)90107-4.
174. Thompson, C. L., Pathak, S. D., Jeromin, A., Ng, L. L., MacPherson, C. R., Mortrud, M. T., et al. (2008). Genomic anatomy of the hippocampus. Neuron 60, 1010-1021. doi: 10. 1016/j. neuron. 2008. 12. 008.
175. Thompson, R. H., Canteras, N. S., and Swanson, L. W. (1996). Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J. Comp. Neurol. 376, 143-173.
176. Thompson, R. H., and Swanson, L. W. (1998). Organization of inputs to the dorsomedial nucleus of the hypothalamus: a reexamination with Fluorogold and PHAL in the rat. Brain Res. Brain Res. Rev. 27, 89-118. doi: 10. 1016/S0165-0173(98)00010-1.
177. Thompson, R. H., and Swanson, L. W. (2003). Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res. Brain Res. Rev. 41, 153-202. doi: 10. 1016/S0165-0173(02)00232-1.
178. Thompson, R. H., and Swanson, L. W. (2010). Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc. Natl. Acad. Sci. U. S. A. 107, 15235-15239. doi: 10. 1073/pnas. 1009112107.
179. Thomson, A. M., West, D. C., Hahn, J., and Deuchars, J. (1996). Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J. Physiol. 496(Pt 1), 81-102. doi: 10. 1113/jphysiol. 1996. sp021667.
180. Toth, M., Fuzesi, T., Halasz, J., Tulogdi, A., and Haller, J. (2010). Neural inputs of the hypothalamic "aggression area" in the rat. Behav. Brain Res. 215, 7-20. doi: 10. 1016/j. bbr. 2010. 05. 050.
181. Trojanowski, J. Q., Gonatas, J. O., and Gonatas, N. K. (1981). Conjugates of horseradish peroxidase (HRP) with cholera toxin and wheat germ agglutinin are superior to free HRP as orthogradely transported markers. Brain Res. 223, 381-385. doi: 10. 1016/0006-8993(81)91151-3.
182. Tweedle, C. D., Smithson, K. G., and Hatton, G. I. (1989). Neurosecretory endings in the rat neurohypophysis are en passant. Exp. Neurol. 106, 20-26. doi: 10. 1016/0014-4886(89)90140-4.
183. Veening, J. G., and Coolen, L. M. (1998). Neural activation following sexual behavior in the male and female rat brain. Behav. Brain Res. 92, 181-193. doi: 10. 1016/S0166-4328(97)00190-3.
184. Veening, J. G., and Coolen, L. M. (2014). Neural mechanisms of sexual behavior in the male rat: emphasis on ejaculation-related circuits. Pharmacol. Biochem. Behav. 121, 170-183. doi: 10. 1016/j. pbb. 2013. 12. 017.
185. Veening, J. G., Swanson, L. W., Cowan, W. M., Nieuwenhuys, R., and Geeraedts, L. M. (1982). The medial forebrain bundle of the rat. II. An autoradiographic study of the topography of the major descending and ascending components. J. Comp. Neurol. 206, 82-108. doi: 10. 1002/cne. 902060107.
186. Veronneau-Longueville, F., Rampin, O., Freund-Mercier, M. J., Tang, Y., Calas, A., Marson, L., et al. (1999). Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat. Neuroscience 93, 1437-1447. doi: 10. 1016/S0306-4522(99)00262-6.
187. Wang, M. E., Fraize, N. P., Yin, L., Yuan, R. K., Petsagourakis, D., Wann, E. G., et al. (2013). Differential roles of the dorsal and ventral hippocampus in predator odor contextual fear conditioning. Hippocampus 23, 451-466. doi: 10. 1002/hipo. 22105.
188. Watts, A. G., and Sanchez-Watts, G. (2007). Rapid and preferential activation of Fos protein in hypocretin/orexin neurons following the reversal of dehydration-anorexia. J. Comp. Neurol. 502, 768-782. doi: 10. 1002/cne. 21316.
189. Weiland, N. G., Orikasa, C., Hayashi, S., and McEwen, B. S. (1997). Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J. Comp. Neurol. 388, 603-612.
190. Wiegand, S. J., and Terasawa, E. (1982). Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 34, 395-404. doi: 10. 1159/000123335.
191. Witkin, J. W., Paden, C. M., and Silverman, A. J. (1982). The luteinizing hormone-releasing hormone (LHRH) systems in the rat brain. Neuroendocrinology 35, 429-438. doi: 10. 1159/000123419.
192. Witter, M. P. (2006). Connections of the subiculum of the rat: topography in relation to columnar and laminar organization. Behav. Brain Res. 174, 251-264. doi: 10. 1016/j. bbr. 2006. 06. 022.
193. Woolley, C. S., Weiland, N. G., McEwen, B. S., and Schwartzkroin, P. A. (1997). Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci. 17, 1848-1859.
194. Wotjak, C. T., Kubota, M., Liebsch, G., Montkowski, A., Holsboer, F., Neumann, I., et al. (1996). Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: a novel mechanism of regulating adrenocorticotropic hormone secretion? J. Neurosci. 16, 7725-7732.
195. Wouterlood, F. G., and Groenewegen, H. J. (1985). Neuroanatomical tracing by use of Phaseolus vulgaris-leucoagglutinin (PHA-L): electron microscopy of PHA-L-filled neuronal somata, dendrites, axons and axon terminals. Brain Res. 326, 188-191. doi: 10. 1016/0006-8993(85)91402-7.
196. Wray, S., and Hoffman, G. (1986). A developmental study of the quantitative distribution of LHRH neurons within the central nervous system of postnatal male and female rats. J. Comp. Neurol. 252, 522-531. doi: 10. 1002/cne. 902520408.
197. Zaborszky, L. S., Wouterlood, F. G., Lanciego, J. L., and Heimer, L. (2006). Neuroanatomical Tract-Tracing 3: Molecules, Neurons, and Systems. New York, NY: Springer.
198. Zahm, D. S., Parsley, K. P., Schwartz, Z. M., and Cheng, A. Y. (2013). On lateral septum-like characteristics of outputs from the accumbal hedonic "hotspot" of Pecina and Berridge with commentary on the transitional nature of basal forebrain "boundaries". J. Comp. Neurol. 521, 50-68. doi: 10. 1002/cne. 23157.
199. Zhang, L., and Hernandez, V. S. (2013). Synaptic innervation to rat hippocampus by vasopressin-immuno-positive fibres from the hypothalamic supraoptic and paraventricular nuclei. Neuroscience 228, 139-162. doi: 10. 1016/j. neuroscience. 2012. 10. 010.
200. Ziegler, D. R., Cullinan, W. E., and Herman, J. P. (2002). Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J. Comp. Neurol. 448, 217-229. doi: 10. 1002/cne. 10257.
201. Zingg, B., Hintiryan, H., Gou, L., Song, M. Y., Bay, M., Bienkowski, M. S., et al. (2014). Neural networks of the mouse neocortex. Cell 156, 1096-1111. doi: 10. 1016/j. cell. 2014. 02. 023.