Afferent projections to nucleus reuniens of the thalamus

Journal of Comparative Neurology

Volumn 480, Issue 2, 2004, Pages 115-142

  McKenna, James Timothy ^a,b   Vertes, Robert P ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Amygdala; Hippocampus; Hypothalamus; Prefrontal cortex; Theta rhythm

Indexed keywords

FLUOROGOLD;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN COMMISSURE; BRAIN CORTEX; CLAUSTRUM; CONTROLLED STUDY; HIPPOCAMPUS; HYPOTHALAMUS NUCLEUS; INSULA; LATERAL GENICULATE NUCLEUS; MALE; NONHUMAN; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PREOPTIC NUCLEUS; PRETECTUM; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT; REUNIENS NUCLEUS; SUBICULUM; SUBSTANTIA INNOMINATA; SUPERIOR COLLICULUS; THALAMUS; THALAMUS MIDLINE NUCLEUS; ZONA INCERTA;

AFFERENT PATHWAYS; ANIMALS; HIPPOCAMPUS; MALE; MIDLINE THALAMIC NUCLEI; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY;

EID: 8844233460     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20342     Document Type: Article

References (167)

1. Aggleton JP, Mishkin M. 1984. Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56-68.
2. Amaral DG, Witter MP. 1995. Hippocampal formation. In Paxinos G, editor. The rat nervous system. San Diego: Academic Press, p 443-493.
3. Arluison M, Derer P. 1993. Forebrain connections of the rat paraventricular thalamic nucleus as demonstrated using the carbocyanide dye DiI. Neurobiology 1: 337-350.
4. Bernard JF, Dallel R, Raboisson P, Villanueva L, Le Bars D. 1995. Organization of the efferent projections from the spinal cervical enlargement to the parabrachial area and periaqueductal gray: a PHA-L study in the rat. J Comp Neurol 353: 480-505.
5. Bertram EH, Zhang DX. 1999. Thalamic excitation of hippocampal CA1 neurons: a comparison with the effects of CA3 stimulation. Neuroscience 92: 15-26.
6. Bester H, Matsumoto N, Besson JM, Bernard JF. 1997. Further evidence for the involvement of the spinoparabrachial pathway in nociceptive processes: a c-Fos study in the rat. J Comp Neurol 383: 439-458.
7. Bester H, Bourgeais L, Villanueva L, Besson JM, Bernard JF. 1999. Differential projections to the intralaminar and gustatory thalamus from the parabrachial area: a PHA-L study in the rat. J Comp Neurol 405: 421-449.
8. Bland BH. 2000. The medial septum: Node of the ascending brainstem hippocampal synchronizing pathways. In: Numan R, editor. The behavioral neuroscience of the septal region. New York: Springer-Verlag. p 115-145.
9. Bland BH, Konopacki J, Kirk IJ, Oddie SD, Dickson CT. 1995. Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethan-anesthetized rat. J Neurophysiol 74: 322-333.
10. Bokor H, Csaki A, Kocsis K, Kiss J. 2002. Cellular architecture of the nucleus reuniens thalami and its putative aspartatergic/glutamatergic projection to the hippocampus and medial septum in the rat. Eur J Neurosci 16: 1227-1239.
11. Broersen LM, Heinsbroek RP, de Bruin JP, Uylings HB, Olivier B. 1995. The role of the medial prefrontal cortex of rats in short-term memory functioning: further support for involvement of cholinergic, rather than dopaminergic mechanisms. Brain Res 674: 221-229.
12. Brog JS, Salyapongse A, Deutch AY, Zahm DS. 1993. The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338:255-278.
13. Buchanan SL, Thompson RH, Maxwell BL, Powell DA. 1994. Efferent connections of the medial prefrontal cortex in the rabbit. Exp Brain Res 100:469-483.
14. Buckner RL, Kelley WM, Petersen SE. 1999. Frontal cortex contributes to human memory formation. Nat Neurosci 2:311-314.
15. Canteras NS, Goto M. 1999. Connections of the precommissural nucleus. J Comp Neurol 408:23-45.
16. Canteras NS, Swanson LW. 1992a. 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.
17. Canteras NS, Swanson LW. 1992b. The dorsal premammillary nucleus: an unusual component of the mammillary body. Proc Natl Acad Sci U S A 89:10089-10093.
18. Canteras NS, Simerly RB, Swanson LW. 1992. Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143-179.
19. 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.
20. 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.
21. Canteras NS, Chiavegatto S, Valle LE, Swanson LW. 1997. Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res Bull 44:297-305.
22. Canteras NS, Ribeiro-Barbosa ER, Comoli E. 2001. Tracing from the dorsal premammillary nucleus prosencephalic systems involved in the organization of innate fear responses. Neurosci Biobehav Rev 25:661-668.
23. Carr DB, Sesack SR. 1996. Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopamine terminals. J Comp Neurol 369:1-15.
24. Cavada C, Llamas A, Reinoso-Suarez F. 1983. Allocortical afferent connections of the prefrontal cortex in the cat. Brain Res 260:117-120.
25. Cechetto DF, Standaert DG, Saper CB. 1985. Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat. J Comp Neurol 240:153-160.
26. Chafee MV, Goldman-Rakic PS. 1998. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol 79:2919-2940.
27. Chiba T, Murata Y. 1985. Afferent and efferent connections of the medial preoptic area in the rat: a WGA-HRP study. Brain Res Bull 14:261-272.
28. Comoli E, Ribeiro-Barbosa ER, Canteras NS. 2000. Afferent connections of the dorsal premammillary nucleus. J Comp Neurol 423:83-98.
29. Conde F, Maire-Lepoivre E, Audinat E, Crepel F. 1995. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J Comp Neurol 352:567-593.
30. Conrad LC, Pfaff DW. 1976a. Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area. J Comp Neurol 169:185-219.
31. Conrad LC, Pfaff DW. 1976b. Efferents from medial basal forebrain and hypothalamus in the rat. II. An autoradiographic study of the anterior hypothalamus. J Comp Neurol 169:221-261.
32. Cornwall J, Cooper JD, Phillipson OT. 1990. Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat. Brain Res Bull 25:271-284.
33. Cullinan WE, Zaborszky L. 1991. Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J Comp Neurol 306:631-667.
34. Dean P, Redgrave P. 1992. Behavioural consequences of manipulating GABA neurotransmission in the superior colliculus. Prog Brain Res 90:263-281.
35. Dean P, Redgrave P, Sahibzada N, Tsuji K. 1986. Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19:367-380.
36. Delatour B, Gisquet-Verrier P. 1996. Prelimbic cortex specific lesions disrupt delayed-variable response tasks in the rat. Behav Neurosci 110: 1282-1298.
37. Delatour B, Gisquet-Verrier P. 1999. Lesions of the prelimbic-infralimbic cortices in rats do not disrupt response selection processes but induce delay-dependent deficits: evidence for a role in working memory? Behav Neurosci 113:941-955.
38. Desbois C, Villanueva L. 2001. The organization of lateral ventromedial thalamic connections in the rat: a link for the distribution of nociceptive signals to widespread cortical regions. Neuroscience 102:885-898.
39. Dolleman-Van der Weel MJ, Lopes da Silva FH, Witter MP. 1997. Nucleus reuniens thalami modulates activity in hippocampal field CA1 through excitatory and inhibitory mechanisms. J Neurosci 17:5640-5650.
40. Erro E, Lanciego JL, Gimenez-Amaya JM. 1999. Relationships between thalamostriatal neurons and pedunculopontine projections to the thalamus: a neuroanatomical tract-tracing study in the rat. Exp Brain Res 127:162-170.
41. Ferino F, Thierry AM, Glowinski J. 1987. Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat. Exp Brain Res 65:421-426.
42. Finn PD, De Vries GJ, Yahr P. 1993. Efferent projections of the sexually dimorphic area of the gerbil hypothalamus: anterograde identification and retrograde verification in males and females. J Comp Neurol 338:491-520.
43. Fulwiler CE, Saper CB. 1984. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319:229-259.
44. Funahashi S, Bruce CJ, Goldman-Rakic PS. 1989. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331-349.
45. Funahashi S, Bruce CJ, Goldman-Rakic PS. 1993. Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas." J Neurosci 13:1479-1497.
46. Fuster JM. 1989. The prefrontal cortex anatomy, physiology, and neuropsychology of the frontal lobe, 2nd ed. New York: Raven Press.
47. Goldman PS, Rosvold HE. 1970. Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. Exp Neurol 27:291-304.
48. Goldman-Rakic PS. 1987. Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Mountcastle VB, Plum F, Geiger SR, editors. Handbook of physiology: 1. The nervous system, vol V. Higher functions of the brain. Bethesda, MD: American Physiological Society. p 373-417.
49. Goldman-Rakic PS. 1994. The issue of memory in the study of prefrontal function. In: Thierry AM, Glowinsky J, Goldman-Rakic PS, Christen Y, editors. Motor and cognitive functions of the prefrontal cortex. Berlin: Springer-Verlag. p 112-123.
50. Goldman-Rakic PS. 1995. Cellular basis of working memory. Neuron 14: 477-485.
51. Goldman-Rakic PS, Selemon LD, Schwartz ML. 1984. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12:719-743.
52. 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.
53. Goto M, Swanson LW, Canteras NS. 2001. Connections of the nucleus incertus. J Comp Neurol 438:86-122.
54. Granon S, Vidal C, Thinus-Blanc C, Changeux JP, Poucet B. 1994. Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. Behav Neurosci 108:883-891.
55. Groenewegen HJ, Vermeulen-Van der Zee E, te Kortschot A, Witter MP. 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.
56. Grove EA. 1988. Efferent connections of the substantia innominata in the rat. J Comp Neurol 277:347-364.
57. Harrison LM, Mair RG. 1996. A comparison of the effects of frontal cortical and thalamic lesions on measures of spatial learning and memory in the rat. Behav Brain Res 75:195-206.
58. Herkenham M. 1978. The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J Comp Neurol 177:589-610.
59. Herkenham M. 1979. The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J Comp Neurol 183:487-517.
60. Hurley KM, Herbert H, Moga MM, Saper CB. 1991. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249-276.
61. Hylden JL, Anton F, Nahin RL. 1989. Spinal lamina I projection neurons in the rat: collateral innervation of parabrachial area and thalamus. Neuroscience 28:27-37.
62. Irle E, Markowitsch HJ. 1982. Connections of the hippocampal formation, mamillary bodies, anterior thalamus and cingulate cortex. A retrograde study using horseradish peroxidase in the cat. Exp Brain Res 47:79-94.
63. Ishikawa A, Nakamura S. 2003. Convergence and interaction of hippocampal and amygdalar projections within the prefrontal cortex in the rat. J Neurosci 23:9987-9995.
64. Jasmin L, Granato A, Ohara PT. 2004. Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J Comp Neurol 468:425-440.
65. Jay TM, Witter MP. 1991. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313:574-586.
66. Jay TM, Glowinski J, Thierry AM. 1989. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 505:337-340.
67. Jeljeli M, Strazielle C, Caston J, Lalonde R. 2003. Effects of ventrolateral-ventromedial thalamic lesions on motor coordination and spatial orientation in rats. Neurosci Res 47:309-316.
68. Kanemaru H, Nakamura H, Isayama H, Kawabuchi M, Tashiro N. 2000. Efferent connections of the anterior hypothalamic nucleus: a biocytin study in the cat. Brain Res Bull 51:219-232.
69. Kesner RP, Hunt ME, Williams JM, Long JM. 1996. Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb Cortex 6:311-318.
70. Kha HT, Finkelstein DI, Tomas D, Drago J, Pow DV, Horne MK. 2001. Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: single axon reconstructions and immunohistochemical study. J Comp Neurol 440:20-30.
71. Kilpatrick IC, Collingridge GL, Starr MS. 1982. Evidence for the participation of nigrotectal gamma-aminobutyrate-containing neurones in striatal and nigral-derived circling in the rat. Neuroscience 7:207-222.
72. Kirk IJ, Mackay JC. 2003. The role of theta-range oscillations in synchronising and integrating activity in distributed mnemonic networks. Cortex 39:993-1008.
73. Kirk IJ, McNaughton N. 1991. Supramammillary cell firing and hippocampal rhythmical slow activity. Neuroreport 2:723-725.
74. Kocsis B, Vertes RP. 1994. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci 14:7040-7052.
75. Kojima S, Goldman-Rakic PS. 1982. Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response. Brain Res 248:43-49.
76. Kolb B. 1990. Animal models for human PFC-related disorders. Prog Brain Res 85:501-519.
77. Krayniak PF, Weiner S, Siegel A. 1980. An analysis of the efferent connections of the septal area in the cat. Brain Res 189:15-29.
78. Krout KE, Loewy AD. 2000a. Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 424:111-141.
79. Krout KE, Loewy AD. 2000b. Parabrachial nucleus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 428:475-494.
80. Krout KE, Loewy AD, Westby GW, Redgrave P. 2001. Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 431:198-216.
81. Krout KE, Belzer RE, Loewy AD. 2002. Brainstem projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 448:53-101.
82. Leranth C, Vertes RP. 2000. Neuronal networks that control the septal pacemaker system: Synaptic interconnections between the septal complex, hippocampus, supramammillary area, and median raphe. In: Numan R, editor. The behavioral neuroscience of the septal region. New York: Springer-Verlag. p 15-47.
83. Masino T, Knudsen EI. 1992. Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl. Exp Brain Res 92:194-208.
84. Materi LM, Kirk IJ, Oddie SD, Sainsbury RS, Bland BH. 1995. The influence of the thalamic nucleus reuniens on hippocampal theta and sharp-wave field activity in the urethane-anesthetized rat. Soc Neurosci Abstr 21:1205.
85. Meibach RC, Siegel A. 1977. Efferent connections of the septal area in the rat: an analysis utilizing retrograde and anterograde transport methods. Brain Res 119:1-20.
86. Miller EK, Erickson CA, Desimone R. 1996. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16: 5154-5167.
87. Mishkin M, Manning FJ. 1978. Non-spatial memory after selective prefrontal lesions in monkeys. Brain Res 143:313-323.
88. Mitchell IJ, Dean P, Redgrave P. 1988. The projection from superior colliculus to cuneiform area in the rat. II. Defence-like responses to stimulation with glutamate in cuneiform nucleus and surrounding structures. Exp Brain Res 72:626-639.
89. Moga MM, Weis RP, Moore RY. 1995. Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221-238.
90. Moore RY, Weis R, Moga MM. 2000. Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420:398-418.
91. Morin LP, Blanchard JH. 1999. Forebrain connections of the hamster intergeniculate leaflet: comparison with those of ventral lateral geniculate nucleus and retina. Vis Neurosci 16:1037-1054.
92. Morin LP, Meyer-Bernstein EL. 1999. The ascending serotonergic system in the hamster: comparison with projections of the dorsal and median raphe nuclei. Neuroscience 91:81-105.
93. Morin LP, Blanchard J, Moore RY. 1992. Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the golden hamster. Vis Neurosci 8:219-230.
94. Mufson EJ, Mesulam MM. 1984. Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus. J Comp Neurol 227:109-120.
95. Naber PA, Witter MP. 1998. Subicular efferents are organized mostly as parallel projections: a double-labeling, retrograde-tracing study in the rat. J Comp Neurol 393:284-297.
96. Niki H. 1974. Prefrontal unit activity during delayed alternation in the monkey. I. Relation to direction of response. Brain Res 68:185-196.
97. Northmore DP, Levine ES, Schneider GE. 1988. Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595-605.
98. Ohtake T, Yamada H. 1989. Efferent connections of the nucleus reuniens and the rhomboid nucleus in the rat: an anterograde PHA-L tracing study. Neurosci Res 6:556-568.
99. Olucha-Bordonau FE, Teruel V, Barcia-Gonzalez J, Ruiz-Torner A, Valverde-Navarro AA, Martinez-Soriano F. 2003. Cytoarchitecture and efferent projections of the nucleus incertus of the rat. J Comp Neurol 464:62-97.
100. Passingham R. 1975. Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta). Brain Res 92:89-102.
101. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates, 2nd ed. New York: Academic Press.
102. Petrides M. 1995. Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey. J Neurosci 15:359-375.
103. Petrides M. 1998. Specialized systems for the processing of mnemonic information within the primate frontal cortex. In: Roberts AC, Robbins TW, Weiskrantz L, editors. The prefrontal cortex: executive and cognitive functions. New York: Oxford University Press, p 103-116.
104. Petrides M. 2000. Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory. J Neurosci 20:7496-7503.
105. 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.
106. Porter MC, Mair RG. 1997. The effects of frontal cortical lesions on remembering depend on the procedural demands of tasks performed in the radial arm maze. Behav Brain Res 87:115-125.
107. Price JL. 1995. Thalamus. In: Paxinos G, editor. The rat nervous system, 2nd ed. New York: Academic Press, p 629-648.
108. Price JL, Amaral DG. 1981. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242-1259.
109. Quintana J, Yajeya J, Fuster JM. 1988. Prefrontal representation of stimulus attributes during delay tasks. I. Unit activity in cross-temporal integration of sensory and sensory-motor information. Brain Res 474:211-221.
110. Redgrave P, Simkins M, McHaffie JG, Stein BE. 1996. Nociceptive neurones in rat superior colliculus. II. Effects of lesions to the contralateral descending output pathway on nocifensive behaviours. Exp Brain Res 109:197-208.
111. Redgrave P, Prescott TJ, Gurney K. 1999. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009-1023.
112. Reep RL, Corwin JV. 1999. Topographic organization of the striatal and thalamic connections of rat medial agranular cortex. Brain Res 841: 43-52.
113. Reep RL, Corwin JV, King V. 1996. Neuronal connections of orbital cortex in rats: topography of cortical and thalamic afferents. Exp Brain Res 111:215-232.
114. Ricardo JA. 1981. Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Res 214:43-60.
115. Risold PY, Swanson LW. 1995. Evidence for a hypothalamothalamocortical circuit mediating pheromonal influences on eye and head movements. Proc Natl Acad Sci U S A 92:3898-3902.
116. Risold PY, Swanson LW. 1997. Connections of the rat lateral septal complex. Brain Res Rev 24:115-195.
117. 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.
118. Risold PY, Thompson RH, Swanson LW. 1997. The structural organization of connections between hypothalamus and cerebral cortex. Brain Res Rev 24:197-254.
119. Romo R, Brody CD, Hernandez A, Lemus L. 1999. Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399:470-473.
120. Room P, Russchen FT, Groenewegen HJ, Lohman AH. 1985. Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat. J Comp Neurol 242:40-55.
121. Ruggiero DA, Anwar S, Kim J, Glickstein SB. 1998. Visceral afferent pathways to the thalamus and olfactory tubercle: behavioral implications. Brain Res 799:159-171.
122. Sahibzada N, Dean P, Redgrave P. 1986. Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci 6:723-733.
123. Sakai ST, Grofova I, Bruce K. 1998. Nigrothalamic projections and nigrothalamocortical pathway to the medial agranular cortex in the rat: single- and double-labeling light and electron microscopic studies. J Comp Neurol 391:506-525.
124. Saper CB, Loewy AD. 1980. Efferent connections of the parabrachial nucleus in the rat. Brain Res 197:291-317.
125. Saper CB, Swanson LW, Cowan WM. 1978. The efferent connections of the anterior hypothalamic area of the rat, cat and monkey. J Comp Neurol 182:575-599.
126. Sawaguchi T, Yamane I. 1999. Properties of delay-period neuronal activity in the monkey dorsolateral prefrontal cortex during a spatial delayed matching-to-sample task. J Neurophysiol 82:2070-2080.
127. Seamans JK, Floresco SB, Phillips AG. 1995. Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063-1073.
128. Sesack SR, Deutch AY, Roth RH, Bunney BS. 1989. 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 290:213-242.
129. Shaw C, Aggleton JP. 1993. The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behav Brain Res 54:91-102.
130. Shehab S, Simkins M, Dean P, Redgrave P. 1995. The dorsal midbrain anticonvulsant zone - III. Effects of efferent pathway transections on suppression of electroshock seizures and defence-like reactions produced by local injections of bicuculline. Neuroscience 65:697-708.
131. Shen CL, Anderson CH. 1980. Efferents from the medial anterior hypothalamic area in the guinea pig. Brain Res Bull 5:693-701.
132. Simerly RB, Swanson LW. 1988. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 270:209-242.
133. Staiger JF, Nurnberger F. 1991. The efferent connections of the lateral septal nucleus in the guinea pig: projections to the diencephalon and brainstem. Cell Tissue Res 264:391-413.
134. Swanson LW. 1976. An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol 167:227-256.
135. Swanson LW. 1981. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res 217:150-154.
136. Swanson LW. 1998. Brain maps: structure of the rat brain. New York: Elsevier.
137. Takagishi M, Chiba T. 1991. Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res 566:26-39.
138. Thompson RH, Swanson LW. 1998. Organization of inputs to the dorsomedial nucleus of the hypothalamus: a reexamination with Fluorogold and PHAL in the rat. Brain Res Rev 27:89-118.
139. Van der Werf YD, Witter MP, Groenewegen HJ. 2002. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39:107-140.
140. van Groen T, Wyss JM. 1990a. Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 300:593-606.
141. van Groen T, Wyss JM. 1990b. The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227-243.
142. van Groen T, Wyss JM. 1992. Connections of the retrosplenial dysgranular cortex in the rat. J Comp Neurol 315:200-216.
143. van Groen T, Wyss JM. 2003. Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:249-263.
144. Vertes RP. 1991. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643-668.
145. Vertes RP. 1992. PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neurol 326:595-622.
146. Vertes RP. 2002. Analysis of projections from the medial prefrontal cortex to the thalamus in the rat, with emphasis on nucleus reuniens. J Comp Neurol 442:163-187.
147. Vertes RP. 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
148. Vertes RP, Kocsis B. 1997. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
149. Vertes RP, Martin GF. 1988. Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J Comp Neurol 275:511-541.
150. 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.
151. Vertes RP, Fortin WJ, Crane AM. 1999. Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555-582.
152. Vertes RP, Hoover WB, Sherman A. 2002. Afferent projections to the medial prefrontal cortex in rats. Soc Neurosci Abstr, Online Program No. 282.2.
153. Vertes RP, McKenna JT, do Valle A, Sherman A, Hoover WB. 2003. Efferent projections of ventral midline nuclei of the thalamus. Soc Neurosci Abstr, Online Program No. 921.5.
154. Viana Di Prisco G, Vertes RP. 2003. Midline thalamic input to the medial prefrontal cortex. Soc Neurosci Abstr, Online Program No. 89.9.
155. Wagner CK, Eaton MJ, Moore KE, Lookingland KJ. 1995. Efferent projections from the region of the medial zona incerta containing A13 dopaminergic neurons: a PHA-L anterograde tract-tracing study in the rat. Brain Res 677:229-237.
156. Watanabe K, Kawana E. 1982. The cells of origin of the incertofugal projections to the tectum, thalamus, tegmentum and spinal cord in the rat: a study using the autoradiographic and horseradish peroxidase methods. Neuroscience 7:2389-2406.
157. Witter MP. 1986. A survey of the anatomy of the hippocampal formation, with emphasis on the septotemporal organization of its intrinsic and extrinsic connections. In: Schwarcz R, Ben-Ari Y, editors. Excitatory amino acids and epilepsy. Advances in experimental and medical biology, vol 203. New York: Plenum Press, p 67-82.
158. Witter MP, Groenewegen HJ. 1990. The subiculum: cytoarchitectonically a simple structure, but hodologically complex. Prog Brain Res 83:47-58.
159. Witter MP, Ostendorf RH, Groenewegen HJ. 1990. Heterogeneity in the dorsal subiculum of the rat. Distinct neuronal zones project to different cortical and subcortical targets. Eur J Neurosci 2:718-725.
160. Wouterlood FG. 1991. Innervation of entorhinal principal cells by neurons of the nucleus reuniens thalami. Anterograde PHA-L tracing combined with retrograde fluorescent tracing and intracellular injection with lucifer yellow in the rat. Eur J Neurosci 3:641-647.
161. Wouterlood FG, Saldana E, Witter MP. 1990. Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 296:179-203.
162. Yasui Y, Breder CD, Saper CB, Cechetto DF. 1991. Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol 303:355-374.
163. Yeomans JS, Tehovnik EJ. 1988. Turning responses evoked by stimulation of visuomotor pathways. Brain Res 472:235-259.
164. Yoshida A, Dostrovsky JO, Chiang CY. 1992. The afferent and efferent connections of the nucleus submedius in the rat. J Comp Neurol 324:115-133.
165. Young HL, Stevens AA, Converse E, Mair RG. 1996. A comparison of temporal decay in place memory tasks in rats (Rattus norvegicus) with lesions affecting thalamus, frontal cortex, or the hippocampal system. Behav Neurosci 110:1244-1260.
166. Zhang DX, Bertram EH. 2002. Midline thalamic region: widespread excitatory input to the entorhinal cortex and amygdala. J Neurosci 22: 3277-3284.
167. Zhang X, Hannesson DK, Saucier DM, Wallace AE, Howland J, Corcoran ME. 2001. Susceptibility to kindling and neuronal connections of the anterior claustrum. J Neurosci 21:3674-3687.