A mesoscale connectome of the mouse brain

Nature

Volumn 508, Issue 7495, 2014, Pages 207-214

  Oh, Seung Wook ^a   Harris, Julie A ^a   Ng, Lydia ^a   Winslow, Brent ^a   Cain, Nicholas ^a   Mihalas, Stefan ^a   Wang, Quanxin ^a   Lau, Chris ^a   Kuan, Leonard ^a   Henry, Alex M ^a   Mortrud, Marty T ^a   Ouellette, Benjamin ^a   Nguyen, Thuc Nghi ^a   Sorensen, Staci A ^a   Slaughterbeck, Clifford R ^a   Wakeman, Wayne ^a   Li, Yang ^a   Feng, David ^a   Ho, Anh ^a   Nicholas, Eric ^a   Hirokawa, Karla E ^a   Bohn, Phillip ^a   Joines, Kevin M ^a   Peng, Hanchuan ^a   Hawrylycz, Michael J ^a   Phillips, John W ^a   Hohmann, John G ^a   Wohnoutka, Paul ^a   Gerfen, Charles R ^b   Koch, Christof ^a   Bernard, Amy ^a   Dang, Chinh ^a   Jones, Allan R ^a   Zeng, Hongkui ^a   more..

^a ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CELLS AND CELL COMPONENTS; COGNITION; DISEASE INCIDENCE; GENE EXPRESSION; NERVOUS SYSTEM; PROTEIN; RODENT; THREE-DIMENSIONAL MODELING;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; AUDITORY CORTEX; BRAIN ANALYSIS; BRAIN CORTEX; BRAIN MAPPING; BRAIN REGION; CELL LEVEL; COGNITION; CONNECTOME; CONTROLLED STUDY; CORPUS STRIATUM; FRONTAL CORTEX; GLOBUS PALLIDUS; GRAY MATTER; HIPPOCAMPAL CA1 REGION; IMAGE QUALITY; INJECTION SITE; MALE; MEDULLA OBLONGATA; MESENCEPHALON; MOTOR CORTEX; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NERVE FIBER; NEUROANATOMY; NONHUMAN; PONS; PRIORITY JOURNAL; RETROSPLENIAL CORTEX; SIGNAL DETECTION; SOMATOSENSORY CORTEX; THALAMUS; THALAMUS NUCLEUS; TISSUE STRUCTURE; TRACTOGRAPHY; VISUAL CORTEX; ZONA INCERTA; ANIMAL; BIOLOGICAL MODEL; BOOK; BRAIN; C57BL MOUSE; CYTOLOGY; HISTOLOGY; NEUROANATOMICAL TRACT TRACING; PHYSIOLOGY;

CAENORHABDITIS ELEGANS;

ANIMALS; ATLASES AS TOPIC; AXONS; BRAIN; CEREBRAL CORTEX; CONNECTOME; CORPUS STRIATUM; MALE; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; THALAMUS;

EID: 84898684536     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13186     Document Type: Article

References (127)

1. Swanson, L. W. Brain Architecture: Understanding the Basic Plan 331 (Oxford Univ. Press, 2012).
2. Seung, S. Connectome: How The Brain's Wiring Makes Us Who We Are 359 (Houghton Mifflin Harcourt, 2012).
3. Sporns, O. Networks of the Brain 412 (The MIT Press, 2011).
4. White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous systemof the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1-340 (1986).
5. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1-47 (1991).
6. Bota, M., Dong, H. W.& Swanson, L. W. Combining collation and annotation efforts toward completion of the rat and mouse connectomes in BAMS. Front. Neuroinform. 6, 2 (2012).
7. Chiang, A. S. et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 21, 1-11 (2011).
8. Jenett, A. et al.A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2, 991-1001 (2012).
9. Sporns, O., Tononi, G. & Kotter, R. The human connectome: A structural description of the human brain. PLoS Comput. Biol. 1, e42 (2005).
10. Van Essen, D. C. et al. The WU-Minn Human Connectome Project: an overview. NeuroImage 80, 62-79 (2013).
11. Bock, D. D. et al. Network anatomy andin vivophysiology of visual cortical neurons. Nature 471, 177-182 (2011).
12. Briggman, K. L., Helmstaedter, M. & Denk, W. Wiring specificity in the directionselectivity circuit of the retina. Nature 471, 183-188 (2011).
13. Chklovskii, D. B., Vitaladevuni, S. & Scheffer, L. K. Semi-automated reconstruction of neural circuits using electron microscopy. Curr. Opin. Neurobiol. 20, 667-675 (2010).
14. Helmstaedter, M. et al. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500, 168-174 (2013).
15. Takemura, S. Y. et al. A visual motion detection circuit suggested by Drosophila connectomics. Nature 500, 175-181 (2013).
16. Huang, Z. J. & Zeng, H. Genetic approaches to neural circuits in the mouse. Annu. Rev. Neurosci. 36, 183-215 (2013).
17. Masland, R. H. The neuronal organization of the retina. Neuron 76, 266-280 (2012).
18. Bohland, J. W. et al. A proposal for a coordinated effort for the determination of brainwide neuroanatomical connectivity in model organisms at a mesoscopic scale. PLoS Comput. Biol. 5, e1000334 (2009).
19. Chamberlin, N. L., Du, B., de Lacalle, S. & Saper, C. B. Recombinant adenoassociated virus vector: use for transgene expression and anterograde tract tracing in the CNS. Brain Res. 793, 169-175 (1998).
20. Harris, J. A., Oh, S. W. & Zeng, H. Adeno-associated viral vectors for anterograde axonal tracing with fluorescent proteins in nontransgenic and Cre driver mice. Curr. Protoc. Neurosci. 59, 1.20.1-1.20. 18 http://dx.doi.org/10.1002/0471142301.ns0120s59 (2012).
21. Wang, Q. et al. Systematic comparison of adeno-associated virus and biotinylated dextranamine reveals equivalent sensitivity between tracers and novel projection targets in the mouse brain. J. Comp. Neurol. http://dx.doi.org/10.1002/cne.23567 (Feb 22, 2014).
22. Ragan, T. et al. Serial two-photon tomography for automated ex vivo mouse brain imaging. Nature Methods 9, 255-258 (2012).
23. Dong, H. W. The Allen Reference Atlas: a Digital Color Brain Atlas of the C57BL/6J Male Mouse (John Wiley & Sons, 2008).
24. Markov, N. T. et al. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex 24, 17-36 (2014).
25. Ercsey-Ravasz, M. et al. A predictive network model of cerebral cortical connectivity based on a distance rule. Neuron 80, 184-197 (2013).
26. Wang, Q., Sporns, O. & Burkhalter, A. Network analysis of corticocortical connections reveals ventral anddorsal processingstreamsinmouse visual cortex. J. Neurosci. 32, 4386-4399 (2012).
27. Bullmore, E. & Sporns, O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Rev. Neurosci. 10, 186-198 (2009).
28. Schmitt, O. et al. The intrinsic connectome of the rat amygdala. Front. Neural Circuits 6, 81 (2012).
29. Erdos, P. & Rényi, A. On the evolution of random graphs. Publ. Math. Inst. Hung. Acad. Sci. 5, 17-61 ( (1960).
30. Bollobás, B. Random Graphs (Cambridge Univ. Press, 2001).
31. Watts, D. J. & Strogatz, S. H. Collective dynamics of 'small-world' networks. Nature 393, 440-442 (1998).
32. Barabási, A. L.&Albert, R.Emergence of scaling in randomnetworks. Science 286, 509-512 (1999).
33. Groenewegen, H. J. & Berendse, H. W. The specificity of the 'nonspecific' midline and intralaminar thalamic nuclei. Trends Neurosci. 17, 52-57 (1994).
34. Joel, D. & Weiner, I. The organization of the basal ganglia-thalamocortical circuits: open interconnected rather than closed segregated. Neuroscience 63, 363-379 (1994).
35. Mailly, P., Aliane, V., Groenewegen, H. J., Haber, S. N. & Deniau, J. M. The rat prefrontostriatal system analyzed in 3D: evidence for multiple interacting functional units. J. Neurosci. 33, 5718-5727 (2013).
36. Gerfen, C. R. in The Rat Nervous System (ed. Paxinos, G.) 455-508 (Elsevier Academic Press, 2004).
37. Jones, E. G. The Thalamus (Cambridge Univ. Press, 2007).
38. Jones, E. G. Viewpoint: the core and matrix of thalamic organization. Neuroscience 85, 331-345 (1998).
39. Scannell, J. W., Burns, G. A., Hilgetag, C. C., O'Neil, M. A. & Young, M. P. The connectional organization of the cortico-thalamic systemof the cat. Cereb. Cortex 9, 277-299 (1999).
40. Barbas, H. & Rempel-Clower, N. Cortical structure predicts the pattern of corticocortical connections. Cereb. Cortex 7, 635-646 (1997).
41. Bargmann, C. I. & Marder, E. From the connectome to brain function. Nature Methods 10, 483-490 (2013).
42. Lo, L. & Anderson, D. J. A. Cre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons. Neuron 72, 938-950 (2011).
43. Wall, N. R., Wickersham, I. R., Cetin, A., De La Parra, M. & Callaway, E. M. Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc. Natl Acad. Sci. USA 107, 21848-21853 (2010).
44. Wickersham, I. R. et al. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53, 639-647 (2007).
45. Paxinos, G. & Franklin, K. B. J. The Mouse Brain in Stereotaxic Coordinates (Academic Press, 2001).
46. Dang, C. et al. The Allen Brain Atlas: Delivering Neuroscience to the Web on a Genome Wide Scale. Lecture Notes in Computer Science 4544, 17-26 (2007).
47. Alloway, K. D., Olson, M. L. & Smith, J. B. Contralateral corticothalamic projections fromMI whisker cortex: potential route for modulating hemispheric interactions. J. Comp. Neurol. 510, 100-116 (2008).
48. Aronoff, R. et al. Long-range connectivity of mouse primary somatosensory barrel cortex. Eur. J. Neurosci. 31, 2221-2233 (2010).
49. Azuma, M. & Chiba, T. Afferent projections of the infralimbic cortex (area 25) in rats: a WGA-HRP study. Kaibogaku Zasshi 71, 523-540 (1996).
50. Beckstead, R. M. An autoradiographic examination of corticocortical and subcortical projections of themediodorsal-projection(prefrontal) cortex in the rat. J. Comp. Neurol. 184, 43-62 (1979).
51. Benzinger, H. & Massopust, L. C. Brain stem projections from cortical area 18 in the albino rat. Exp. Brain Res. 50, 1-8 (1983).
52. Berendse, H. W. & Groenewegen, H. J. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42, 73-102 (1991).
53. Bokor, H., Acsady, L. & Deschenes, M. Vibrissal responses of thalamic cells that project to the septal columns of the barrel cortex and to the second somatosensory area. J. Neurosci. 28, 5169-5177 (2008).
54. Burwell, R. D. & Amaral, D. G. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J.Comp.Neurol.391, 293-321 (1998).
55. Cechetto, D. F.& Saper, C. B. Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J. Comp. Neurol. 262, 27-45 (1987).
56. Conte, W.L.,Kamishina, H.,Corwin, J. V.&Reep, R. L.Topography in the projections of lateral posterior thalamus with cingulate and medial agranular cortex in relation to circuitry for directed attention and neglect. Brain Res. 1240, 87-95 (2008).
57. Cornwall, J. & Phillipson, O. T. Afferent projections to the parafascicular thalamic nucleus of the rat, as shown by the retrograde transport of wheat germagglutinin. Brain Res. Bull. 20, 139-150 (1988).
58. Deacon, T. W., Eichenbaum, H., Rosenberg, P. & Eckmann, K. W. Afferent connections of the perirhinal cortex in the rat. J. Comp. Neurol. 220, 168-190 (1983).
59. Desbois, C. & Villanueva, L. 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 (2001).
60. Donaldson, L., Hand, P. J. & Morrison, A. R. Cortical-thalamic relationships in the rat. Exp. Neurol. 47, 448-458 (1975).
61. Féger, J., Bevan, M. & Crossman, A. R. The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: a comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study. Neuroscience 60, 125-132 (1994).
62. Graziano, A., Liu, X. B.,Murray, K. D.&Jones, E. G. Vesicular glutamate transporters define two sets of glutamatergic afferents to thesomatosensory thalamus and two thalamocortical projections in the mouse. J. Comp. Neurol. 507, 1258-1276 (2008).
63. Guldin, W. O. & Markowitsch, H. J. Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat. J. Comp. Neurol. 215, 135-153 (1983).
64. Haque, T. et al. Thalamic afferent and efferent connectivity to cerebral cortical areas with direct projections to identified subgroups of trigeminal premotoneurons in the rat. Brain Res. 1346, 69-82 (2010).
65. Hoogland, P. V., Welker, E. & Van der Loos, H. Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP. Exp. Brain Res. 68, 73-87 (1987).
66. Hoover, W. B. & Vertes, R. P. Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct. 212, 149-179 (2007).
67. Hoover, W. B. & Vertes, R. P. Projections of the medial orbital and ventral orbital cortex in the rat. J. Comp. Neurol. 519, 3766-3801 (2011).
68. Hsu, D. T. & Price, J. L. Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys. J. Comp. Neurol. 504, 89-111 (2007).
69. Hsu, D. T. & Price, J. L. Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J. Comp. Neurol. 512, 825-848 (2009).
70. Hurley, K. M., Herbert, H., Moga, M. M. & Saper, C. B. Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 308, 249-276 (1991).
71. Kaitz, S. S. & Robertson, R. T. Thalamic connections with limbic cortex. II. Corticothalamic projections. J. Comp. Neurol. 195, 527-545 (1981).
72. Kamishina, H. et al. Cortical connections of the rat lateral posterior thalamic nucleus. Brain Res. 1264, 39-56 (2009).
73. Kealy, J. & Commins, S. The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function. Prog. Neurobiol. 93, 522-548 (2011).
74. Killackey, H. P. & Sherman, S. M. Corticothalamic projections fromthe rat primary somatosensory cortex. J. Neurosci. 23, 7381-7384 (2003).
75. Kolmac, C. I., Power, B. D. & Mitrofanis, J. Dorsal thalamic connections of the ventral lateral geniculate nucleus of rats. J. Neurocytol. 29, 31-41 (2000).
76. Krettek, J. E. & Price, J. L. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J. Comp. Neurol. 171, 157-191 (1977).
77. Kuramoto, E. et al. Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb. Cortex 19, 2065-2077 (2009).
78. Li, S.& Kirouac, G. J. Projections fromthe paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J. Comp. Neurol. 506, 263-287 (2008).
79. Li, S. & Kirouac, G. J. Sources of inputs to the anterior and posterior aspects of the paraventricular nucleus of the thalamus. Brain Struct. Funct. 217, 257-273 (2012).
80. Liao, C. C., Chen, R. F., Lai, W. S., Lin, R. C. & Yen, C. T. Distribution of large terminal inputs from the primary and secondary somatosensory cortices to the dorsal thalamus in the rodent. J. Comp. Neurol. 518, 2592-2611 (2010).
81. Linke, R. & Schwegler, H. Convergent and complementary projections of the caudal paralaminar thalamic nuclei to rat temporal and insular cortex. Cereb. Cortex 10, 753-771 (2000).
82. Llano, D. A. & Sherman, S. M. Evidence for nonreciprocal organization of the mouse auditory thalamocortical-corticothalamic projection systems. J. Comp. Neurol. 507, 1209-1227 (2008).
83. Lu, S. M. & Lin, R. C. Thalamic afferents of the rat barrel cortex: a light-and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens. Mot. Res. 10, 1-16 (1993).
84. Mason, R. & Groos, G. A. Cortico-recipient and tecto-recipient visual zones in the rat's lateral posterior (pulvinar) nucleus: an anatomical study. Neurosci. Lett. 25, 107-112 (1981).
85. McIntyre, D. C., Kelly, M. E. & Staines, W. A. Efferent projections of the anterior perirhinal cortex in the rat. J. Comp. Neurol. 369, 302-318 (1996).
86. McKenna, J. T. & Vertes, R. P. Afferent projections to nucleus reuniens of the thalamus. J. Comp. Neurol. 480, 115-142 (2004).
87. Miller, M. W. & Vogt, B. A. Direct connections of rat visual cortex with sensory, motor, and association cortices. J. Comp. Neurol. 226, 184-202 (1984).
88. Mitchell, B. D. & Cauller, L. J. Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats. Brain Res. 921, 68-77 (2001).
89. Monconduit, L., Bourgeais, L., Bernard, J. F., Le Bars, D. & Villanueva, L. Ventromedial thalamic neurons convey nociceptive signals from the whole body surface to the dorsolateral neocortex. J. Neurosci. 19, 9063-9072 (1999).
90. Nakashima, M. et al. An anterograde and retrograde tract-tracing study on the projections from the thalamic gustatory area in the rat: distribution of neurons projecting to the insular cortex and amygdaloid complex. Neurosci. Res. 36, 297-309 (2000).
91. Ohno, S. et al. A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb. Cortex 22, 2840-2857 (2012).
92. Porter, L. L. & White, E. L. Afferent and efferent pathways of the vibrissal region of primary motor cortex in the mouse. J. Comp. Neurol. 214, 279-289 (1983).
93. Reep, R. L., Chandler, H. C., King, V. & Corwin, J. V. Rat posterior parietal cortex: topography of corticocortical and thalamic connections. Exp. Brain Res. 100, 67-84 (1994).
94. Reep, R. L. & Corwin, J. V. Topographic organization of the striatal and thalamic connections of rat medial agranular cortex. Brain Res. 841, 43-52 (1999).
95. Reep, R. L., Corwin, J. V. & King, V. Neuronal connections of orbital cortex in rats: topography of cortical and thalamic afferents. Exp. Brain Res. 111, 215-232 (1996).
96. Reep, R. L. & Winans, S. S. Efferent connections of dorsal and ventral agranular insular cortex in the hamster, Mesocricetus auratus. Neuroscience 7, 2609-2635 (1982).
97. Robertson, R. T. & Kaitz, S. S. Thalamic connections with limbic cortex. I. Thalamocortical projections. J. Comp. Neurol. 195, 501-525 (1981).
98. Roger, M. & Arnault, P. Anatomical study of the connections of the primary auditory area in the rat. J. Comp. Neurol. 287, 339-356 (1989).
99. Samuelsen, C. L., Gardner, M. P. & Fontanini, A. Thalamic contribution to cortical processing of taste and expectation. J. Neurosci. 33, 1815-1827 (2013).
100. Sanderson, K. J., Dreher, B. & Gayer, N. Prosencephalic connections of striate and extrastriate areas of rat visual cortex. Exp. Brain Res. 85, 324-334 (1991).
101. Schobber, W. Efferent and afferent connections of the nucleus lateralis posterior thalami (''pulvinar'') in the albino rats. Z. Mikrosk. Anat. Forsch. 95, 827-844 (1981).
102. Sherman, S. M. Thalamic relays and cortical functioning. Prog. Brain Res. 149, 107-126 (2005).
103. Shi, C. J. & Cassell, M. D. Cortical, thalamic, and amygdaloid projections of rat temporal cortex. J. Comp. Neurol. 382, 153-175 (1997).
104. Shi, C. J. & Cassell, M. D. Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J. Comp. Neurol. 399, 440-468 (1998).
105. Shibata, H. Efferent projections fromthe anterior thalamic nuclei to the cingulate cortex in the rat. J. Comp. Neurol. 330, 533-542 (1993).
106. Shibata, H. & Honda, Y. Thalamocortical projections of the anterodorsal thalamic nucleus in the rabbit. J. Comp. Neurol. 520, 2647-2656 (2012).
107. Shibata, H. & Naito, J. Organization of anterior cingulate and frontal cortical projections to the anterior and laterodorsal thalamic nuclei in the rat. Brain Res. 1059, 93-103 (2005).
108. Shipley, M. T. & Geinisman, Y. Anatomical evidence for convergence of olfactory, gustatory, and visceral afferent pathways inmouse cerebral cortex. Brain Res. Bull. 12, 221-226 (1984).
109. Simmons, P. A., Lemmon, V.&Pearlman, A. L. Afferent and efferent connections of the striate and extrastriate visual cortex of the normal and reeler mouse. J. Comp. Neurol. 211, 295-308 (1982).
110. Takagishi, M. & Chiba, T. Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res. 566, 26-39 (1991).
111. VanderWerf, Y. D., Witter, M. P.&Groenewegen, H. J. The intralaminar andmidline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 39, 107-140 (2002).
112. van Groen, T., Kadish, I. & Wyss, J. M. Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res. Brain Res. Rev. 30, 1-26 (1999).
113. van Groen, T.&Wyss, J. M. Connections of the retrosplenial granular a cortex in the rat. J. Comp. Neurol. 300, 593-606 (1990).
114. Van Groen, T. & Wyss, J. M. Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J. Comp. Neurol. 358, 584-604 (1995).
115. Van Groen, T. & Wyss, J. M. Connections of the retrosplenial granular b cortex in the rat. J. Comp. Neurol. 463, 249-263 (2003).
116. Vaudano, E., Legg, C. R. & Glickstein, M. Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur. J. Neurosci. 3, 317-330 (1991).
117. Vertes, R. P. 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 (2002).
118. Vertes, R. P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51, 32-58 (2004).
119. Vertes, R. P., Hoover, W. B., Do Valle, A. C., Sherman, A. & Rodriguez, J. J. Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J. Comp. Neurol. 499, 768-796 (2006).
120. Vertes, R. P., Hoover, W. B. & Rodriguez, J. J. Projections of the central medial nucleus of the thalamus in the rat: node in cortical, striatal and limbic forebrain circuitry. Neuroscience 219, 120-136 (2012).
121. Vogt, B. A. & Miller, M. W. Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J. Comp. Neurol. 216, 192-210 (1983).
122. Wang, Y. & Kurata, K. Quantitative analyses of thalamic and cortical origins of neurons projecting to the rostral and caudal forelimb motor areas in the cerebral cortex of rats. Brain Res. 781, 137-147 (1998).
123. Welker, E., Hoogland, P. V. & Van der Loos, H. Organization of feedback and feedforward projections of the barrel cortex: a PHA-L study in the mouse. Exp. Brain Res. 73, 411-435 (1988).
124. Wimmer, V. C., Bruno, R. M., de Kock, C. P., Kuner, T. & Sakmann, B. Dimensions of a projection column and architecture of VPM and POm axons in rat vibrissal cortex. Cereb. Cortex 20, 2265-2276 (2010).
125. Wright, N. F., Vann, S. D., Erichsen, J. T., O'Mara, S. M. & Aggleton, J. P. Segregation of parallel inputs to the anteromedial and anteroventral thalamic nuclei of the rat. J. Comp. Neurol. 521, 2966-2986 (2013).
126. Yasui, Y., Itoh, K., Sugimoto, T., Kaneko, T. & Mizuno, N. Thalamocortical and thalamo-amygdaloid projections from the parvicellular division of the posteromedial ventral nucleus in the cat. J. Comp. Neurol. 257, 253-268 (1987).
127. Zhang, Z. W. & Deschenes, M. Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb. Cortex 8, 428-436 (1998).