Circuit-Based Corticostriatal Homologies Between Rat and Primate

Biological Psychiatry

Volumn 80, Issue 7, 2016, Pages 509-521

  Heilbronner, Sarah R ^a   Rodriguez Romaguera, Jose ^b   Quirk, Gregory J ^b   Groenewegen, Henk J ^c   Haber, Suzanne N ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cingulate; Homology; Infralimbic; Orbitofrontal; Prefrontal; Prelimbic

Indexed keywords

ADULT; AMYGDALA; ANTERIOR CINGULATE; ARTICLE; CORPUS STRIATUM; DORSAL STRIATUM; EMOTION; HAPLORHINI; INFRALIMBIC CORTEX; MACACA; NONHUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; RAT; SURFACE AREA; VENTRAL STRIATUM; ANATOMY AND HISTOLOGY; ANIMAL; CINGULATE GYRUS; COMPARATIVE STUDY; MALE; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; SPECIES DIFFERENCE;

AMYGDALA; ANIMALS; CORPUS STRIATUM; GYRUS CINGULI; MACACA; MALE; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RATS; SPECIES SPECIFICITY;

EID: 84979619768     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2016.05.012     Document Type: Article

References (81)

1. 1 Mayberg, H.S., Brannan, S.K., Mahurin, R.K., Jerabek, P.A., Brickman, J.S., Tekell, J.L., et al. Cingulate function in depression: a potential predictor of treatment response. Neuroreport 8 (1997), 1057–1061.
2. 2 Milad, M.R., Quirk, G.J., Fear extinction as a model for translational neuroscience: Ten years of progress. Annu Rev Psychol 63 (2012), 129–151.
3. 3 Volkow, N.D., Wang, G.J., Fowler, J.S., Tomasi, D., Telang, F., Addiction: Beyond dopamine reward circuitry. Proc Natl Acad Sci U S A 108 (2011), 15037–15042.
4. 4 Haber, S.N., Heilbronner, S.R., Translational research in OCD: Circuitry and mechanisms. Neuropsychopharmacology 38 (2013), 252–253.
5. 5 Petrides, M., Pandya, D.N., Comparative architectonic analysis of the human and macaque frontal cortex. Boller, F., Grafman, J., (eds.) Handbook of Neuropsychology., 1994, Elsevier, Amsterdam, 17–58.
6. 6 Sallet, J., Mars, R.B., Noonan, M.P., Neubert, F.X., Jbabdi, S., O'Reilly, J.X., et al. The organization of dorsal frontal cortex in humans and macaques. J Neurosci 33 (2013), 12255–12274.
7. 7 Ongur, D., Price, J.L., The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10 (2000), 206–219.
8. 8 Seamans, J.K., Lapish, C.C., Durstewitz, D., Comparing the prefrontal cortex of rats and primates: Insights from electrophysiology. Neurotox Res 14 (2008), 249–262.
9. 9 Kesner, R., Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology 28 (2000), 219–228.
10. 10 Wise, S.P., Forward frontal fields: phylogeny and fundamental function. Trends Neurosci 31 (2008), 599–608.
11. 11 Price, J.L., Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121 (2007), 54–71.
12. 12 Preuss, T.M., Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J Cogn Neurosci 7 (1995), 1–24.
13. 13 Schoenbaum, G., Roesch, M.R., Stalnaker, T.A., Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci 29 (2006), 116–124.
14. 14 Kelley, A.E., Functional specificity of ventral striatal compartments in appetitive behaviors. Ann N Y Acad Sci 877 (1999), 71–90.
15. 15 Corbit, L.H., Muir, J.L., Balleine, B.W., The role of the nucleus accumbens in instrumental conditioning: Evidence of a functional dissociation between accumbens core and shell. J Neurosci 21 (2001), 3251–3260.
16. 16 Voorn, P., Gerfen, C.R., Groenewegen, H.J., Compartmental organization of the ventral striatum of the rat: Immunohistochemical distribution of enkephalin, substance P, dopamine, and calcium-binding protein. J Comp Neurol 289 (1989), 189–201.
17. 17 Meredith, G.E., Pattiselanno, A., Groenewegen, H.J., Haber, S.N., Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin-D28k. J Comp Neurol 365 (1996), 628–639.
18. 18 Everitt, B.J., Cador, M., Robbins, T.W., Interactions between the amygdala and ventral striatum in stimulus-reward associations: Studies using a second-order schedule of sexual reinforcement. Neuroscience 30 (1989), 63–75.
19. 19 McDonald, A.J., Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44 (1991), 15–33.
20. 20 Friedman, D.P., Aggleton, J.P., Saunders, R.C., Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: Combined anterograde and retrograde tracing study in the Macaque brain. J Comp Neurol 450 (2002), 345–365.
21. 21 Squire, L.R., Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99 (1992), 195–231.
22. 22 Insausti, R., Comparative anatomy of the entorhinal cortex and hippocampus in mammals. Hippocampus 3 (1993), 19–26.
23. 23 Goto, Y., Grace, A.A., Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci 31 (2008), 552–558.
24. 24 Phelps, E.A., LeDoux, J.E., Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron 48 (2005), 175–187.
25. 25 Phelps, E.A., Human emotion and memory: Interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14 (2004), 198–202.
26. 26 Zaborszky, L., Alheid, G.F., Beinfeld, M.C., Eiden, L.E., Heimer, L., Palkovits, M., Cholecystokinin innervation of the ventral striatum: A morphological and radioimmunological study. Neuroscience 14 (1985), 427–453.
27. 27 Heimer, L., Zahm, D.S., Churchill, L., Kalivas, P.W., Wohltmann, C., Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41 (1991), 89–125.
28. 28 Krettek, J.E., Price, J.L., Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178 (1978), 225–254.
29. 29 Wright, C.I., Beijer, A.V.J., Groenewegen, H.J., Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci 16 (1996), 1877–1893.
30. 30 Kelley, A.E., Domesick, V.B., The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: An anterograde- and retrograde-horseradish peroxidase study. Neuroscience 7 (1982), 2321–2335.
31. 31 Groenewegen, H.J., Vermeulen-Van der Zee, E., Te Kortschot, A., Witter, M.P., 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 (1987), 103–120.
32. 32 Haber, S.N., McFarland, N.R., The concept of the ventral striatum in nonhuman primates. Ann N Y Acad Sci 877 (1999), 33–48.
33. 33 Averbeck, B.B., Lehman, J., Jacobson, M., Haber, S.N., Estimates of projection overlap and zones of convergence within frontal-striatal circuits. J Neurosci 34 (2014), 9497–9505.
34. 34 Calzavara, R., Mailly, P., Haber, S.N., Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: An anatomical substrate for cognition to action. Eur J Neurosci 26 (2007), 2005–2024.
35. 35 Haber, S.N., Kim, K.S., Mailly, P., Calzavara, R., Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26 (2006), 8368–8376.
36. 36 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 (2013), 5718–5727.
37. 37 Yeterian, E.H., Van Hoesen, G.W., Cortico-striate projections in the rhesus monkey: The organization of certain cortico-caudate connections. Brain Res 139 (1978), 43–63.
38. 38 Berendse, H.W., Galis-de Graaf, Y., Groenewegen, H.J., Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316 (1992), 314–347.
39. 39 Schilman, E.A., Uylings, H.B., Galis-de Graaf, Y., Joel, D., Groenewegen, H.J., The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci Lett 432 (2008), 40–45.
40. 40 Mailly, P., Haber, S.N., Groenewegen, H.J., Deniau, J.M., A 3D multi-modal and multi-dimensional digital brain model as a framework for data sharing. J Neurosci Methods 194 (2010), 56–63.
41. 41 Kremer, J.R., Mastronarde, D.N., McIntosh, J.R., Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116 (1996), 71–76.
42. 42 Jongen-Relo, A.L., Docter, G.J., Jonker, A.J., Vreugdenhil, E., Groenewegen, H.J., Voorn, P., Differential effects of dopamine depletion on the binding and mRNA levels of dopamine receptors in the shell and core of the rat nucleus accumbens. Brain Res Mol Brain Res 25 (1994), 333–343.
43. 43 Fudge, J.L., Haber, S.N., Bed nucleus of the stria terminalis and extended amygdala inputs to dopamine subpopulations in primates. Neuroscience 104 (2001), 807–827.
44. 44 Zahm, D.S., Brog, J.S., On the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience 50 (1992), 751–767.
45. 45 Brown, P., Molliver, M.E., Dual serotonin (5-HT) projections to the nucleus accumbens core and shell: Relation of the 5-HT transporter to amphetamine-induced neurotoxicity. J Neurosci 20 (2000), 1952–1963.
46. 46 Paxinos, G., Watson, C., The Rat Brain in Stereotactic Coordinates. 1986, Academic, New York.
47. 47 Quirk, G.J., Beer, J.S., Prefrontal involvement in the regulation of emotion: Convergence of rat and human studies. Curr Opin Neurobiol 16 (2006), 723–727.
48. 48 Passingham, R.E., Wise, S.P., The Neurobiology of the Prefrontal Cortex: Anatomy, Evolution, and the Origin of Insight (No. 50). 2012, Oxford University Press, Oxford.
49. 49 Uylings, H.B., van Eden, C.G., Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog Brain Res 85 (1990), 31–62.
50. 50 Granon, S., Poucet, B., Involvement of the rat prefrontal cortex in cognitive functions: A central role for the prelimbic area. Psychobiology 28 (2000), 229–237.
51. 51 Milad, M.R., Quirk, G.J., Pitman, R.K., Orr, S.P., Fischl, B., Rauch, S.L., A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry 62 (2007), 1191–1194.
52. 52 Mayberg, H.S., Liotti, M., Brannan, S.K., McGinnis, S., Mahurin, R.K., Jerabek, P.A., et al. Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. Am J Psychiatry 156 (1999), 675–682.
53. 53 Koenigs, M., Grafman, J., The functional neuroanatomy of depression: Distinct roles for ventromedial and dorsolateral prefrontal cortex. Behav Brain Res 201 (2009), 239–243.
54. 54 Goudriaan, A.E., De Ruiter, M.B., Van Den Brink, W., Oosterlaan, J., Veltman, D.J., Brain activation patterns associated with cue reactivity and craving in abstinent problem gamblers, heavy smokers and healthy controls: An fMRI study. Addict Biol 15 (2010), 491–503.
55. 55 Seo, D., Lacadie, C.M., Tuit, K., Hong, K.I., Constable, R.T., Sinha, R., Disrupted ventromedial prefrontal function, alcohol craving, and subsequent relapse risk. JAMA Psychiatry 70 (2013), 727–739.
56. 56 Nakao, T., Nakagawa, A., Yoshiura, T., Nakatani, E., Nabeyama, M., Yoshizato, C., et al. Brain activation of patients with obsessive-compulsive disorder during neuropsychological and symptom provocation tasks before and after symptom improvement: A functional magnetic resonance imaging study. Biol Psychiatry 57 (2005), 901–910.
57. 57 Goldstein, R.Z., Volkow, N.D., Dysfunction of the prefrontal cortex in addiction: Neuroimaging findings and clinical implications. Nat Rev Neurosci 12 (2011), 652–669.
58. 58 Pitman, R.K., Rasmusson, A.M., Koenen, K.C., Shin, L.M., Orr, S.P., Gilbertson, M.W., et al. Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 13 (2012), 769–787.
59. 59 Harrison, B.J., Soriano-Mas, C., Pujol, J., Ortiz, H., Lopez-Sola, M., Hernandez-Ribas, R., et al. Altered corticostriatal functional connectivity in obsessive-compulsive disorder. Arch Gen Psychiatry 66 (2009), 1189–1200.
60. 60 Ahmari, S.E., Spellman, T., Douglass, N.L., Kheirbek, M.A., Simpson, H.B., Deisseroth, K., et al. Repeated cortico-striatal stimulation generates persistent OCD-like behavior. Science 340 (2013), 1234–1239.
61. 61 Voorn, P., Vanderschuren, L.J., Groenewegen, H.J., Robbins, T.W., Pennartz, C.M., Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27 (2004), 468–474.
62. 62 Belin, D., Everitt, B.J., Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57 (2008), 432–441.
63. 63 Kelley, A.E., Ventral striatal control of appetitive motivation: Role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27 (2004), 765–776.
64. 64 Featherstone, R.E., McDonald, R.J., Dorsal striatum and stimulus-response learning: Lesions of the dorsolateral, but not dorsomedial, striatum impair acquisition of a stimulus-response-based instrumental discrimination task, while sparing conditioned place preference learning. Neuroscience 124 (2004), 23–31.
65. 65 Thorn, C.A., Atallah, H., Howe, M., Graybiel, A.M., Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66 (2010), 781–795.
66. 66 Kim, H.F., Hikosaka, O., Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards. Brain 138 (2015), 1776–1800.
67. 67 Kim, H.F., Hikosaka, O., Distinct basal ganglia circuits controlling behaviors guided by flexible and stable values. Neuron 79 (2013), 1001–1010.
68. 68 Yin, H.H., Ostlund, S.B., Knowlton, B.J., Balleine, B.W., The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22 (2005), 513–523.
69. 69 Porrino, L.J., Lyons, D., Smith, H.R., Daunais, J.B., Nader, M.A., Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J Neurosci 24 (2004), 3554–3562.
70. 70 Yin, H.H., Knowlton, B.J., Balleine, B.W., Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19 (2004), 181–189.
71. 71 Mars, R.B., Jbabdi, S., Sallet, J., O'Reilly, J.X., Croxson, P.L., Olivier, E., et al. Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31 (2011), 4087–4100.
72. 72 Reep, R.L., Cheatwood, J.L., Corwin, J.V., The associative striatum: Organization of cortical projections to the dorsocentral striatum in rats. J Comp Neurol 467 (2003), 271–292.
73. 73 Hurley, K.M., Herbert, H., Moga, M.M., Saper, C.B., Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308 (1991), 249–276.
74. 74 Sesack, S.R., Deutch, A.Y., Roth, R.H., Bunney, B.S., 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 (1989), 213–242.
75. 75 Zeng, D., Stuesse, S.L., Morphological heterogeneity within the cingulate cortex in rat: A horseradish peroxidase transport study. Brain Res 565 (1991), 290–300.
76. 76 Hoover, W.B., Vertes, R.P., Projections of the medial orbital and ventral orbital cortex in the rat. J Comp Neurol 519 (2011), 3766–3801.
77. 77 Vertes, R.P., Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51 (2004), 32–58.
78. 78 Cho, Y.T., Ernst, M., Fudge, J.L., Cortico-amygdala-striatal circuits are organized as hierarchical subsystems through the primate amygdala. J Neurosci 33 (2013), 14017–14030.
79. 79 Chiba, T., Kayahara, T., Nakano, K., Efferent projections of infralimbic and prelimbic areas of the medial prefrontal cortex in the Japanese monkey, Macaca fuscata. Brain Res 888 (2001), 83–101.
80. 80 Ferry, A.T., Ongur, D., An, X., Price, J.L., Prefrontal cortical projections to the striatum in macaque monkeys: Evidence for an organization related to prefrontal networks. J Comp Neurol 425 (2000), 447–470.
81. 81 Paxinos, G., Huang, X.F., Toga, A.W., The Rhesus Monkey in Stereotaxic Coordinates. 2000, Academic Press, San Diego.