The non-human primate striatum undergoes marked prolonged remodeling during postnatal development

Frontiers in Cellular Neuroscience

Volumn 8, Issue , 2014, Pages

  Martin, Lee J ^a   Cork, Linda C ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autism; Epigenetics; Infant; Leucine enkephalin; Nucleus accumbens; Rhesus monkey; Striatal mosaic; Striosome

Indexed keywords

CALBINDIN 1; LEUCINE ENKEPHALIN; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE;

ADULT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; BRAIN DEVELOPMENT; BRAIN SIZE; BRAIN WEIGHT; CAUDATE NUCLEUS; CELL STRUCTURE; CORPUS STRIATUM; FEMALE; HISTOLOGY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFANT; INNERVATION; MALE; MATURATION; NEUROANATOMY; NISSL STAINING; NONHUMAN; NUCLEUS ACCUMBENS; ONTOGENY; POSTNATAL DEVELOPMENT; RHESUS MONKEY;

EID: 84907380815     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00294     Document Type: Article

References (102)

1. Al-Abdulla, N. A., Portera-Cailliau, C., and Martin, L. J. (1998). Occipital cortex ablation in adult rat causes retrograde neuronal death in the lateral geniculate nucleus that resembles apoptosis. Neuroscience 86, 191-209. doi: 10.1016/S0306-4522(98)00014-1
2. Alexander, G. E., DeLong, M. R., and Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann. Rev. Neurosci. 9, 357-381. doi: 10.1146/annurev.ne.09.030186.002041
3. Baez-Mendoza, R., and Schultz, W. (2013). The role of the striatum in social behavior. Front. Neurosci. 7:233. doi: 10.3389/fnins,2013.00233
4. Ballough, G. P. H., Martin, L. J., Cann, F. J., Graham, J. S., Smith, C. D., Kling, C. E., et al. (1995). Microtubule-associated protein 2 (MAP-2): a sensitive marker of seizure-related brain damage. J. Neurosci. Methods 61, 23-32. doi: 10.1016/0165-0270(95)00019-Q
5. Bedard, A., Cossette, M., Levesque, M., and Parent, A. (2002). Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci. Lett. 328, 213-216. doi: 10.1016/S0304-3940(02)00530-X
6. Bedard, A., Gravel, C., and Parent, A. (2006). Chemical characterization of newly generated neurons in the striatum of adult primates. Exp. Brain Res. 170, 501-512. doi: 10.1007/s00221-005-0233-5
7. Bogart, S. L., Bennet, A. J., Schapiro, S. J., Reamer, L. A., and Hopkins, W. D. (2014). Different early rearing experiences have long-term effects on cortical organization in captive chimpanzees (Pan troglodytes). Dev. Sci. 17, 161-174. doi: 10.1111/desc.12106
8. Boylan, M. K., Levine, M. S., Buchwald, N. A., and Fisher, R. S. (1990). Patterns of tachykinin expression and localizations in developing feline neostriatum. J. Comp. Neurol. 293, 151-163. doi: 10.1002/cne.902930112
9. Brana, C., Caille, I., Pellevoisin, C., Charron, G., Aubert, I., Caron, M. G., et al. (1996). Ontogeny of the striatal neurons expressing the D1 dopamine receptor in humans. J. Comp. Neurol. 370, 23-34. doi: 10.1002/(SICI)1096-9861(19960617)370:1<23::AID-CNE3>3.0.CO;2-N
10. Brand, S., and Rakic, P. (1979). Genesis of the primate neostriatum: 3H thymidine autoradiographic analysis of the time of neuron origin in the rhesus monkey. Neuroscience 4, 767-778. doi: 10.1016/0306-4522(79)90005-8
11. Brand, S., and Rakic, P. (1980). Neurogenesis of the nucleus accumbens septi and neighboring septal nuclei in the rhesus monkey: a combined 3H thymidine and electron microscopic study. Neuroscience 5, 2125-2138. doi: 10.1016/0306-4522(80)90128-1
12. Brauer, K., Häusser, M., Hartig, W., and Arendt, T. (2000). The core-shell dichotomy of nucleus accumbens in the rhesus monkey as revealed by double-immunofluorescence and morphology of cholinergic interneurons. Brain Res. 858, 151-162. doi: 10.1016/S0006-8993(00)01938-7
13. Calhoun, M. E., Jucker, M., Martin, L. J., Thinakaran, G., Price, D. L., and Mouton, P. R. (1996). Comparative evaluation of synaptophysin-based methods for quantification of synapses. J. Neurocytology 25, 821-828. doi: 10.1007/BF02284844
14. Cimino, M., Zoli, M., and Weiss, B. (1991). Differential ontogenetic expression and regulation of proenkephalin and preprosomatostatin mRNAs in rat caudate-putamen as studied by in situ hybridization histochemistry. Brain Res. Dev. Brain Res. 60, 115-122. doi: 10.1016/0165-3806(91)90039-L
15. Cohen, R. A., Grieve, S., Hoth, K. F., Paul, R. H., Sweet, L., Tate, D., et al. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol. Psychiatry 59, 975-982. doi: 10.1016/j.biopsych.2005.12.016
16. Cote, P. Y., Sadikot, A. F., and Parent, A. (1991). Complementary distribution of calbindin D-28k and parvalbumin in the basal forebrain and midbrain of squirrel monkey. Eur. J. Neurosci. 3, 1316-1329. doi: 10.1111/j.1460-9568.1991.tb00064.x
17. Crittenden, J. R., and Graybiel, A. M. (2011). Basal ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front. Neuroanat. 5:59. doi: 10.3389/fnana.2011.00059
18. Dekaban, A. S. (1978). Changes in brain weight during the span of human life: relation of brain weights to body heights and body weights. Ann. Neurol. 4, 345-356. doi: 10.1002/ana.410040410
19. Desban, M., Gauchy, C., Kemel, M. L., Besson, M. J., and Glowinski, J. (1989). Three-dimensional organization of the striosomal compartment and patchy distribution of striatonigral projections in the matrix of the cat caudate nucleus. Neuroscience 29, 551-566. doi: 10.1016/0306-4522(89)90130-9
20. Duerden, E. G., Card, D., Lax, I. D., Donner, E. J., and Taylor, M. J. (2013). Alterations in frontostriatal pathways in children born very preterm. Dev. Med. Child Neurol. 55, 952-958. doi: 10.1111/dmcn.12198
21. Ernst, A., Alkass, K., Bernard, S., Salehpour, M., Perl, S., Tisdale, J., et al. (2014). Neurogenesis in the striatum of the adult human brain. Cell 156, 1072-1083. doi: 10.1016/j.cell.2014.01.044
22. Faull, R. L. M., Dragunow, M., and Villiger, J. W. (1989). The distribution of neurotensin receptors and acetylcholinesterase in the human caudate nucleus: evidence for the existence of a third neurochemical compartment. Brain Res. 488, 381-386. doi: 10.1016/0006-8993(89)90735-X
23. Fishell, G., and van der Kooy, D. (1987). Pattern formation in the striatum: developmental changes in the distribution of striatonigral neurons. J. Neurosci. 7, 1969-1978.
24. Fishell, G., and van der Kooy, D. (1991). Pattern formation in the striatum: neurons with early projection to the substantia nigra survive the cell death period. J. Comp. Neurol. 312, 33-42. doi: 10.1002/cne.903120104
25. Fotuhi, M., Dawson, T. M., Sharp, A. H., Martin, L. J., Graybiel, A. M., and Snyder, S. H. (1993). Phosphoinositide second messenger system is enriched in striosomes: immunohistochemical demonstration of inositol 1,4,5-trisphosphate receptors and phospholipase C β and γ in primate basal ganglia. J. Neurosci. 13, 3300-3308.
26. Gerfen, C. R. (1984). The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311, 461-464. doi: 10.1038/311461a0
27. Gerfen, C. R. (1985). The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J. Comp. Neurol. 236, 454-476. doi: 10.1002/cne.902360404
28. Gerfen, C. R., and Young, W. S. III. (1988). Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 460, 161-167. doi: 10.1016/0006-8993(88)91217-6
29. Gimenez-Amaya, J.-M., and Graybiel, A. M. (1991). Modular organization of projection neurons in the matrix compartment of the primate striatum. J. Neurosci. 11, 779-791.
30. Goedert, M., Hunt, S. P., Mantyh, P. W., and Emson, P. C. (1985). The ontogenetic development of neurotensin-like immunoreactivity and neurotensin receptors in the cat striatum. Brain Res. 352, 127-131. doi: 10.1016/0165-3806(85)90095-1
31. Goff, B., Gee, D. G., Telzer, E. H., Humphreys, K. L., Gabard-Durnam, L., Flannery, J., et al. (2013). Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience 249, 129-138. doi: 10.1016/j.neuroscience.2012.12.010
32. Goldman-Rakic, P. S. (1981). Prenatal formation of cortical input and development of cytoarchitectonic compartments in the neostriatum of the rhesus monkey. J. Neurosci. 1, 721-735.
33. Goldman-Rakic, P. S. (1982). Cytoarchitectonic heterogeneity of the primate neostriatum: subdivision into island and matrix cellular compartments. J. Comp. Neurol. 205, 398-413. doi: 10.1002/cne.902050408
34. Goto, S., Yamada, K., Ushio, Y., Fukunaga, K., and Miyamoto, E. (1994). Neostriatal mosaic and type II Ca2+/calmodulin-dependent protein kinase: an immunohis-tochemical study on the adult rat striatum. Neurosci. Lett. 173, 177-180. doi: 10.1016/0304-3940(94)90177-5
35. Graybiel, A. M., Pickel, V. M., Joh, T. H., Reis, D. T., and Ragsdale, C. W. Jr. (1981). Direct demonstration of a correspondence between the dopamine islands and acetylcholinesterase patches in the developing striatum. Proc. Natl. Acad. Sci. U.S.A. 78, 5871-5875. doi: 10.1073/pnas.78.9.5871
36. Graybiel, A. M., and Ragsdale, C. W. Jr. (1978). Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylcholinesterase staining. Proc. Natl. Acad. Sci. U.S.A. 75, 5723-5726. doi: 10.1073/pnas.75.11.5723
37. Graybiel, A. M., and Ragsdale, C. W. Jr. (1980). Clumping of acetylcholinesterase activity in the developing striatum of the human fetus and young infant. Proc. Natl. Acad. Sci. U.S.A. 77, 1214-1218. doi: 10.1073/pnas.77.2.1214
38. Graybiel, A. M., and Ragsdale, C. W. Jr. (1983). "Biochemical anatomy of the striatum," in Chemical Neuroanatomy, ed. P. C. Emson (New York: Raven Press), 427-504.
39. Greif, K. F., Tillakaratne, N. J., Erlander, M. G., Feldblum, S., and Tobin, A. J. (1992). Transient increase in expression of a glutamate decarboxylase (GAD) mRNA during the postnatal development of the rat striatum. Dev. Biol. 153, 158-164. doi: 10.1016/0012-1606(92)90100-U
40. Groves, P. M., Martone, M., Young, S. J., and Armstrong, D. M. (1988). Three-dimensional patterns of enkephalin-like immunoreactivity in the caudate nucleus of the cat. J. Neurosci. 8, 892-900.
41. Guennoun, R., and Bloch, B. (1991). D2 dopamine receptor gene expression in the rat striatum during ontogeny: an in situ hybridization study. Brain Res. Dev. Brain Res. 60, 79-89. doi: 10.1016/0165-3806(91)90157-E
42. Haber, S., and Elde, R. (1982). The distribution of enkephalin immunoreactive fibers and terminals in the monkey central nervous system: an immunohistochemical study. Neuroscience 7, 1049-1095. doi: 10.1016/0306-4522(82)91118-6
43. Haber, S. H., Adler, A., and Bergman, H. (2012). "The basal ganglia," in The Human Nervous System, eds J. K. Mai and G. Paxinos (London: Elsevier), 678-738.
44. Haverstick, D. M., Jeziorski, M., and Bannon, M. J. (1990). Developmental profile of striatal preprotachykinin gene expression. J. Neurochem. 55, 764-768. doi: 10.1111/j.1471-4159.1990.tb04557.x
45. Heimer, L., Alheid, G. F., de Olmos, J. S., Groenewegen, H. J., Haber, S. N., Harlan, R. E., et al. (1997). The accumbens: beyond the core-shell dichotomy. J. Neuropsychiatry Clin. Neurosci. 9, 354-381.
46. Heimer, L., and Van Hoesen, G. W. (2006). The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci. Biobehav. Rev. 30, 126-147. doi: 10.1016/j.neubiorev.2005.06.006
47. Holt, D. J., Graybiel, A. M., and Saper, C. B. (1997). Neurochemical architecture of the human striatum. J. Comp. Neurol. 384, 1-25. doi: 10.1002/(SICI)1096-9861(19970721)384:1<1::AID-CNE1>3.0.CO;2-5
48. Humphrey, T. (1968). The development of the human amygdala during embryonic life. J. Comp. Neurol. 132, 135-166. doi: 10.1002/cne.901320108
49. Jakab, R. L., Hazrati, L. N., and Goldman-Rakic, P. (1996). Distribution and neurochemical character of substance P receptor (SPR)-immunoreactive striatal neurons of the macaque monkey: accumulation of SP fibers and SPR neurons and dendrites in "striocapsules" encircling striosomes. J. Comp. Neurol. 369. 137-149. doi: 10.1002/(SICI)1096-9861(19960520)369:1<137::AID-CNE10>3.0.CO;2-O
50. Kent, J. L., Pert, C. B., and Herkenham, M. (1981). Ontogeny of opiate receptors in rat forebrain: visualization by in vitro autoradiography. Brain Res. 254, 487-504. doi: 10.1016/0165-3806(81)90018-3
51. Langen, M., Schnack, H. G., Nederveen, H., Bos, D., Lahuis, B. E., de Jonge M. V., et al. (2009). Changes in the developmental trajectories of striatum in autism. Biol. Psychiartry 66, 327-333. doi: 10.1016/j.biopsych.2009.03.017
52. Letinic, K., and Kostovic, I. (1996). Transient patterns of calbindin-D28k expression in the developing striatum of man. Neurosci. Lett. 220, 211-214. doi: 10.1016/S0304-3940(96)13270-5
53. Levesque, M., and Parent, A. (2005). The striatofugal fiber system in primates: a reevaluation of its organization based on single-axon tracing studies. Proc. Natl. Acad. Sci. U.S.A. 102, 11888-11893. doi: 10.1073/pnas.0502710102
54. Loizou, L. A. (1972). The postnatal ontogeny of monoamine-containing neurons in the central nervous system of the albino rat. Brain Res. 40, 395-418. doi: 10.1016/0006-8993(72)90142-4
55. Lok, J., and Martin, L. J. (2002). Rapid subcellular redistribution of bax precedes caspase-3 and endonuclease activation during excitotoxic neuronal apoptosis. J. Neurotrauma 19, 815-828. doi: 10.1089/08977150260190410
56. Lowenstein, P. R., Slesinger, P. A., Singer, H. S., Walker, L. C., Casanova, M. F., Price, D. L., et al. (1987). An autoradiographic study of the development of 3H hemicholinium-3 binding sites in human and baboon basal ganglia: a marker for the sodium-dependent high affinity choline uptake system. Brain Res. 431, 291-297. doi: 10.1016/0165-3806(87)90216-1
57. Lowenstein, P. R., Slesinger, P. A., Singer, H. S., Walker, L. C., Casanova, M. F., Raskin, L. S., et al. (1989). Compartment-specific changes in the density of cholinergic and dopamine uptake sites and muscarinic and dopaminergic receptors during the development of the baboon striatum: a quantitative receptor autoradiographic study. J. Comp. Neurol. 288, 428-446. doi: 10.1002/cne.902880306
58. Mack, K. J., O’Malley, K. L., and Todd, R. D. (1991). Differential expression of dopaminergic D2 receptor mRNAs during development. Brain Res. Dev. Brain Res. 59, 249-251. doi: 10.1016/0165-3806(91)90105-R
59. Manley, M. S., Young, S. J., and Groves, P. M. (1994). Compartmental organization of the peptide network in the human caudate nucleus. J. Chem. Neuroanat. 7, 191-201. doi: 10.1016/0891-0618(94)90029-9
60. Marchand, R., and Lajoie, L. (1986). Histogenesis of the striatopallidal system in the rat. Neuroscience 17, 573-590. doi: 10.1016/0306-4522(86)90031-X
61. Martin, L. J. (2001). Neuronal cell death in nervous system development, disease, and injury. Intl. J. Mol. Med. 7, 455-478.
62. Martin, L. J., Blackstone, C. D., Huganir, R. L., and Price, D. L. (1993). The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits. J. Neurosci. 13, 782-792.
63. Martin, L. J., Hadfield, M. G., Dellovade, T. L., and Price, D. L. (1991a). The striatal mosaic in primates: patterns of neuropeptide immunoreactivity differentiate the ventral striatum from the dorsal striatum. Neuroscience 43, 397-417. doi: 10.1016/0306-4522(91)90303-6
64. Martin, L. J., Powers, R. E., Dellovade, T. L., and Price, D. L. (1991b). The bed nucleus-amygdala continuum in human and monkey. J. Comp. Neurol. 309, 445-485. doi: 10.1002/cne.903090404
65. Martin, L. J., Spicer, D. M., Lewis, M. H., Gluck, J. P., and Cork, L. C. (1991c). Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: i. Subcortical regions. J. Neurosci. 11, 3344-3358.
66. Martin, L. J., Kaiser, A., and Price, A. C. (1999). Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J. Neurobiol. 40, 185-201. doi: 10.1002/(SICI)1097-4695(199908)40:2<185::AID-NEU5>3.0.CO;2-#
67. McGeer, P. L., McGeer, E. G., Fibiger, H. C., and Wickson, V. (1971). Neostriatal choline acetylase and cholinesterase following selective brain lesions. Brain Res. 35, 308-314. doi: 10.1016/0006-8993(71)90625-1
68. Meredith, G. E., Pattiselanno, A., Groenewegen, H. J., and Haber, S. N. (1996). Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin-D28k. J. Comp. Neurol. 365, 628-639. doi: 10.1002/(SICI)1096-9861(19960219)365:4<628::AID-CNE9>3.0.CO;2-6
69. Mikula, S., Parrish, S. K., Trimmer, J. S., and Jones, E. G. (2009). Complete 3D visualization of primate striosomes by KChIP1 immunostaining. J. Comp. Neurol. 514, 507-517. doi: 10.1002/cne.22051
70. Mouton, P. R., Martin, L. J., Calhoun, M. E., Dal Forno, G., and Price, D. L. (1998). Cognitive decline strongly correlates with cortical atrophy in Alzheimer’s disease. Neurobiol. Aging 19, 371-377. doi: 10.1016/S0197-4580(98)00080-3
71. Mueller, D. M., Shamblott, M. J., Fox, H. E., Gearhart, J. D., and Martin, L. J. (2005). Transplanted human embryonic germ cell-derived neuronal stem cells replace neurons and oligodendrocytes in the forebrain of neonatal mice with excitotoxic brain damage. J. Neurosci. Res. 82, 592-608. doi: 10.1002/jnr.20673
72. Murrin, L. C., and Zeng, W. Y. (1989). Dopamine D1 receptor development in the rat striatum: early localization in striosomes. Brain Res. 480, 170-177. doi: 10.1016/0006-8993(89)91579-5
73. Nastuk, M. A., and Graybiel, A. M. (1985). Patterns of muscarinic cholinergic binding in the striatum and their relation to dopamine islands and striosomes. J. Comp. Neurol. 237, 176-194. doi: 10.1002/cne.902370204
74. Northington, F. J., Ferriero, D. M., Flock, D. L., and Martin, L. J. (2001). Delayed neurodegeneration in neonatal rat thalamus after hypoxia-ischemia is apoptosis. J. Neurosci. 21, 1931-1938.
75. Olson, L., Seiger, A., and Fuxe, K. (1972). Heterogeneity of striatal and limbic dopamine innervations: highly fluorescent islands in developing and adult rats. Brain Res. 44, 283-288. doi: 10.1016/0006-8993(72)90385-X
76. Pauly, M. C., Dobrossy, M. D., Nikkhah, G., Winkler, C., and Piroth, T. (2014). Organization of the human fetal subpallium. Front. Neuroanat. 7:54. doi: 10.3389/fnana.2013.00054
77. Petanjek, Z., Judas, M., Simic, G., Rasin, M. R., Uylings, H. B. M., Rakic, P., et al. (2011). Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 108, 13281-13286. doi: 10.1073/pnas.1105108108
78. Petracca, F. M., Baskin, D. G., Diaz, J., and Dorsa, D. M. (1986). Ontogenetic changes in vasopressin binding site distribution in rat brain. Brain Res. 393, 63-68. doi: 10.1016/0165-3806(86)90065-9
79. Prensa, L., Gimenez-Amya, J. M., and Parent, A. (1999). Chemical hetero- geneity of the striosomal compartment in the human striatum. J. Comp. Neurol. 413, 603-618. doi: 10.1002/(SICI)1096-9861(19991101)413:4<603::AID-CNE9>3.0.CO;2-K
80. Prensa, L., Richard, S., and Parent, A. (2003). Chemical anatomy of the human ventral striatum and adjacent basal forebrain structures. J. Comp. Neurol. 460, 345-367. doi: 10.1002/cne.10627
81. Quirion, R., and Dam, T. V. (1986). Ontogeny of substance P receptor binding sites in rat brain. J. Neurosci. 6, 2187-2199.
82. Robbins, T. W., Jones, G. H., and Wilkinson, L. S. (1996). Behavioural and neurochemical effects of early social deprivation in the rat. J. Psychopharmacol. 20, 39-47. doi: 10.1177/026988119601000107
83. Sajin, B., Sestan, N., and Dmitrovic, B. (1992). Compartmentalization of NADPH-diaphorase staining in the developing human striatum. Neurosci. Lett. 140, 117-120. doi: 10.1016/0304-3940(92)90695-4
84. Sakai, T., Matsui, M., Mikami, A., Malkova, L., Hamada, Y., Tomonaga, M., et al. (2012). Developmental patterns of chimpanzee cerebral tissue provide important clues for understanding the remarkable enlargement of the human brain. Proc. R. Soc. B Biol. Sci. 280, 2012-2398. doi: 10.1098/rspb.2012.2398
85. Selemon, L. D., Gottleib, J. P., and Goldman-Rakic, P. S. (1994). Islands and striosomes in the neostriatum of the rhesus monkey: non-equivalent compartments. Neuroscience 58, 183-192. doi: 10.1016/0306-4522(94)90165-1
86. Shepherd, G. M. G. (2013). Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14, 278-291. doi: 10.1038/nrn3469
87. Shi, J., Wang, Y., Ceschin, R., An, X., Lao, Y., Vanderbilt, D., et al. (2013). A multivariate surface-based analysis of the putamen in premature newborns: regional differences within the ventral striatum. PLoS ONE 8:e66736. doi: 10.1371/journal.pone.0066736
88. Slesinger, P. A., Lowenstein, P. R., Singer, H. S., Walker, L. C., Casanova, M. F., Price, D. L., et al. (1988). Development of beta 1 and beta 2 adrenergic receptors in baboon brain: an autoradiographic study using 125I iodocyanopindolol. J. Comp. Neurol. 273, 318-329. doi: 10.1002/cne.902730304
89. Smith, Y., Wichmann, T., and DeLong, M. R. (2014). Corticostriatal and mesocortical dopamine systems: do species differences matter? Nat. Rev. Neurosci. 15, 63. doi: 10.1038/nrn3469-c1
90. Steindler, D. A., O’Brien, T. F., and Cooper, N. G. (1988). Glycoconjugate boundaries during early postnatal development of the neostriatal mosaic. J. Comp. Neurol. 267, 357-369. doi: 10.1002/cne.902670306
91. Takahashi, K., Liu, F. C., Oishi, T., Mori, T., Higo, N., Hayashi, M., et al. (2008). Expression of FOXP2 in the developing monkey forebrain: comparison with the expression of the genes FOXP1, PBX3, and MEIS2. J. Comp. Neurol. 509, 180-189. doi: 10.1002/cne.21740
92. Tecott, H., Rubenstein, J. L., Paxinos, G., Evans, C. J., Eberwine, J. H., and Valentino, K. L. (1989). Developmental expression of proenkephalin mRNA and peptides in rat striatum. Brain Res. Dev. Brain Res. 49, 75-86. doi: 10.1016/0165-3806(89)90060-6
93. Tennyson, V. M., Barrett, R. E., Cohen, G., Cote, L., Heikkila, R., and Mytilineou, C. (1972). The developing neostriatum of the rabbit: correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and (3H) dopamine uptake. Brain Res. 46, 251-285. doi: 10.1016/0006-8993(72)90019-4
94. Thorsell, A., Slawecki, C. J., El Khoury, A., Mathe, A. A., and Ehlers, C. L. (2006). The effects of social isolation on neuropeptide Y levels, exploratory and anxiety-related behaviors in rat. Pharmacol. Biochem. Behav. 83, 28-34. doi: 10.1016/j.pbb.2005.12.005
95. Tribollet, E., Charpak, S., Schmidt, A., Dubois-Dauphin, M., and Dreifuss, J. J. (1989). Appearance and transient expression of oxytocin receptors in fetal, infant, and peripubertal rat brain studied by autoradiography. J. Neurosci. 9, 1764-1773.
96. Ulfig, N., Neudorfer, F., and Bohl, J. (2001). Development-related expression of AKAP79 in the striatal compartments of the human brain. Cells Tissues Organs 168, 319-329. doi: 10.1159/000047848
97. Ulfig, N., Setzer, M., Neudorfer, F., and Saretzki, U. (2000). Changing distribution patterns of synaptophysin-immunoreactive structures in the human dorsal striatum of the fetal brain. Anat. Rec. 258, 198-209. doi: 10.1002/(SICI)1097-0185(20000201)258:1<198::AID-AR9>3.0.CO;2-L
98. van der Kooy, D. (1984). Developmental relationships between opiate receptors and dopamine in the forebrain of caudate-putamen patches. Brain Res. 316, 300-303. doi: 10.1016/0165-3806(84)90318-3
99. van der Kooy, D., and Fishell, G. (1987). Neuronal birthdate underlies the development of striatal compartments. Brain Res. 401, 155-161. doi: 10.1016/0006-8993(87)91176-0
100. Vicedo, M. (2009). Mothers, machines, and morals: Harry Harlow’s work on primate love from lab to legend. J. Hist. Behav. Sci. 45, 193-218. doi: 10.1002/jhbs.20378
101. Yetnikoff, L., Reichard, R. A., Schwartz, Z. M., Parsely, K. P., and Zahm, D. S. (2014). Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat. J. Comp. Neurol. 522, 1031-1047. doi: 10.1002/cne.23459
102. Zahm, D. S., Eggerman, K. W., Sprung, R. F., Wesche, D. E., and Payne, E. (1990). Postnatal development of striatal neurotensin immunoreactivity in realtion to clusters of substance P immunoreactivive neurons and the "dopamine islands" in the rat. J. Comp. Neurol. 296, 403-414. doi: 10.1002/cne.902960306