Postnatal developmental trajectories of neural circuits in the primate prefrontal cortex: Identifying sensitive periods for vulnerability to schizophrenia

Schizophrenia Bulletin

Volumn 37, Issue 3, 2011, Pages 493-503

  Hoftman, Gil D ^a,b   Lewis, David A ^b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c NONE   (United States)

Author keywords

cannabinoid; cholecystokinin; GABA; parvalbumin; pyramidal; working memory

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR;

ARTICLE; BRAIN CORTEX; ENVIRONMENTAL EXPOSURE; HUMAN; MACACA; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PREFRONTAL CORTEX; PRIMATE; PRIORITY JOURNAL; RISK ASSESSMENT; SCHIZOPHRENIA;

ADOLESCENT; ADOLESCENT DEVELOPMENT; AGE OF ONSET; ANIMALS; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HUMANS; MACACA; NEURAL PATHWAYS; PREFRONTAL CORTEX; RISK FACTORS; SCHIZOPHRENIA;

EID: 79955438333     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbr029     Document Type: Article

References (99)

1. Lewis DA, Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 2002;25:409-432. (Pubitemid 34748023)
2. Keefe RS, Fenton WS. How should DSM-V criteria for schizophrenia include cognitive impairment? Schizophr Bull. 2007;33:912-920. (Pubitemid 47216649)
3. Barch DM, Smith E. The cognitive neuroscience of working memory: relevance to CNTRICS and schizophrenia. Biol Psychiatry. 2008;64:11-17.
4. Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167-202. (Pubitemid 32695227)
5. Luna B, Padmanabhan A, O'Hearn K. What has fMRI told us about the development of cognitive control through adolescence? Brain Cogn. 2010;72:101-113.
6. Cannon TD, Glahn DC, Kim J, et al. Dorsolateral prefrontal cortex activity during maintenance and manipulation of information in working memory in patients with schizophrenia. Arch Gen Psychiatry. 2005;62:1071-1080. (Pubitemid 41396932)
7. Cannon TD, van Erp TGM, Huttunen M, et al. Regional gray matter, white matter, and cerebrospinal fluid distributions in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry. 1998;55:1084-1091. (Pubitemid 28558280)
8. Giedd JN, Rapoport JL. Structural MRI of pediatric brain development: what have we learned and where are we going? Neuron. 2010;67:728-734.
9. Cannon M, Jones PB, Murray RM. Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatry. 2002;159:1080-1092. (Pubitemid 34743246)
10. van Os J, Kenis G, Rutten BP. The environment and schizophrenia. Nature. 2010;468:203-212.
11. Goldman-Rakic PS. Development of cortical circuitry and cognitive function. Child Dev. 1987;58:601-622.
12. Alexander GE, Goldman PS. Functional development of the dorsolateral prefrontal cortex: an analysis utilizing reversible cryogenic depression. Brain Res. 1978;143:233-249. (Pubitemid 8277907)
13. Alexander GE. Functional development of frontal association cortex in monkeys: behavioural and electrophysiological studies. Neurosci Res Program Bull. 1982;20:471-479. (Pubitemid 12045853)
14. Funahashi S, Bruce CJ, Goldman-Rakic PS. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol. 1989;61:331-349. (Pubitemid 19063448)
15. White EL. Cortical Circuits. Synaptic Organization of the Cerebral Cortex. Structure, Function and Theory. Boston, MA: Birkḧuser; 1989.
16. Akbarian S, Kim JJ, Potkin SG, et al. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry. 1995;52:258-266.
17. Thune JJ, Uylings HBM, Pakkenberg B. No deficit in total number of neurons in the prefrontal cortex in schizophrenics. J Psychiatr Res. 2001;35:15-21. (Pubitemid 32233166)
18. Selemon LD, Rajkowska G, Goldman-Rakic PS. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J Comp Neurol. 1998;392:402-412. (Pubitemid 28165894)
19. Glantz LA, Lewis DA. Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia: regional and diagnostic specificity. Arch Gen Psychiatry. 1997;54:943-952. (Pubitemid 128719705)
20. Karson CN, Mrak RE, Schluterman KO, et al. Alterations in synaptic proteins and their encoding mRNAs in prefrontal cortex in schizophenia: a possible neurochemical basis for 'hypofrontality'. Mol Psychiatry. 1999;4:39-45. (Pubitemid 29050199)
21. Garey LJ, Ong WY, Patel TS, et al. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry. 1998;65:446-453. (Pubitemid 28438871)
22. Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57:65-73. (Pubitemid 30035660)
23. Kolluri N, Sun Z, Sampson AR, Lewis DA. Lamina-specific reductions in dendritic spine density in the prefrontal cortex of subjects with schizophrenia. Am J Psychiatry. 2005;162:1200-1202. (Pubitemid 40770705)
24. Rajkowska G, Selemon LD, Goldman-Rakic PS. Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch of Gen Psychiatry. 1998;55:215-224.
25. Pierri JN, Volk CLE, Auh S, Sampson A, Lewis DA. Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry. 2001;58:466-473. (Pubitemid 32411327)
26. Sweet RA, Pierri JN, Auh S, Sampson AR, Lewis DA. Reduced pyramidal cell somal volume in auditory association cortex of subjects with schizophrenia. Neuropsychopharmacology. 2003;28:599-609.
27. Arnold SE, Franz BR, Gur RC, et al. Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am J Psychiatry. 1995; 152:738-748.
28. SweetRA, Bergen SE, Sun Z, et al. Pyramidal cell size reduction in schizophrenia: evidence for involvement of auditory feedforward circuits. Biol Psychiatry. 2004;55:1128-1137. (Pubitemid 38739446)
29. Lewis DA, Gonzalez-Burgos G. Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacol Rev. 2008;33:141-165. (Pubitemid 350191315)
30. Anderson SA, Classey JD, Condé F, Lund JS, Lewis DA. Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience. 1995;67:7-22.
31. Arellano JI, Espinosa A, Fairen A, Yuste R, DeFelipe J. Non-synaptic dendritic spines in neocortex. Neuroscience. 2007;145:464-469. (Pubitemid 46341650)
32. Bourgeois JP, Goldman-Rakic PS, Rakic P. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex. 1994;4:78-96. (Pubitemid 24066074)
33. Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997;387:167-178. (Pubitemid 27430343)
34. Mirnics K, Middleton FA, Lewis DA, Levitt P. Analysis of complex brain disorders with gene expression microarrays: schizophrenia as a disease of the synapse. Trends Neurosci. 2001;24:479-486. (Pubitemid 32695360)
35. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol. 2002;64:355-405. (Pubitemid 34259234)
36. Schneggenburger R, Sakaba T, Neher E. Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci. 2002;25:206-212. (Pubitemid 34615538)
37. Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA. Maturation of cognitive processes from late childhood to adulthood. Child Dev. 2004;75:1357-1372. (Pubitemid 39442885)
38. van Leijenhorst L, Crone EA, van der Molen MW. Developmental trends for object and spatial working memory: a psychophysiological analysis. Child Dev. 2007;78:987-1000.
39. Gonzalez-Burgos G, Kroener S, Zaitsev AV, et al. Functional maturation of excitatory synapses in layer 3 pyramidal neurons during postnatal development of the primate prefrontal cortex. Cereb Cortex. 2008;18:626-637. (Pubitemid 351264233)
40. Woo TU, Pucak ML, Kye CH, Matus CV, Lewis DA. Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex. Neuroscience. 1997;80: 1149-1158. (Pubitemid 27359799)
41. Gonzalez-Burgos G, Hashimoto T, Lewis DA. Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr Psychiatry Rep. 2010;12:335-344.
42. Guidotti A, Auta J, Davis JM, et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder. Arch Gen Psychiatry. 2000;57:1061-1069.
43. Hashimoto T, Arion D, Unger T, et al. Alterations in GABArelated transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry. 2008;13:147-161.
44. Hashimoto T, Bazmi HH, Mirnics K, et al. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry. 2008;165:479-489. (Pubitemid 351694291)
45. Ascoli GA, Alonso-Nanclares L, Anderson SA, et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nature Rev Neurosci. 2008; 9:557-568. (Pubitemid 351873463)
46. Eggan SM, Lewis DA. Immunocytochemical distribution of the cannabinoid CB1 receptor in the primate neocortex: a regional and laminar analysis. Cereb Cortex. 2007;17: 175-191. (Pubitemid 44973906)
47. Eggan SM, Melchitzky DS, Sesack SR, Fish KN, Lewis DA. Relationship of cannabinoid CB1 receptor and cholecystokinin immunoreactivity in monkey dorsolateral prefrontal cortex. Neuroscience. 2010;169:1651-1661.
48. Eggan SM, Hashimoto T, Lewis DA. Reduced cortical cannabinoid 1 receptor messenger RNA and protein expression in schizophrenia. Arch Gen Psychiatry. 2008;65:772-784. (Pubitemid 351957703)
49. Eggan SM, Stoyak SR, Verrico CD, Lewis DA. Cannabinoid CB1 receptor immunoreactivity in the prefrontal cortex: comparison of schizophrenia and major depressive disorder. Neuropsychopharmacology. 2010;35:2060-2071.
50. Williams SM, Goldman-Rakic PS, Leranth C. The synaptology of parvalbumin-immunoreactive neurons in primate prefrontal cortex. J Comp Neurol. 1992;320:353-369.
51. Woo TU, Miller JL, Lewis DA. Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry. 1997;154:1013-1015. (Pubitemid 27274547)
52. Hashimoto T, Volk DW, Eggan SM, et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci. 2003;23: 6315-6326. (Pubitemid 36875633)
53. Woo TU, Whitehead RE, Melchitzky DS, Lewis DA. A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci U S A. 1998;95:5341-5346. (Pubitemid 28208599)
54. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P. Differential synaptic localization of two major c-aminobutyric acid type A receptor a subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA. 1996;93:11939-11944. (Pubitemid 26347227)
55. Volk DW, Pierri JN, Fritschy JM, et al. Reciprocal alterations in pre- and postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. Cereb Cortex. 2002;12:1063-1070.
56. Cruz DA, Weaver CL, Lovallo EM, Melchitzky DS, Lewis DA. Selective alterations in postsynaptic markers of chandelier cell inputs to cortical pyramidal neurons in subjects with schizophrenia. Neuropsychopharmacology. 2009;34:2112-2124.
57. Lewis DA, Cruz DA,Melchitzky DS, Pierri JN. Lamina-specific deficits in parvalbumin-immunoreactive varicosities in the prefrontal cortex of subjects with schizophrenia: evidence for fewer projections from the thalamus. Am J Psychiatry. 2001;158:1411-1422. (Pubitemid 32847239)
58. BeneytoM, Abbott A, Hashimoto T, Lewis DA. Lamina-specific alterations in cortical GABAA receptor subunit expression in schizophrenia. Cereb Cortex. September 15, 2010; doi: 10.1093/ cercor/bhq169.
59. Freund TF, Katona I, Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev. 2003;83:1017-1066. (Pubitemid 36828930)
60. Katona I, Freund TF. Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med. 2008;14:923-930.
61. Oeth KM, Lewis DA. Postnatal development of the cholecystokinin innervation of monkey prefrontal cortex. J Comp Neurol. 1993;336:400-418. (Pubitemid 23294119)
62. Eggan SM, Mizoguchi Y, Stoyak SR, Lewis DA. Development of cannabinoid 1 receptor protein and messenger RNA in monkey dorsolateral prefrontal cortex. Cereb Cortex. 2010;20:1164-1174.
63. Erickson SL, Lewis DA. Postnatal development of parvalbumin- and GABA transporter-immunoreactive axon terminals in monkey prefrontal cortex. J Comp Neurol. 2002;448: 186-202. (Pubitemid 34538767)
64. Lund JS, Lewis DA. Local circuit neurons of developing and mature macaque prefrontal cortex: golgi and immunocytochemical characteristics. J Comp Neurol. 1993;328: 282-312. (Pubitemid 23057965)
65. Cruz DA, Eggan SM, Lewis DA. Postnatal development of pre- and post-synaptic GABA markers at chandelier cell inputs to pyramidal neurons in monkey prefrontal cortex. J Comp Neurol. 2003;465:385-400. (Pubitemid 37174203)
66. Loup F, Weinmann O, Yonekawa Y, et al. A highly sensitive immunofluorescence procedure for analyzing the subcellular distribution of GABAA receptor subunits in the human brain. J Histochem Cytochem. 1998;46:1129-1139. (Pubitemid 28445287)
67. Lavoie AM, Tingey JJ, Harrison NL, Pritchett DB, Twyman RE. Activation and deactivation rates of recombinant GABAA receptor channels are dependent on a-subunit isoform. Biophysical J. 1997;73:2518-2526. (Pubitemid 27471460)
68. Tretter V, Jacob TC, Mukherjee J, et al. The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. J Neurosci. 2008;28:1356-1365. (Pubitemid 351231519)
69. Cruz DA, Lovallo EM, Stockton S, Rasband M, Lewis DA. Postnatal development of synaptic structure proteins in pyramidal neuron axon initial segments in monkey prefrontal cortex. J Comp Neurol. 2009;514:353-367.
70. Susuki K, Rasband MN. Spectrin and ankyrin-based cytoskeletons at polarized domains in myelinated axons. Exp Biol Med (Maywood). 2008;233:394-400. (Pubitemid 351469294)
71. Giedd JN, Blumenthal J, Jeffries NO, et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nature Neurosci. 1999;2:861-863. (Pubitemid 30602596)
72. Vreugdenhil M, Jefferys JG, Celio MR, Schwaller B. Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J Neurophysiol. 2003;89:1414-1422. (Pubitemid 36323988)
73. Mager S, Naeve J, Quick M, et al. Steady states, charge movements, and rates for a cloned GABA transporter expressed in xenopus oocytes. Neuron. 1993;10:177-188. (Pubitemid 23079540)
74. Collin T, Chat M, Lucas MG, et al. Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J Neurosci. 2005;25:96-107. (Pubitemid 40110770)
75. Muller M, Felmy F, Schwaller B, Schneggenburger R. Parvalbumin is a mobile presynaptic Ca2+ buffer in the calyx of held that accelerates the decay of Ca2+ and short-term facilitation. J Neurosci. 2007;27:2261-2271. (Pubitemid 46340950)
76. Overstreet LS, Westbrook GL. Synapse density regulates independence at unitary inhibitory synapses. J Neurosci. 2003;23:2618-2626. (Pubitemid 36418596)
77. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci. 2002;3:728-739. (Pubitemid 135706678)
78. Stein V, Nicol RA. GABA generates excitement. Neuron. 2003;37:375-378. (Pubitemid 36183360)
79. Szabadics J, Varga C, Molnar G, et al. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science. 2006;311:233-235. (Pubitemid 43108189)
80. Khirug S, Yamada J, Afzalov R, et al. GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J Neurosci. 2008;28:4635-4639.
81. Molnar G, Olah S, Komlosi G, et al. Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biology. 2008;6:e222.
82. Glickfeld LL, Roberts JD, Somogyi P, Scanziani M. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nature Neurosci. 2009;12:21-23.
83. Woodruff A, Xu Q, Anderson SA, Yuste R. Depolarizing effect of neocortical chandelier neurons. Front Neural Circuits. 2009;3:15.
84. Arion D, Lewis DA. Altered expression of regulators of the cortical chloride transporters NKCC1 and KCC2 in schizophrenia. Arch Gen Psychiatry. 2011;68:21-31.
85. Fillman SG, Duncan CE, Webster MJ, Elashoff M, Weickert CS. Developmental co-regulation of the beta and gamma GABAA receptor subunits with distinct alpha subunits in the human dorsolateral prefrontal cortex. Int J Dev Neurosci. 2010;28:513-519.
86. Duncan CE, Webster MJ, Rothmond DA, et al. Prefrontal GABA(A) receptor alpha-subunit expression in normal postnatal human development and schizophrenia. J Psychiatr Res. 2010;44:673-681.
87. Hashimoto T, Nguyen QL, Rotaru D, et al. Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biol Psychiatry. 2009;65:1015-1023.
88. Maldonado-Aviles JG, Curley AA, Hashimoto T, et al. Altered markers of tonic inhibition in the dorsolateral prefrontal cortex of subjects with schizophrenia. Am J Psychiatry. 2009;166:450-459.
89. Howard MW, Rizzuto DS, Caplan JB, et al. Gamma oscillations correlate with working memory load in humans. Cereb Cortex. 2003;13:1369-1374. (Pubitemid 37466784)
90. Klausberger T, Roberts JD, Somogyi P. Cell type- and inputspecific differences in the number and subtypes of synaptic GABAA receptors in the hippocampus. J Neurosci. 2002;22: 2513-2521. (Pubitemid 37465800)
91. Uhlhaas PJ, Roux F, Singer W, et al. The development of neural synchrony reflects late maturation and restructuring of functional networks in humans. Proc Natl Acad Sci U S A. 2009;106:9866-9871.
92. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci. 2005;6:215-229. (Pubitemid 40342416)
93. Saxena NC, Macdonald RL. Assembly of GABAA receptor subunits: role of the delta subunit. J Neurosci. 1994;14(11 Pt 2):7077-7086.
94. Sun C, Sieghart W, Kapur J. Distribution of alpha1, alpha4, gamma2, and delta subunits of GABAA receptors in hippocampal granule cells. Brain Res. 2004;1029:207-216. (Pubitemid 39470177)
95. Moore TH, Zammit S, Lingford-Hughes A, et al. Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet. 2007;370: 319-328. (Pubitemid 47094993)
96. Bodor AL, Katona I, Nyiri G, et al. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci. 2005;25:6845-6856. (Pubitemid 41023152)
97. Karson MA, Tang AH, Milner TA, Alger BE. Synaptic cross talk between perisomatic-targeting interneuron classes expressing cholecystokinin and parvalbumin in hippocampus. J Neurosci. 2009;29:4140-4154.
98. Crone EA, Wendelken C, Donohue S, van Leijenhorst L, Bunge SA. Neurocognitive development of the ability to manipulate information in working memory. Proc Natl Acad Sci U S A. 2006;103:9315-9320. (Pubitemid 43904341)
99. Insel TR. Rethinking schizophrenia. Nature. 2010;468:187-193.