Mediodorsal thalamic afferents to layer III of the rat prefrontal cortex: Synaptic relationships to subclasses of interneurons

Journal of Comparative Neurology

Volumn 490, Issue 3, 2005, Pages 220-238

  Rotaru, Diana C ^b   Barrionuevo, German ^b   Sesack, Susan R ^a  

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

^b NONE

Author keywords

Calbindin; Calretinin; GABA; Parvalbumin; Thalamus; Ultrastructure

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; PARVALBUMIN; TRACER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; COGNITION; CONTROLLED STUDY; DENDRITIC SPINE; ELECTRON MICROSCOPY; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD LABELING; INTERNEURON; MALE; NERVE FIBER; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; SENSORY NERVE; SILVER STAINING; SYNAPSE; THALAMUS DORSOMEDIAL NUCLEUS;

AFFERENT PATHWAYS; ANIMALS; CALCIUM-BINDING PROTEINS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICROSCOPY, IMMUNOELECTRON; MODELS, BIOLOGICAL; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; THALAMUS;

EID: 23744499209     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20661     Document Type: Article

References (126)

1. Beierlein M, Connors BW. 2002. Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. J Neurophysiol 88:1924-1932.
2. Beierlein M, Gibson JR, Connors BW. 2003. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000.
3. Bender D. 1983. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res 279:258-261.
4. Bernardo KL, Woolsey TA. 1987, Axonal trajectories between mouse somatosensory thalamus and cortex. J Comp Neurol 258:542-564.
5. Castro-Alamancos MA, Connors BW. 1997. Thalamocortical synapses. Prog Neurobiol 51:581-606.
6. Celio MR. 1986. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231:995-997.
7. Celio MR, Heizmann CW. 1981. Calcium-binding protein parvalbumin as a neuronal marker. Nature 293:300-302.
8. Celio MR, Baier W, Scharer L, de Viragh PA, Gerday C. 1988. Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81-86.
9. Celio MR, Baier W, Scharer L, Gregersen HJ, de Viragh PA, Norman AW. 1990. Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium 11:599-602.
10. Chan J, Aoki C, Pickel V. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33:113-127.
11. Chmielowska J, Stewart MG, Bourne RC. 1988. gamma-Aminobutyric acid (GABA) immunoreactivity in mouse and rat first somatosensory (SI) cortex: description and comparison. Brain Res 439:155-168.
12. Chmielowska J, Carvell GE, Simons DJ. 1989. Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J Comp Neurol 285:325-338.
13. Cobb S, Buhl E, Halasy K, Paulsen O, Somogyi P. 1995. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
14. Conde F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA. 1994. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95-116.
15. Cullen TJ, Walker MA, Parkinson N, Craven R, Crow TJ, Esiri MM, Harrison PJ. 2003. A postmortem study of the mediodorsal nucleus of the thalamus in schizophrenia. Schizophr Res 60:157-166.
16. Daum I, Ackermann H. 1994. Frontal-type memory impairment associated with thalamic damage. Int J Neurosci 77:187-198.
17. DeFelipe J. 1997. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1-19.
18. DeFelipe J, Jones EG. 1992. High-resolution light and electron microscopic immunocytochemistry of colocalized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex, Eur J Neurosci 4:46-60.
19. DeFelipe J, Hendry SH, Hashikawa T, Molinari M, Jones EG. 1990. A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37:655-673.
20. del Rio MR, DeFelipe J. 1995. A light and electron microscopic study of calbindin D-28k immunoreactive double bouquet cells in the human temporal cortex. Brain Res 690:133-140.
21. del Rio MR, DeFelipe J. 1997. Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J Chem Neuroanat 13:243-251.
22. Deschenes M, Veinante P, Zhang ZW. 1998. The organization of corticothalamic projections: reciprocity versus parity. Brain Res Brain Res Rev 28:286-308.
23. Diamond ME, Armstrong-James M, Ebner FF. 1992. Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus. J Comp Neurol 318:462-476.
24. Dorph-Petersen KA, Pierri JN, Sun Z, Sampson AR, Lewis DA. 2004. Stereological analysis of the mediodorsal thalamic nucleus in schizophrenia: volume, neuron number, and cell types. J Comp Neurol 472: 449-462.
25. Erickson SL, Lewis DA. 2004. Cortical connections of the lateral mediodorsal thalamus in cynomolgus monkeys. J Comp Neurol 473:107-127.
26. Eysel UT. 1992. Lateral inhibitory interactions in areas 17 and 18 of the cat visual cortex. Prog Brain Res 90:407-422.
27. Floresco S, Grace A. 2003. Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J Neurosci 23:3930-3943.
28. Floresco S, Braaksma D, Phillips A. 1999. Thalamic-cortical-striatal circuitry subserves working memory during delayed responding on a radial arm maze. J Neurosci 19:11061-11071.
29. Freeman JJ, Cuppernell C, Flannery K, Gabriel M. 1996. Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits. J Neurosci 16:1538-1549.
30. Freund TF, Martin KA, Whitteridge D. 1985. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y-type thalamic afferents. I, Arborization patterns and quantitative distribution of postsynaptic elements. J Comp Neurol 242:263-274.
31. Fuster JM. 1997. The prefrontal cortex: anatomy, physiology, and neuropsychology of the frontal lobe. New York: Raven Press.
32. Gabbott PL, Somogyi P. 1986. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp Brain Res 61:323-331.
33. Gabbott PL, Somogyi J, Stewart MG, Hamori J. 1985. GABA-immunoreactive neurons in the rat dorsal lateral geniculate nucleus: light microscopical observations. Brain Res 346:171-175.
34. Gabbott PL, Somogyi J, Stewart MG, Hamori J. 1986. GABA-immunoreactive neurons in the rat cerebellum: a light and electron microscope study. J Comp Neurol 251:474-490.
35. Gabbott PL, Dickie BG, Vaid RR, Headlam AJ, Bacon SJ. 1997. Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J Comp Neurol 377:465-499.
36. Gabbott P, Headlam A, Busby S. 2002. Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (Areas 25/32) of the rat. Brain Res 946:314-322.
37. Gaffan D, Parker A. 2000. Mediodorsal thalamic function in scene memory in rhesus monkeys. Brain 123:816-827.
38. Gibson J, Beierlein M, Connors B. 1999. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
39. Giguere M, Goldman-Rakic PS. 1988. Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277:195-213.
40. Groenewegen H. 1988. Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsalprefrontal topography. Neuroscience 24:379-431.
41. Guillery RW. 1995. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J Anat 187:583-592.
42. Guillery R, Sherman S. 2002. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33:163-175.
43. Gulyas AI, Megias M, Emri Z, Freund TF. 1999. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci 19:10082-10097.
44. Gupta A, Wang Y, Markram H. 2000. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
45. Hayes T, Lewis D. 1992. Nonphosphorylated neurofilament protein and calbindin immunoreactivity in layer III pyramidal neurons of human neocortex. Cereb Cortex 2:56-67.
46. Hersch SM, White EL. 1981a. Quantification of synapses formed with apical dendrites of Golgi-impregnated pyramidal cells: variability in thalamocortical inputs, but consistency in the ratios of asymmetrical to symmetrical synapses. Neuroscience 6:1043-1051.
47. Hersch SM, White EL. 1981b. Thalamocortical synapses involving identified neurons in mouse primary somatosensory cortex: a terminal degeneration and Golgi/EM study. J Comp Neurol 195:253-263.
48. Hersch SM, White EL. 1981c. Thalamocortical synapses with corticothalamic projection neurons in mouse SmI cortex: electron microscopic demonstration of a monosynaptic feedback loop. Neurosci Lett 24:207-210.
49. Hunt PR, Aggleton JP. 1998a. An examination of the spatial working memory deficit following neurotoxic medial dorsal thalamic lesions in rats. Behav Brain Res 97:129-141.
50. Hunt PR, Aggleton JP. 1998b. Neurotoxic lesions of the dorsomedial thalamus impair the acquisition but not the performance of delayed matching to place by rats: a deficit in shifting response rules. J Neurosci 18:10045-10052.
51. Jensen KF, Killackey HP. 1987. Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J Neurosci 7:3529-3543.
52. Jinno S, Kosaka T. 2004. Parvalbumin is expressed in glutamatergic and GABAergic corticostriatal pathway in mice. J Comp Neurol 477:188-201.
53. Jones EG. 2001. The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595-601.
54. Kawaguchi Y. 1995. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
55. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31:277-287.
56. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
57. Keller A, White EL. 1986. Distribution of glutamic acid decarboxylase-immunoreactive structures in the barrel region of mouse somatosensory cortex. Neurosci Lett 66:245-250.
58. Keller A, White EL. 1987. Synaptic organization of GABAergic neurons in the mouse SmI cortex. J Comp Neurol 262:1-12.
59. Kinomura S, Larsson J, Gulyas B, Roland PE, 1996. Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 271:512-515.
60. Kisvarday ZF, Kim DS, Eysel UT, Bonhoeffer T. 1994. Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex. Eur J Neurosci 6:1619-1632.
61. Krettek J, Price J. 1977. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157-191.
62. Kubota Y, Hattori R, Yui Y. 1994. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649: 159-173.
63. Kuroda M, Murakami K, Oda S, Shinkai M, Kishi K. 1993. Direct synaptic connections between thalamocortical axon terminals from the mediodorsal thalamic nucleus (MD) and corticothalamic neurons to MD in the prefrontal cortex. Brain Res 612:339-344.
64. Kuroda M, Murakami K, Shinkai M, Ojima H, Kishi K. 1995a. Electron microscopic evidence that axon terminals from the mediodorsal thalamic nucleus make direct synaptic contacts with callosal cells in the prelimbic cortex of the rat. Brain Res 677:348-353.
65. Kuroda M, Murakami K, Kishi K, Price JL. 1995b. Thalamocortical synapses between axons from the mediodorsal thalamic nucleus and pyramidal cells in the prelimbic cortex of the rat. J Comp Neurol 356: 143-151.
66. Kuroda M, Ojima H, Igarashi H, Murakami K, Okada A, Shinkai M. 1996a. Synaptic relationships between axon terminals from the mediodorsal thalamic nucleus and layer III pyramidal cells in the prelimbic cortex of the rat. Brain Res 708:185-190.
67. Kuroda M, Murakami K, Igarashi H, Okada A. 1996b. The convergence of axon terminals from the mediodorsal thalamic nucleus and ventral tegmental area on pyramidal cells in layer V of the rat prelimbic cortex. Eur J Neurosci 8:1340-1349.
68. Kuroda M, Yokofujita J, Murakami K. 1998. An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus. Prog Neurobiol 54:417-458.
69. Kuroda M, Yokofujita J, Oda S, Price JL. 2004. Synaptic relationships between axon terminals from the mediodorsal thalamic nucleus and gamma-aminobutyric acidergic cortical cells in the prelimbic cortex of the rat. J Comp Neurol 477:220-234.
70. Lewis DA. 2000. GABAergic local circuit neurons and prefrontal cortical dysfunction in schizophrenia. Brain Res Brain Res Rev 31:270-276.
71. Lewis DA, Cruz DA, Melchitzky DS, Pierri JN. 2001. 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 158:1411-1422.
72. Matthews DE, Farewell VT. 1996. Fisher's tests for 2×2 contingency tables. Using and understanding medical statistics. Basel: Karger, p 19-37.
73. McCasland JS, Hibbard LS. 1997. GABAergic neurons in barrel cortex show strong, whisker-dependent metabolic activation during normal behavior. J Neurosci 17:5509-5527.
74. McFarland NR, Haber SN. 2002. Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 22:8117-8132.
75. Melchitzky D, Lewis D. 2003. Pyramidal neuron local axon terminals in monkey prefrontal cortex: differential targeting of subclasses of GABA neurons. Cereb Cortex 13:452-460.
76. Melchitzky DS, Sesack SR, Lewis DA. 1999. Parvalbumin-immunoreactive axon terminals in macaque monkey and human prefrontal cortex: laminar, regional, and target specificity of type I and type II synapses. J Comp Neurol 408:11-22.
77. Melchitzky DS, Gonzalez-Burgos G, Barrionuevo G, Lewis DA. 2001. Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex. J Comp Neurol 430:209-221.
78. Miettinen R, Gulyas A, Baimbridge K, Jacobowitz D, Freund T. 1992. Calretinin is present in non-pyramidal cells of the rat hippocampus. II. Co-existence with other calcium binding proteins and GABA. Neuroscience 48:29-43.
79. Moruzzi G, Magoun H. 1995. Brain stem reticular formation and activation of the EEG. J Neuropsychiatry Clin Neurosci 7:251-267.
80. Mumby D, Pinel J, Dastur F. 1993. Mediodorsal thalamic lesions and object recognition in rats. Psychobiology 21:27-36.
81. Nie F, Wong-Riley MT. 1995. Double labeling of GABA and cytochrome oxidase in the macaque visual cortex: quantitative EM analysis. J Comp Neurol 356:115-131.
82. Novikov LN. 2001. Labeling of central projections of primary afferents in adult rats: a comparison between biotinylated dextran amine, neurobiotin and Phaseolus vulgaris-leucoagglutinin. J Neurosci Methods 112:145-154.
83. Pakkenberg B. 1990. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 47:1023-1028.
84. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates, 2nd ed. New York: Academic Press.
85. Peters A, Saldanha J. 1976. The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. III. Layer VI. Brain Res 105:533-537.
86. Petersen CC, Sakmann B. 2001. Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging. J Neurosci 21:8435-8446.
87. Pinto A, Jankowski M, Sesack SR. 2003. Projections from the paraventricular nucleus of the thalamus to the rat prefrontal cortex and nucleus accumbens shell: ultrastructural characteristics and spatial relationships with dopamine afferents. J Comp Neurol 459:142-155.
88. Popken GJ, Bunney WE Jr, Potkin SG, Jones EG. 2000. Subnucleus-specific loss of neurons in medial thalamus of schizophrenics. Proc Natl Acad Sci U S A 97:9276-9280.
89. Porter J, Johnson C, Agmon A. 2001. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 21:2699-2710.
90. Pouille F, Scanziani M. 2001. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163.
91. Preuss TM, Kaas JH. 1996. Parvalbumin-like immunoreactivity of layer V pyramidal cells in the motor and somatosensory cortex of adult primates. Brain Res 712:353-357.
92. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG. 2000. Pathway tracing using biotinylated dextran amines. J Neurosci Methods 103:23-37.
93. Rogers JH. 1987. Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J Cell Biol 105:1343-1353.
94. Romanski LM, LeDoux JE. 1993. Organization of rodent auditory cortex: anterograde transport of PHA-L from MGv to temporal neocortex. Cereb Cortex 3:499-514.
95. Schwaller B, Buchwald P, Blumcke I, Celio MR, Hunziker W. 1993. Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639-648.
96. Sesack SR, Bressler CN, Lewis DA. 1995. Ultrastructural associations between dopamine terminals and local circuit neurons in the monkey prefrontal cortex: a study of calretinin-immunoreactive cells. Neurosci Lett 200:9-12.
97. Sesack SR, Hawrylak VA, Melchitzky DS, Lewis DA. 1998. Dopamine innervation of a subclass of local circuit neurons in monkey prefrontal cortex: ultrastructural analysis of tyrosine hydroxylase and parvalbumin immunoreactive structures. Cereb Cortex 8:614-622.
98. Sesack S, Medvitz N, Miner L, Ekema G. 2001. Pyramidal neuron intrinsic collaterals in the rat prefrontal cortex: synaptic targets and selective input to parvalbumin-containing interneurons. Soc Neurosci Abstr 27: 1930.
99. Sillito A. 1975. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol 250:305-329.
100. Simons DJ, Carvell GE. 1989. Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61:311-330.
101. Smiley J, Goldman-Rakic P. 1993. Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. Cereb Cortex 3:223-238.
102. Staiger J, Zilles K, Freund T. 1996. Distribution of GABAergic elements postsynaptic to ventroposteromedial thalamic projections in layer IV of rat barrel cortex. Eur J Neurosci 8:2273-2285.
103. Steriade M. 1997. Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb Cortex 7:583-604.
104. Tamas G, Buhl E, Somogyi P. 1997. Massive autaptic self-innervation of GABAergic neurons in cat visual cortex. J Neurosci 17:6352-6364.
105. Tamas G, Somogyi P, Buhl E. 1998. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J Neurosci 18:4255-4270.
106. Tamminga C, Hashimoto T, Volk DW, Lewis DA. 2004. GABA neurons in the human prefrontal cortex. Am J Psychiatry 161:1764.
107. Tanibuchi I, Goldman-Rakic PS. 2003. Dissociation of spatial-, object-, and sound-coding neurons in the mediodorsal nucleus of the primate thalamus. J Neurophysiol 89:1067-1077.
108. van Brederode JF, Helliesen MK, Hendrickson AE. 1991. Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat. Neuroscience 44:157-171.
109. 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 Brain Res Rev 39:107-140.
110. Veenman CL, Reiner A. 1996. Ultrastructural morphology of synapses formed by corticostriatal terminals in the avian striatum. Brain Res 707:1-12.
111. Veenman CL, Reiner A, Honig MG. 1992. Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J Neurosci Methods 41:239-254.
112. Veznedaroglu E, Milner T. 1992. Elimination of artifactual labeling of hippocampal mossy fibers seen following pre-embedding immunogoldsilver technique by pretreatment with zinc chelator. Microsc Res Tech 23:100-101.
113. Vogt BA, Rosene DL, Peters A. 1981. Synaptic termination of thalamic and callosal afferents in cingulate cortex of the rat. J Comp Neurol 201: 265-283.
114. Volk DW, Lewis DA. 2002. Impaired prefrontal inhibition in schizophrenia: relevance for cognitive dysfunction. Physiol Behav 77:501-505.
115. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. 2002. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12:395-410.
116. Watanabe Y, Funahashi S. 2004a. Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. I. Cue-, delay-, and response-period activity. J Neurophysiol 92:1738-1755.
117. Watanabe Y, Funahashi S. 2004b. Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. II. Activity encoding visual versus motor signal. J Neurophysiol 92:1756-1769.
118. Welker E, Armstrong-James M, Van der Loos H, Kraftsik R. 1993. The mode of activation of a barrel column: response properties of single units in the somatosensory cortex of the mouse upon whisker deflection. Eur J Neurosci 5:691-712.
119. White EL. 1978. Identified neurons in mouse Sml cortex which are postsynaptic to thalamocortical axon terminals: a combined Golgi-electron microscopic and degeneration study. J Comp Neurol 181:627-661.
120. Williams SM, Goldman-Rakic PS, Leranth C. 1992. The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J Comp Neurol 320:353-369.
121. Woo TU, Miller JL, Lewis DA. 1997. Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry 154:1013-1015.
122. Wouterlood FG, Groenewegen HJ. 1985. Neuroanatomical tracing by use of Phaseolus vulgaris-leucoagglutinin (PHA-L): electron microscopy of PHA-L-filled neuronal somata, dendrites, axons and axon terminals. Brain Res 326:188-191.
123. Wouterlood FG, Jorritsma-Byham B. 1993. The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J Neurosci Methods 48:75-87.
124. Young KA, Manaye KF, Liang C, Hicks PB, German DC. 2000. Reduced number of mediodorsal and anterior thalamic neurons in schizophrenia. Biol Psychiatry 47:944-953.
125. Zhu Y, Stornetta RL, Zhu JJ. 2004. Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons. J Neurosci 24:5101-5108.
126. Zimmermann L, Schwaller B. 2002. Monoclonal antibodies recognizing epitopes of calretinins: dependence on Ca2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium 31:13-25.