Parallel driving and modulatory pathways link the prefrontal cortex and thalamus

PLoS ONE

Volumn 2, Issue 9, 2007, Pages

  Zikopoulos, Basilis ^a   Barbas, Helen ^a,b,c  

^a BOSTON UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALBINDIN; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; PARVALBUMIN;

ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; ASSOCIATION CORTEX; CONTROLLED STUDY; MENTAL DISEASE; NERVE PROJECTION; NEUROCHEMISTRY; NONHUMAN; PREFRONTAL CORTEX; RHESUS MONKEY; SENSORY SYSTEM; SYNAPSE; THALAMUS NUCLEUS; ANIMAL; CYTOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; MACACA; NERVE CELL; PHYSIOLOGY; THALAMUS;

PRIMATES;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; MACACA MULATTA; NEURONS; PREFRONTAL CORTEX; SYNAPSES; THALAMUS;

EID: 41049110218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000848     Document Type: Article

References (105)

1. Steriade M, Jones EG, McCormick DA (1997) Thalamus-Organisation and function. Oxford: Elsevier Science.
2. Jones EG (1985) The Thalamus. New York (NY): Plenum Press.
3. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37: 563-576.
4. Llinas RR, Steriade M (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95: 3297-3308.
5. Steriade, M (2004) Local gating of information processing through the thalamus. Neuron 41: 493-494.
6. Contreras D, Destexhe A, Terrence JS, Steriade M. (1996) Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274: 771-774.
7. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.
8. Guillery RW, Sherman SM (2002) Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33: 163-175.
9. Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357: 1695-1708.
10. Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B Biol Sci 357: 1659-1673.
11. Jones EG (1998) A new view of specific and nonspecific thalamocortical connections. Adv Neurol 77: 49-71.
12. Guillery RW (1995) Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J Anat 187 ( Pt 3): 583-592.
13. Rouiller EM, Welker E (2000) A comparative analysis of the morphology of corticothalamic projections in mammals. Brain Res Bull 53: 727-741.
14. Reichova I, Sherman SM (2004) Somatosemory corticothalamic projections: distinguishing drivers from modulators. J Neurophysiol 92: 2185-2197.
15. Sherman SM, Guillery RW (1998) On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". Proc Natl Acad Sci U S A 95: 7121-7126.
16. Eaton SA, Salt TE (1996) Role of N-methyl-D-aspartate and metabotropic glutamate receptors in corticothalamic excitatory postsynaptic potentials in vivo. Neuroscience 73: 1-5.
17. Li J, Guido W, Bickford ME (2003) Two distinct types of corticothalamic EPSPs and their contribution to short-term synaptic plasticity. J Neurophysiol 90: 3429-3440.
18. Jones EG, Hendry SHC (1989) Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1: 222-246.
19. Jones EG (1998) Viewpoint: the core and matrix of thalamic organization. Neuroscience, 85: 331-345.
20. Rockland KS (1996) Two types of corticopulvinar terminations: round (type 2) and elongate (type I). J Comp Neurol 368: 57-87.
21. Rockland KS, Andresen J, Cowie RJ, Robinson DL (1999) Single axon analysis of pulvinocortical connections to several visual areas in the macaque. J Comp Neurol 406: 221-250.
22. Casagrande VA, Guillery RW, Sherman SM (2005) Cortical function: A view from the thalamus. Prog Brain Res 149.
23. Abbott LF, Chance FS (2005) Drivers and modulators from push-pull and balanced synaptic input. Prog Brain Res 149: 147-155.
24. Barbas H, Henion TH, Dermon CR (1991) Diverse thalamic projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 313: 65-94.
25. 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.
26. Xiao D, Barbas H (2004) Circuits through prefrontal cortex, basal ganglia, and ventral anterior nucleus map pathways beyond motor control. Thalamus & Related Systems 2: 325-343.
27. Zikopoulas B, Barbas H (2006) Prefromal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanism. J Neurosci 26: 7348-7361.
28. Germuska M, Saha S, Fiala J, Barbas H (2006) Synaptic distinction of laminar specific prefrontal-temporal pathways in primates. Cereb Cortex 16: 865-875.
29. Medalla M, Lera P, Feinberg M, Barbas H (2007) Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in primates. Cereb Cortex, In press.
30. Negyessy L, Goldman-Rakic PS (2005) Morphometric characterization of synapses in the primate prefrontal cortex formed by afferents from the mediodorsal thalamic nucleus. Exp Brain Res 164: 148-154.
31. Schwartz ML, Dekker JJ, Goldman-Rakic PS (1991) Dual mode of corticothalamic synaptic termination in the mediodorsal nucleus of the rhesus monkey. J Comp Neurol 309: 289-304.
32. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, et al. (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375: 493-497.
33. Schweizer FE, Ryan TA (2006) The synaptic vesicle: cycle of exocytosis and endocytosis. Curr Opin Neurobiol 16: 298-304.
34. Becherer U, Rettig J (2006) Vesicle pools, docking, priming, and release. Cell Tissue Res 326: 393-407.
35. Rollenhagen A, Lubke JH (2006) The morphology of excitatory central synapses: from structure to function. Cell Tissue Res 326: 221-237.
36. Gabbott PL, Bacon SJ (1996) Local circuit neurons in the medial prefrontal cortex (areas 24ab,c, 25 and 32) in die monkey: II. Quantitative areal and laminar distributions. J Comp Neurol 364: 609-636.
37. Dombrowski SM, Hilgetag CC, Barbas H (2001) Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb Cortex 11: 975-988.
38. Vidnyanszky Z, Gorcs TJ, Negyessy L, Borostyankio, Z, Knopfel T, et al. (1996) Immunocytochemical visualization of the mGluR1a metabotropic glutamate reciptor at synapses of corticothalamic terminals originating from area 17 of the rat. Eur J Neurosci 8: 1061-1071.
39. Ilinsky IA, Kultas-Ilinsky K (1990) Fine structure of the magnocellular subdivision of the ventral anterior thalamic nucleus (VAmc) of Macaca mulatta: I. Cell types and synaptology. J Comp Neurol 294: 455-478.
40. Wurtz RH, Sommer MA, Cavanaugh J (2005) Drivers from the deep: the contribution of collicular input to thalamocortical processing. Prog Brain Res 149: 207-225.
41. Guillery RW (2005) Anatomical pathways that link perception and action. Cortical Function: A View from the Thalamus 149: 235-256.
42. Guillery RW (2003) Branching thalamic afferents link action and perception. Journal of Neurophysiology 90: 539-548.
43. Guillery RW, Sherman SM (2002) The thalamus as a monitor of motor outputs. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357: 1809-1821.
44. Kao CQ Coulter DA (1997) Physiology and pharmacology of corticothalamic stimulation-evoked responses in rat somatosensory thalamic neurons in vitro. J Neurophysiol 77: 2661-2676.
45. Golshani P, Warren RA, Jones EG (1998) Progression of change in NMDA, non-NMDA, and metabotropic glutamate receptor function at the developing corticothalamic synapse. Journal of Neurophysiology 80: 113-154.
46. Turner JP, Salt TE (1998) Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurotics in vitro. J Physiol 510 (Pt 3): 829-843.
47. Ojima H (1994) Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb Cortex 4: 646-63.
48. Rouiller EM, Simm GM, Villa AE, deRibaupierre Y, deRibaupierre F (1991) Auditory corticocordcal interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp Brain Res 86: 483-505.
49. Pierce JP, Mendell LM (1993) Quantitative ultrastructure of la boutons in the ventral norn: scaling and positional relationships. J Neurosci 13: 4748-4763.
50. Pierce JP, Lewin GR (1994) An ultrastructural size principle. Neuroscience 58: 441-446.
51. Shepherd GM, Harris KM (1993) Three-dimensional structure and composition of CA3->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartment. J Neurosci 18: 8300-8310.
52. Rosemmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207.
53. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18: 599-612.
54. Thomson AM (2000) Molecular frequency filters at central synapses. Prog Neurobiol 62: 159-196.
55. Wang S, Eiscriback MA, Bickford ME (2002) Relative distribution of synapses in the pulvinar nucleus of the cat: implications regarding the "driver/modulator" theory of thalamic function. J Comp Neurol. 454: 482-494.
56. Montero VM (1991) A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Exp Brain Res 86: 257-270.
57. Madarasz M, Tombol T, Hajdu F, Somogyi G (1981) Some comparative quantitative data on the different (relay and associative) thalamic nuclei in the cat. A quantitative EM study. Anat Embryol (Berl) 162: 363-378.
58. Liu XB, Honda CN Jones EG (1995) Distribution offour types of synapse on physiologically identified relay neurons in, the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352: 69-91X.
59. Ramcharan EJ, Gnadt JW, Sherman SM (2005) Higher-order thalamic relays burst more than first-order relays. Proc Natl Acad Sci U S A 102: 12236-12241.
60. Van Horn SC, Erisir A, Sherman SM (9009) Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 416: 509-520.
61. Lund JS, Lund RD, Hendrickson AE, Hunt AB, Fuchs AF (1976) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164: 287-304.
62. Abramson BP, Chalupa LM (1985) The laminar distribution of cortical connections with the tecto- and cortico-recipient zones in the caes lateral posterior nucleus. Neuroscience 15: 81-95.
63. 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.
64. Shipp S (2003) The functional logic of cortico-pulvinar connections. Philos Trans R Soc Lond Biol Sci 358: 1605-1624.
65. Lee CC, Sherman SM (2006) The thalamocortical synapse: driver properties from higher order nuclei. 2006 Neuroscience Meeting Planner Atlanta, GA: Society for Neuroscience, 2006 Online 446.4.
66. Somogyi P, Tamas G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26: 113-135.
67. Peters A, Payne BR (1993) Numerical relationships between gemiculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3: 69-78.
68. Kubota Y, Hatad S, Kondo S, Karabe F, Kawaguchi Y, (2007) Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J Neurosci 27: 1139-1150.
69. Volk DW, Lewis DA (2003) Effects of a mediodorsal thalamus lesion on prefrontal inhibitory circuitry: implications for schizophrenia. Biol Psychiatry 53: 385-389.
70. Cipolloni PB, Keller A (1989) Thalamocortical synapses with identified neurons in monkey primary auditory cortex: a combined golgi/EM and GABA/ peptide immunocytochemistry study. Brain Res 492: 347-355.
71. Kwegyir-Afful EE, Bruno RM, Simons DJ, Keller A (2005) The role of thalamic inputs in surround receptive fields of barrel neurons. J Neurosci 25: 5926-5934.
72. 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.
73. Hoover JE, Strick PL (1993) Multiple output channels in the basal ganglia. Science 259: 819-821.
74. Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate, cortex to behaviour. Brain 118: 279-306.
75. Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, et al. (2000) Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. Brain 123 (Pt 2): 394-403.
76. Conn PJ, Battaglia G, Marino MJ, Nicoletti F (2005) Metabotropic glutamate reccptors in the basal ganglia motor circuit. Nat Rev Neurosci 6: 787-798.
77. Llinas RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP (1999) Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci U S A 96: 15222-15227.
78. Garcia-Cabezas MA, Rico B, Sanchez-Gonzalez MA, Cavada C (2007) Distribution of the dopamine innervation in the macaque and human thalamus. Neuroimage 34: 965-984.
79. Lewis DA, Foote SL, Goldstein M, Morrison JH (1988) The dopaminergic innervation of monkey prefrontal cortex: A tyrosine hydroxylase immunohistochemical study. Brain Res 449: 225-243.
80. Goldman-Rakic PS, Lidow MS, Smiley JF, Williams MS (1992) The anatomy of dopamine in monkey and human prefrontal cortex. Journal of Neural Transmission - Supplementum 36: 163-Supplement.
81. Mizuno A, Villalobos ME, Davies MM, Dahl BC, Muller RA (2006) Partially enhanced thalamocortical functional connectivity in autism. Brain Res 1104: 160-174.
82. Herbert MR, Ziegler DA, Makris N, Filipek PA, Kemper TL, et al. (2004) Localization of white matter volume increase in autism and developmental language disorder. Ann Neurol 55: 530-540.
83. Courchesne E, Pierce K (2005) Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 15: 225-230.
84. Larkum ME, Senn W, Luscher HR (2004) Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex 14: 1059-1070.
85. Zikopoulos B, Barbas H (2007) Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci, In Press.
86. Rubenstein JL, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255-267.
87. Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24: 595-601.
88. Xiao D, Barbas H (2002) Pathways for emotions and memory II. afferent input to the anterior thalamic nuclei from prefrontal, temporal, hypothalamic areas and the basal ganglia in the rhesus monkey. Thalamus and Related Systems 2: 33-48.
89. Barbas H, Medalla M, Alade O, Suski J, Zikopoulos B, et al. (2005) Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. Cereb Cortex 15: 1356-1370.
90. Richmond FJR, Gladdy R, Creasy JL, Ditamura S, Smits E, et al. (1994) Efficacy of seven retrograde tracers, compared in multiple-labelling studies of feline motoneurones. J Neurosci Meth 53: 35-46.
91. 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.
92. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, et al. (2000) Pathway tracing using biotinylated dextran amines. J Neurosci Methods 103: 23-37.
93. Jones EG, Tighilet B, Tran BV, Huntsman MM (1998) Nucleus- and cell-specific expression of NMDA and non-NMDA receptor subunits in monkey thalamus. J Comp Neurol 397: 371-393.
94. McCormick DA, von Krosigk M (1992) Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. Proc Natl Acad Sci U S A 89: 2774-2778.
95. Godwin DW, Van Horn SC, Erisir A, Sesma M, Romano C, et al. (1996) Ultrastructural localization suggests that retinal and cortical inputs access different metabotrophic glutamate receptors in the lateral geniculate nucleus. J Neurosci 16(24): 8181-8192.
96. Olszewski J (1952) The Thalamus of the Macaca mulatta. An Atlas for Use with the Stereotasic Instrument. Basel, Switzerland: Karger,S.
97. Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286: 353-375.
98. Walker AE (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73: 59-86.
99. Howard CV, Reed MG (1998) Unbiased Stereology, Three-dimensional Measurement in Microscopy. Oxford: BIOS Scientific Publishers Limited.
100. Gundersen HJ (1986) Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 143 (Pt 1): 3-45.
101. West MJ, Slomianka L, Gundersen HJG (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
102. Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218: 52-61.
103. Hashikawa T, Molinari M, Rausell E, Jones EG (1995) Patchy and laminar terminations of medial geniculate axons in monkey auditory cortex. J Comp Neurol 362: 195-208.
104. Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system. Neurons and their supporting cells. New York: Oxford University Press.
105. Barbas H, Saha S, Rempel-Clower N, Ghashghaei T (2003) Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci 4: 25.