Prefrontal pathways target excitatory and inhibitory systems in memory-related medial temporal cortices

NeuroImage

Volumn 55, Issue 4, 2011, Pages 1461-1474

  Bunce, Jamie G ^a   Barbas, Helen ^a,b  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anterior cingulate; Calbindin; Non human primate; Parahippocampal cortex; Parvalbumin; Triple labeling immunohistochemisty

Indexed keywords

ANIMAL EXPERIMENT; ANTERIOR CINGULATE; ARTICLE; ATTENTION; BRAIN CORTEX; BRAIN SIZE; CONTROLLED STUDY; EXCITATION; FEMALE; INNERVATION; MALE; MEMORY; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PARAHIPPOCAMPUS CORTEX; POSTSYNAPTIC INHIBITION; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GYRUS CINGULI; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; NEURAL INHIBITION; NEURAL PATHWAYS; PREFRONTAL CORTEX; TEMPORAL LOBE;

EID: 79952703619     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.01.064     Document Type: Article

References (108)

1. Apergis-Schoute J., Pinto A., Paré D. Ultrastructural organization of medial prefrontal inputs to the rhinal cortices. Eur. J. Neurosci. 2006, 24(1):135-144.
2. Barbas H., Blatt G.J. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 1995, 5:511-533.
3. Barbas H., Ghashghaei H., Dombrowski S.M., Rempel-Clower N.L. Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J. Comp. Neurol. 1999, 410:343-367.
4. Barbas H., Medalla M., Alade O., Suski L., Zikopoulos B., Lera P. Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. Cereb. Cortex 2005, 15:1356-1370.
5. Barbas H., Saha S., Rempel-Clower N., Ghashghaei T. Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci. 2003, 4:25.
6. Biella G., Uva L., de Curtis M. Propagation of neuronal activity along the neocortical-perirhinal-entorhinal pathway in the guinea pig. J. Neurosci. 2002, 22:9972-9979.
7. Blatt G.J., Pandya D.N., Rosene D.L. Parcellation of cortical afferents to three distinct sectors in the parahippocampal gyrus of the rhesus monkey: an anatomical and neurophysiological study. J. Comp. Neurol. 2003, 466:161-179.
8. Borgers C., Epstein S., Kopell N.J. Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(46):18023-18028.
9. Botvinick M.M., Cohen J.D., Carter C.S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci. 2004, 8(12):539-546.
10. Buia C., Tiesinga P. Attentional modulation of firing rate and synchrony in a model cortical network. J. Comput. Neurosci. 2006, 20(3):247-264.
11. Bunce JG, Barbas H. (2008) Anterior cingulate projections to medial temporal cortices are positioned to modulate mnemonic output. Washington: Society for Neuroscience Abstract, 2008 Online.
12. Burwell R.D., Amaral D.G. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J. Comp. Neurol. 1998, 391:293-321.
13. Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro N.M., Knight R.T. Gamma power is phase-locked to theta oscillations in human neocortex. Science 2006, 313(5793):1626-1628.
14. Carmichael S.T., Price J.L. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 1995, 363:615-641.
15. Carr D.B., Sesack S.R. Callosal terminals in the rat prefrontal cortex: synaptic targets and association with GABA-immunoreactive structures. Synapse 1998, 29:193-205.
16. Chrobak J.J., Buzsaki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 1998, 18(1):388-398.
17. de Curtis M., Paré D. The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus. Prog. Neurobiol. 2004, 74:101-110.
18. DeFelipe J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 1997, 14:1-19.
19. DeFelipe J., Hendry S.H., Jones E.G. Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity. Brain Res. 1989, 503:49-54.
20. Dombrowski S.M., Hilgetag C.C., Barbas H. Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb. Cortex 2001, 11:975-988.
21. Ellender T.J., Paulsen O. The many tunes of perisomatic targeting interneurons in the hippocampal network. Front Cell Neurosci. 2010, 4:26.
22. Fan J., Byrne J., Worden M.S., Guise K.G., McCandliss B.D., Fossella J., Posner M.I. The relation of brain oscillations to attentional networks. J. Neurosci. 2007, 27(23):6197-6206.
23. Fell J., Klaver P., Lehnertz K., Grunwald T., Schaller C., Elger C.E., Fernandez G. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci. 2001, 4(12):1259-1264.
24. Fiala J.C. Reconstruct: a free editor for serial section microscopy. J. Microsc. 2005, 218:52-61.
25. Fiala J.C., Harris K.M. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J. Microsc. 2001, 202:468-472.
26. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 2005, 9(10):474-480.
27. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291(5508):1560-1563.
28. Fuchs E.C., Zivkovic A.R., Cunningham M.O., Middleton S., Lebeau F.E., Bannerman D.M., Rozov A., Whittington M.A., Traub R.D., Rawlins J.N., Monyer H. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 2007, 53(4):591-604.
29. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J. Comp. Neurol. 2004, 468:86-95.
30. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., Geinisman Y. Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions. Neuroscience 2004, 125(3):615-623.
31. Geinisman Y., Morrell F., de Yoledo-Morell L. Axospinous synapses with segmented postsynaptic densities: a morphologically distinct synaptic subtype contributing to the number of profiles of 'perforated' synapses visualized in random sections. Brain Res. 1987, 423:179-188.
32. Germuska M., Saha S., Fiala J.C., Barbas H. Synaptic distinction of laminar specific prefrontal-temporal pathways in primates. Cereb. Cortex 2006, 16:865-875.
33. Gonchar Y., Burkhalter A. Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J. Neurosci. 2003, 23:10904-10912.
34. Gray C.M., Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci. U. S. A. 1989, 86(5):1698-1702.
35. Greenough W.T., West R.W., DeVoogd T.J. Subsynaptic plate perforations: changes with age and experience in the rat. Science 1978, 202:1096-1098.
36. Gundersen H.J.G., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. The new stereological tools: disector, fractionator, nucleator and point sample intercepts and their use in pathological research and diagnosis. APMIS 1988, 96:857-881.
37. Hendry S.H., Jones E.G., Emson P.C., Lawson D.E., Heizmann C.W., Streit P. Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp. Brain Res. 1989, 76:467-472.
38. Hilgetag C.C., Dombrowski S.M., Barbas H. Classes and gradients of prefrontal cortical organization in the primate. Neurocomputing 2002, 44-46:823-829.
39. Hoistad M., Barbas H. Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala. Neuroimage 2008, 40:1016-1033.
40. Howard C.V., Reed M.G. Unbiased Stereology, Three Dimensional Measurement in Microscopy 1998, BIOS Scientific Publishers Limited, Oxford.
41. Howard M.W., Rizzuto D.S., Caplan J.B., Madsen J.R., Lisman J., Aschenbrenner-Scheibe R., Schulze-Bonhage A., Kahana M.J. Gamma oscillations correlate with working memory load in humans. Cereb. Cortex 2003, 13(12):1369-1374.
42. Insausti R., Amaral D.G. Entorhinal cortex of the monkey: IV Topographical and laminar organization of cortical afferents. J. Comp. Neurol. 2008, 509:608-641.
43. Jutras M.J., Buffalo E.A. Synchronous neural activity and memory formation. Curr. Opin. Neurobiol. 2010, 20(2):150-155.
44. Jutras M.J., Fries P., Buffalo E.A. Gamma-band synchronization in the macaque hippocampus and memory formation. J. Neurosci. 2009, 29(40):12521-12531.
45. Kajiwara R., Takashima I., Mimura Y., Witter M.P., Iijima T. Amygdala input promotes spread of excitatory neural activity from the perirhinal cortex to the entorhinal-hippocampal circuit. J. Neurophysiol. 2003, 89(4):2176-2184.
46. Kennerley S.W., Walton M.E., Behrens T.E., Buckley M.J., Rushworth M.F. Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 2006, 9:940-947.
47. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. J. Neurosci. 2008, 321(5885):53-57.
48. Kloosterman F., Van Haeften T., Witter M.P., Lopes Da Silva F.H. Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re-entrance in the hippocampal-entorhinal system. Eur. J. Neurosci. 2003, 18:3037-3052.
49. Koganezawa N., Taguchi A., Tominaga T., Ohara S., Tsutsui K., Witter M.P., Iijima T. Significance of the deep layers of entorhinal cortex for transfer of both perirhinal and amygdala inputs to the hippocampus. Neurosci. Res. 2008, 61:172-181.
50. Kondo H., Saleem K.S., Price J.L. Differential connections of the perirhinal and parahippocampal cortex with the orbital and medial prefrontal networks in macaque monkeys. J. Comp. Neurol. 2005, 493:479-509.
51. Lavenex P., Amaral D.G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 2000, 10(4):420-430.
52. Lavenex P., Suzuki W.A., Amaral D.G. Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex. J. Comp. Neurol. 2002, 447:394-420.
53. Lavenex P., Suzuki W.A., Amaral D.G. Perirhinal and parahippocampal cortices of the macaque monkey: Intrinsic projections and interconnections. J. Comp. Neurol. 2004, 472:371-394.
54. Le Van Quyen M., Staba R., Bragin A., Dickson C., Valderrama M., Fried I., Engel J. Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. J. Neurosci. 2010, 30(23):7770-7782.
55. MacDonald A.W., Cohen J.D., Stenger V.A., Carter C.S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 2000, 288(5472):2835-2838.
56. Makeig S., Delorme A., Westerfield M., Jung T., Townsend J., Courchesne E., Sejnowski T.J. Electroencephalographic brain dynamics following manually responded visual targets. PLoS Biol. 2004, 2(6):e176.
57. Mann E.O., Mody I. Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat Neurosci. 2010, 13(2):205-221.
58. Manns J.R., Eichenbaum H. Evolution of declarative memory. Hippocampus 2006, 16(9):795-808.
59. Medalla M., Barbas H. Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur. J. Neurosci. 2006, 23:161-179.
60. Medalla M., Barbas H. Synapses with inhibitory neurons differentiate anterior cingulate from dorsolateral prefrontal pathways associated with cognitive control. Neuron 2009, 61(4):609-620.
61. Medalla M., Barbas H. Anterior cingulate synapses in prefrontal areas 10 and 46 suggest differential influence in cognitive control. J. Neurosci. 2010, 30(48):16068-16081.
62. Medalla M., Lera P., Feinberg M., Barbas H. Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in primates. Cereb. Cortex 2007, 17(Suppl 1):i136-i150.
63. Middleton S., Jalic J., Kispersky T., Lebeau F.E., Roopun A.K., Kopell N.J., Whittington M.A., Cunningham M.O. NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(47):18572-18577.
64. Mohedano-Moriano A., Martinez-Marcos A., Pro-Sistiaga P., Blaizot X., Arroyo-Jimenez M.M., Marcos P., Artacho-Pérula E., Insausti R. Convergence of unimodal and polymodal sensory input to the entorhinal cortex in the fascicularis monkey. Neuroscience 2008, 151:255-271.
65. Mohedano-Moriano A., Pro-Sistiaga P., Arroyo-Jimenez M.M., Artacho-Pérula E., Insausti A.M., Marcos P., Cebada-Sánchez S., Martínez-Ruiz J., Muñoz M., Blaizot X., Martinez-Marcos A., Amaral D.G., Insausti R. Topographical and laminar distribution of cortical input to the monkey entorhinal cortex. J. Anat. 2007, 211:250-260.
66. Moore C.T., Wilson C.G., Mayer C.A., Acquah S.S., Massari V.J., Haxhiu M.A. A GABAergic inhibitory microcircuit controlling cholinergic outflow to the airways. J. Appl. Physiol. 2004, 96:260-270.
67. Muñoz M., Insausti R. Cortical efferents of the entorhinal cortex and the adjacent parahippocampal region in the monkey (Macaca fascicularis). Eur. J. Neurosci. 2005, 22:1368-1388.
68. Murthy V.N., Sejnowski T.J., Stevens C.F. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 1997, 18:599-612.
69. Otte S., Hasenstaub A., Callaway E.M. Cell type-specific control of neuronal responsiveness by gamma-band oscillatory inhibition. J. Neurosci. 2010, 30(6):2150-2159.
70. Paz R., Bauer E.P., Paré D. Learning-related facilitation of rhinal interactions by medial prefrontal inputs. J. Neurosci. 2007, 27:6542-6551.
71. Paz R., Bauer E.P., Paré D. Theta synchronizes the activity of medial prefrontal neurons during learning. Learn. Mem. 2008, 15(7):524-531.
72. Pelletier J.G., Apergis J., Paré D. Low-probability transmission of neocortical and entorhinal impulses through the perirhinal cortex. J. Neurophysiol. 2004, 91:2079-2089.
73. Peters A., Palay S.L. The morphology of synapses. J. Neurocytol. 1996, 25:687-700.
74. Peters A., Palay S.L., Webster H.D. The Fine Structure of the Nervous System. Neurons and Their Supporting Cells 1991, Oxford University Press, New York.
75. Pinto A., Jankowski M., Sesack S.R. 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. 2003, 459:142-155.
76. Reiner A., Veenman C.L., Medina L., Jiao Y., Del Mar N., Honig M.G. Pathway tracing using biotinylated dextran amines. J. Neurosci. Methods 2000, 103:23-37.
77. Rempel-Clower N.L., Barbas H. The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. Cereb. Cortex 2000, 10(9):851-865.
78. Rosenmund C., Stevens C.F. Definition of readily releasable pool of vesicles at hippocampal synapses. Neuron 1996, 16(6):1197-1207.
79. Rushworth M.F., Buckley M.J., Behrens T.E., Walton M.E., Bannerman D.M. Functional organization of the medial frontal cortex. Curr. Opin. Neurobiol. 2007, 17:220-227.
80. Rushworth M.F., Mars R.B., Summerfield C. General mechanisms for making decisions?. Curr. Opin. Neurol. 2009, 19(1):75-83.
81. Saleem K.S., Kondo H., Price J.L. Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J. Comp. Neurol. 2008, 506:659-693.
82. Schall J.D., Stuphorn V., Brown J.W. Monitoring and control of action by the frontal lobes. Neuron 2002, 36:309-322.
83. Sederberg P.B., Kahana M.J., Howard M.W., Donner E.J., Madsen J.R. Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci. 2003, 23(34):10809-10814.
84. Seltzer B., Pandya D.N. Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res. 1978, 149(1):1-24.
85. Sirevaag A.M., Greenough W.T. Differential rearing effects on rat visual cortex synapses II. Synaptic morphometry. Brain Res. 1985, 351:215-226.
86. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459(7247):698-702.
87. Somogyi P., Tamas G., Lujam R., Buhl E.H. Salient features of synaptic organization in the cerebral cortex. Brain Res. Brain Res. Rev. 1998, 26:113-135.
88. Stevens C.F. Neurotransmitter release at central synapses. Neuron 2003, 40:381-388.
89. Suzuki W.A. Encoding new memories and making them stick. Neuron 2006, 50:19-21.
90. Suzuki W.A., Amaral D.G. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 1994, 14(3 Pt 2):1856-1877.
91. Suzuki W.A., Amaral D.G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 1994, 350(4):497-533.
92. Suzuki W.A., Zola-Morgan S., Squire L.R., Amaral D.G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J. Neurosci. 1993, 13(6):2430-2451.
93. Swanson L.W., Köhler C. Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J. Neurosci. 1986, 6:3010-3023.
94. Tamas G., Szabadics J., Lorincz A., Somogyi P. Input and frequency-specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin. Eur. J. Neurosci. 2004, 20(10):2681-2690.
95. Tomioka R., Rockland K.S. Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. J Comp Neurol. 2007, 505:526-538.
96. Van Hoesen G.W., Pandya D.N. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey III. Efferent connections. Brain Res. 1975, 95(1):25-38.
97. Van Hoesen G.W., Pandya D.N., Butters N. Cortical afferents to the entorhinal cortex of the rhesus monkey. Science 1972, 175:1471-1473.
98. Veenman C.L., Reiner A., Honig M.G. Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J. Neurosci. Methods 1992, 41:239-254.
99. Von Stein A., Sarnthein J. Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int. J. Psychophysiol. 2000, 38(3):301-313.
100. Walmsley B., Alvarez F.J., Fyffe R.E. Diversity of structure and function at mammalian central synapses. Trends Neurosci. 1998, 21:81-88.
101. Wang C., Ulbert I., Schomer D.L., Marinkovic K., Halgren E. Responses of human anterior cingulate cortex microdomains to error detection, conflict monitoring, stimulus-response mapping familiarity, and orienting. J. Neurosci. 2005, 25(3):604-613.
102. Wang X.J. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 2010, 90(3):1195-1268.
103. Wellman B.J., Rockland K.S. Divergent cortical connections to entorhinal cortex from area TF in the macaque. J. Comp. Neurol. 1997, 389:361-376.
104. Womelsdorf T., Fries P. The role of neuronal synchronization in selective attention. Curr. Opin. Neurobiol. 2007, 17:154-160.
105. Womelsdorf T., Fries P., Mitra P.P., Desimone R. Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 2006, 439:733-736.
106. Zikopoulos B., Barbas H. Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J. Neurosci. 2006, 26:7348-7361.
107. Zikopoulos B., Barbas H. Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLoS ONE 2007, 2:e848. 10.1371/journal.pone.0000848.
108. Zola-Morgan S., Squire L.R., Amaral D.G., Suzuki W.A. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J. Neurosci. 1989, 9(12):4355-4370.