Dynamically allocated hub in task-evoked network predicts the vulnerable prefrontal locus for contextual memory retrieval in macaques

PLoS Biology

Volumn 13, Issue 6, 2015, Pages 1-31

  Osada, Takahiro ^a,b   Adachi, Yusuke ^a   Miyamoto, Kentaro ^a   Jimura, Koji ^c   Setsuie, Rieko ^a   Miyashita, Yasushi ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; BRAIN INJURY; COGNITION; CONNECTOME; CONTROLLED STUDY; DECISION MAKING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; INFORMATION PROCESSING; INJURY SEVERITY; MACACA; MEMORY CONSOLIDATION; MEMORY DISORDER; NERVE CELL NETWORK; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PREDICTION; PREFRONTAL CORTEX; SUPPORT VECTOR MACHINE; TASK PERFORMANCE; TIME PERCEPTION; ANIMAL; ANIMAL BEHAVIOR; INJURIES; MALE; MEMORY; MEMORY DISORDERS; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; RHESUS MONKEY;

MACACA;

ANIMALS; BEHAVIOR, ANIMAL; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MEMORY DISORDERS; PREFRONTAL CORTEX;

EID: 84934755524     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002177     Document Type: Article

References (77)

1. Milner B, Petrides M. (1984) Behavioural effects of frontal-lobe lesions in man. Trends Neurosci 7(11): 403-407.
2. Shimamura AP, Janowsky JS, Squire LR (1991) What is the role of frontal lobe damage in memory disorders? In Levin HS, Eisenberg HM, Benton AL, editors. Frontal Lobe Functioning and Dysfunction. New York: Oxford University Press. pp. 173-195.
3. Miyashita Y. (2004) Cognitive memory: Cellular and network machineries and their top-down control. Science 306(5695): 435-440. PMID: 15486288
4. Petrides M. (2005) Lateral prefrontal cortex: Architectonic and functional organization. Philos Trans R Soc Lond B Biol Sci 360: 781-795. PMID: 15937012
5. Osada T, Adachi Y, Kimura HM, Miyashita Y. (2008) Towards understanding of the cortical network underlying associative memory. Philos Trans R Soc Lond B Biol Sci 363(1500): 2187-2199. doi: 10. 1098/rstb. 2008. 2271 PMID: 18339600
6. Passingham RE, Wise SP. (2012) The neurobiology of the prefrontal cortex: Anatomy, evolution, and the origin of insight. Oxford: Oxford University Press.
7. Mah YH, Husain M, Rees G, Nachev P. (2014) Human brain lesion-deficit inference remapped. Brain 137(Pt 9): 2522-2531. doi: 10. 1093/brain/awu164 PMID: 24974384
8. Sporns O. (2014) Contributions and challenges for network models in cognitive neuroscience. Nat Neurosci 17(5): 652-660. doi: 10. 1038/nn. 3690 PMID: 24686784
9. Menon V. (2011) Large-scale brain networks and psychopathology: A unifying triple network model. Trends Cogn Sci 15(10): 483-506. doi: 10. 1016/j. tics. 2011. 08. 003 PMID: 21908230
10. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E. (2006) A resilient, low-frequency, smallworld human brain functional network with highly connected association cortical hubs. J Neurosci 26 (1): 63-72. PMID: 16399673
11. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, et al. (2009) Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to alzheimer's disease. J Neurosci 29(6): 1860-1873. doi: 10. 1523/JNEUROSCI. 5062-08. 2009 PMID: 19211893
12. van den Heuvel MP, Mandl RC, Stam CJ, Kahn RS, Hulshoff Pol HE. (2010) Aberrant frontal and temporal complex network structure in schizophrenia: A graph theoretical analysis. J Neurosci 30(47): 15915-15926. doi: 10. 1523/JNEUROSCI. 2874-10. 2010 PMID: 21106830
13. Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, et al. (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137(Pt 8): 2382-2395. doi: 10. 1093/ brain/awu132 PMID: 25057133
14. Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, et al. (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11(4): 426-428. doi: 10. 1038/nn2072 PMID: 18344993
15. van den Heuvel MP, Sporns O. (2011) Rich-club organization of the human connectome. J Neurosci 31(44): 15775-15786. doi: 10. 1523/JNEUROSCI. 3539-11. 2011 PMID: 22049421
16. Thompson-Schill SL, Swick D, Farah MJ, D'Esposito M, Kan IP, et al. (1998) Verb generation in patients with focal frontal lesions: A neuropsychological test of neuroimaging findings. Proc Natl Acad Sci U S A 95(26): 15855-15860. PMID: 9861060
17. Milner B, Corsi P, Leonard G. (1991) Frontal-lobe contribution to recency judgements. Neuropsychologia 29(6): 601-618. PMID: 1944864
18. Petrides M (1991) Functional specialization within the dorsolateral frontal cortex for serial order memory. Proc R Soc B 246: 299-306. PMID: 1686096
19. Eyler-Zorrilla LT, Aguirre GK, Zarahn E, Cannon TD, D'Esposito M. (1996) Activation of the prefrontal cortex during judgments of recency: A functional MRI study. Neuroreport 7(15-17): 2803-2806.
20. Cabeza R, Mangels J, Nyberg L, Habib R, Houle S, et al. (1997) Brain regions differentially involved in remembering what and when: A PET study. Neuron 19(4): 863-870. PMID: 9354332
21. Konishi S, Uchida I, Okuaki T, Machida T, Shirouzu I, et al. (2002) Neural correlates of recency judgment. J Neurosci 22(21): 9549-9555. PMID: 12417679
22. Dobbins IG, Foley H, Schacter DL, Wagner AD. (2002) Executive control during episodic retrieval: Multiple prefrontal processes subserve source memory. Neuron 35(5): 989-996. PMID: 12372291
23. Suzuki M, Fujii T, Tsukiura T, Okuda J, Umetsu A, et al. (2002) Neural basis of temporal context memory: A functional MRI study. Neuroimage 17(4): 1790-1796. PMID: 12498752
24. Logothetis NK, Guggenberger H, Peled S, Pauls J. (1999) Functional imaging of the monkey brain. Nat Neurosci 2(6): 555-562. PMID: 10448221
25. VanduffelW, Fize D, Mandeville JB, Nelissen K, Van Hecke P, et al. (2001) Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 32(4): 565-577. PMID: 11719199
26. Nakahara K, Hayashi T, Konishi S, Miyashita Y. (2002) Functional MRI of macaque monkeys performing a cognitive set-shifting task. Science 295(5559): 1532-1536. PMID: 11859197
27. Tsao DY, Freiwald WA, Knutsen TA, Mandeville JB, Tootell RB. (2003) Faces and objects in macaque cerebral cortex. Nat Neurosci 6(9): 989-995. PMID: 12925854
28. Koyama M, Hasegawa I, Osada T, Adachi Y, Nakahara K, et al. (2004) Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: Comparison of cortical eye fields with humans. Neuron 41(5): 795-807. PMID: 15003178
29. Pinsk MA, DeSimone K, Moore T, Gross CG, Kastner S. (2005) Representations of faces and body parts in macaque temporal cortex: A functional MRI study. Proc Natl Acad Sci U S A 102(19): 6996- 7001. PMID: 15860578
30. Maier A, Wilke M, Aura C, Zhu C, Ye FQ, et al. (2008) Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey. Nat Neurosci 11(10): 1193-1200. doi: 10. 1038/nn. 2173 PMID: 18711393
31. Ford KA, Gati JS, Menon RS, Everling S. (2009) BOLD fMRI activation for anti-saccades in nonhuman primates. Neuroimage 45(2): 470-476. doi: 10. 1016/j. neuroimage. 2008. 12. 009 PMID: 19138749
32. Kagan I, Iyer A, Lindner A, Andersen RA. (2010) Space representation for eye movements is more contralateral in monkeys than in humans. Proc Natl Acad Sci U S A 107(17): 7933-7938. doi: 10. 1073/ pnas. 1002825107 PMID: 20385808
33. Lafer-Sousa R, Conway BR. (2013) Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat Neurosci 16(12): 1870-1878. doi: 10. 1038/nn. 3555 PMID: 24141314
34. Miyamoto K, Osada T, Adachi Y, Matsui T, Kimura HM, et al. (2013) Functional differentiation of memory retrieval network in macaque posterior parietal cortex. Neuron 77(4): 787-799. doi: 10. 1016/j. neuron. 2012. 12. 019 PMID: 23439129
35. Wang Z, Chen LM, Negyessy L, Friedman RM, Mishra A, et al. (2013) The relationship of anatomical and functional connectivity to resting-state connectivity in primate somatosensory cortex. Neuron 78 (6): 1116-1126. doi: 10. 1016/j. neuron. 2013. 04. 023 PMID: 23791200
36. Uhrig L, Dehaene S, Jarraya B. (2014) A hierarchy of responses to auditory regularities in the macaque brain. J Neurosci 34(4): 1127-1132. doi: 10. 1523/JNEUROSCI. 3165-13. 2014 PMID: 24453305
37. O'Reilly JX, Woolrich MW, Behrens TE, Smith SM, Johansen-Berg H. (2012) Tools of the trade: Psychophysiological interactions and functional connectivity. Soc Cogn Affect Neurosci 7(5): 604-609. doi: 10. 1093/scan/nss055 PMID: 22569188
38. Miyamoto K, Osada T, Adachi Y. (2014) Remapping of memory encoding and retrieval networks: Insights from neuroimaging in primates. Behav Brain Res 275: 53-61. doi: 10. 1016/j. bbr. 2014. 08. 046 PMID: 25192634
39. VanduffelW, Zhu Q, Orban GA. (2014) Monkey cortex through fMRI glasses. Neuron 83(3): 533-550. doi: 10. 1016/j. neuron. 2014. 07. 015 PMID: 25102559
40. Rubinov M, Sporns O. (2010) Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 52(3): 1059-1069. doi: 10. 1016/j. neuroimage. 2009. 10. 003 PMID: 19819337
41. Stephan KE, Kamper L, Bozkurt A, Burns GA, Young MP, et al. (2001) Advanced database methodology for the collation of connectivity data on the macaque brain (CoCoMac). Philos Trans R Soc Lond B Biol Sci 356(1412): 1159-1186. PMID: 11545697
42. Stephan KE. (2004) On the role of general system theory for functional neuroimaging. J Anat 205(6): 443-470. PMID: 15610393
43. Ezzyat Y, Davachi L. (2014) Similarity breeds proximity: Pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity. Neuron 81(5): 1179-1189. doi: 10. 1016/j. neuron. 2014. 01. 042 PMID: 24607235
44. Hsieh LT, Gruber MJ, Jenkins LJ, Ranganath C. (2014) Hippocampal activity patterns carry information about objects in temporal context. Neuron 81(5): 1165-1178. doi: 10. 1016/j. neuron. 2014. 01. 015 PMID: 24607234
45. Naya Y, Suzuki WA. (2011) Integrating what and when across the primate medial temporal lobe. Science 333(6043): 773-776. doi: 10. 1126/science. 1206773 PMID: 21817056
46. Petrides M. (1994) Frontal lobes and working memory: Evidence from investigations of the effects of cortical excisions in nonhuman primates. In Boller F, Grafman J, editors. Handbook of neuropsychology, vol. 9. Amsterdam: Elsevier. pp. 59-82.
47. Modha DS, Singh R. (2010) Network architecture of the long-distance pathways in the macaque brain. Proc Natl Acad Sci U S A 107(30): 13485-13490. doi: 10. 1073/pnas. 1008054107 PMID: 20628011
48. Harriger L, van den Heuvel MP, Sporns O. (2012) Rich club organization of macaque cerebral cortex and its role in network communication. PLoS One 7(9): e46497. doi: 10. 1371/journal. pone. 0046497 PMID: 23029538
49. Spiegler BJ, Mishkin M. (1981) Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations. Behav Brain Res 3(3): 303-317. PMID: 7306385
50. Mishkin M. (1982) A memory system in the monkey. Philos Trans R Soc Lond B Biol Sci 298(1089): 83-95. PMID: 6125978
51. Horel JA, Pytko-Joiner DE, Voytko ML, Salsbury K. (1987) The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav Brain Res 23(1): 29-42. PMID: 3828045
52. Petrides M. (2000) Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory. J Neurosci 20(19): 7496-7503. PMID: 11007909
53. Badre D, D'Esposito M. (2009) Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci 10(9): 659-669. doi: 10. 1038/nrn2667 PMID: 19672274
54. Neubert FX, Mars RB, Thomas AG, Sallet J, Rushworth MF. (2014) Comparison of human ventral frontal cortex areas for cognitive control and language with areas in monkey frontal cortex. Neuron 81(3): 700-713. doi: 10. 1016/j. neuron. 2013. 11. 012 PMID: 24485097
55. Kaiser M, Martin R, Andras P, Young MP. (2007) Simulation of robustness against lesions of cortical networks. Eur J Neurosci 25(10): 3185-3192. PMID: 17561832
56. Honey CJ, Sporns O. (2008) Dynamical consequences of lesions in cortical networks. Hum Brain Mapp 29(7): 802-809. doi: 10. 1002/hbm. 20579 PMID: 18438885
57. Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O. (2009) Modeling the impact of lesions in the human brain. PLoS Comput Biol 5(6): e1000408. doi: 10. 1371/journal. pcbi. 1000408 PMID: 19521503
58. Isoda M, Tsutsui K, Katsuyama N, Naganuma T, Saito N, et al. (2005) Design of a head fixation device for experiments in behaving monkeys. J Neurosci Methods 141(2): 277-282. PMID: 15661310
59. Koyano KW, Machino A, Takeda M, Matsui T, Fujimichi R, et al. (2011) In vivo visualization of singleunit recording sites using MRI-detectable elgiloy deposit marking. J Neurophysiol 105(3): 1380-1392. doi: 10. 1152/jn. 00358. 2010 PMID: 21123662
60. Matsui T, Tamura K, Koyano KW, Takeuchi D, Adachi Y, et al. (2011) Direct comparison of spontaneous functional connectivity and effective connectivity measured by intracortical microstimulation: An fMRI study in macaque monkeys. Cerebral Cortex 21(10): 2348-2356. doi: 10. 1093/cercor/bhr019 PMID: 21368090
61. Matsui T, Koyano KW, Koyama M, Nakahara K, Takeda M, et al. (2007) MRI-based localization of electrophysiological recording sites within the cerebral cortex at single-voxel accuracy. Nature Methods 4(2): 161-168. PMID: 17179936
62. Adachi Y, Osada T, Sporns O, Watanabe T, Matsui T, et al. (2012) Functional connectivity between anatomically unconnected areas is shaped by collective network-level effects in the macaque cortex. Cerebral Cortex 22(7): 1586-1592. doi: 10. 1093/cercor/bhr234 PMID: 21893683
63. Matsui T, Koyano KW, Tamura K, Osada T, Adachi Y, et al. (2012) FMRI activity in the macaque cerebellum evoked by intracortical microstimulation of the primary somatosensory cortex: Evidence for polysynaptic propagation. PLoS One 7(10): e47515. doi: 10. 1371/journal. pone. 0047515 PMID: 23118875
64. Miyamoto K, Adachi Y, Osada T, Watanabe T, Kimura HM, et al. (2014) Dissociable memory traces within the macaque medial temporal lobe predict subsequent recognition performance. J Neurosci 34 (5): 1988-1997. doi: 10. 1523/JNEUROSCI. 4048-13. 2014 PMID: 24478378
65. Burgund ED, Lugar HM, Miezin FM, Petersen SE. (2003) Sustained and transient activity during an object-naming task: A mixed blocked and event-related fMRI study. Neuroimage 19(1): 29-41. PMID: 12781725
66. Genovese CR, Lazar NA, Nichols T. (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15(4): 870-878. PMID: 11906227
67. Paxinos G, Huang X, Petrides M, Toga A. (2008) The rhesus monkey brain in stereotaxic coordinates. London: Elsevier Academic.
68. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, et al. (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8(5): 443-459. PMID: 11522765
69. Friston K, Buechel C, Fink G, Morris J, Rolls E, et al. (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6(3): 218-229. PMID: 9344826
70. Honey CJ, Kotter R, Breakspear M, Sporns O. (2007) Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci U S A 104(24): 10240-10245. PMID: 17548818
71. Artzy-Randrup Y, Stone L. (2005) Generating uniformly distributed random networks. Phys Rev E Stat Nonlin Soft Matter Phys 72(5 Pt 2): 056708. PMID: 16383786
72. Minati L, Grisoli M, Seth AK, Critchley HD. (2012) Decision-making under risk: A graph-based network analysis using functional MRI. Neuroimage 60(4): 2191-2205. doi: 10. 1016/j. neuroimage. 2012. 02. 048 PMID: 22387471
73. Kamitani Y, Tong F. (2005) Decoding the visual and subjective contents of the human brain. Nat Neurosci 8(5): 679-685. PMID: 15852014
74. Haynes JD, Rees G. (2006) Decoding mental states from brain activity in humans. Nat Rev Neurosci 7 (7): 523-534. PMID: 16791142
75. Watanabe T, Kimura HM, Hirose S, Wada H, Imai Y, et al. (2012) Functional dissociation between anterior and posterior temporal cortical regions during retrieval of remote memory. J Neurosci 32(28): 9659-9670. doi: 10. 1523/JNEUROSCI. 5553-11. 2012 PMID: 22787051
76. Chang C, Lin C. (2011) LIBSVM: A library for support vector machines. ACM Transactions on Intelligent Systems and Technology 2(3): 27:1-27:27.
77. Dosenbach NU, Nardos B, Cohen AL, Fair DA, Power JD, et al. (2010) Prediction of individual brain maturity using fMRI. Science 329(5997): 1358-1361. doi: 10. 1126/science. 1194144 PMID: 20829489