Top

Published in:

01-03-2018 | Original Paper

Parcellation of Macaque Cortex with Anatomical Connectivity Profiles

Authors: Jiaojian Wang, Zhentao Zuo, Sangma Xie, Yifan Miao, Yuanye Ma, Xudong Zhao, Tianzi Jiang

Published in: Brain Topography | Issue 2/2018

Abstract

The macaque model has been widely used to investigate the brain mechanisms of specific cognitive functions and psychiatric disorders. However, a detailed functional architecture map of the macaque cortex in vivo is still lacking. Here, we aimed to construct a new macaque cortex atlas based on its anatomical connectivity profiles using in vivo diffusion MRI. First, we defined the macaque cortical seed areas using the NeuroMaps atlas. Then, we applied the anatomical connectivity patterns-based parcellation approach to parcellate the macaque cortex into 80 subareas in each hemisphere, which were approximately symmetric between the two hemispheres. In each hemisphere, we identified 14 subareas in the frontal cortex, 9 subareas in the somatosensory cortex, 13 subareas in the parietal cortex, 16 subareas in the temporal cortex, 16 subareas in the occipital cortex, and 12 subareas in the limbic system. Finally, the graph-based network analyses of the anatomical network based on newly constructed macaque cortex atlas identified seven hub areas including bilateral ventral premotor cortex, bilateral superior parietal lobule, right medial precentral gyrus, and right precuneus. This newly constructed macaque cortex atlas may facilitate studies of the structure and functions of the macaque brain in the future.

Available only for authorised users

Azadbakht H, Parkes LM, Haroon HA, Augath M, Logothetis NK, de Crespigny A, D’Arceuil HE, Parker GJ (2015) Validation of high-resolution tractography against in vivo tracing in the macaque visual cortex. Cereb Cortex 25(11):4299–4309. doi:10.1093/cercor/bhu326 CrossRefPubMedPubMedCentral

Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256(2):211–228. doi:10.1002/cne.902560203 CrossRefPubMed

Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111(3):209–219CrossRefPubMed

Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103(3):247–254CrossRefPubMed

Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage 34(1):144–155. doi:10.1016/j.neuroimage.2006.09.018 CrossRefPubMed

Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19(12):2767–2796. doi:10.1093/cercor/bhp055 CrossRefPubMedPubMedCentral

Binney RJ, Parker GJ, Lambon Ralph MA (2012) Convergent connectivity and graded specialization in the rostral human temporal lobe as revealed by diffusion-weighted imaging probabilistic tractography. J Cogn Neurosci 24(10):1998–2014. doi:10.1162/jocn_a_00263 CrossRefPubMed

Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186–198. doi:10.1038/nrn2575 CrossRefPubMed

Calabrese E, Badea A, Coe CL, Lubach GR, Shi Y, Styner MA, Johnson GA (2015) A diffusion tensor MRI atlas of the postmortem rhesus macaque brain. NeuroImage 117:408–416. doi:10.1016/j.neuroimage.2015.05.072 CrossRefPubMedPubMedCentral

Capitanio JP, Emborg ME (2008) Contributions of non-human primates to neuroscience research. Lancet 371(9618):1126–1135. doi:10.1016/S0140-6736(08)60489-4 CrossRefPubMed

Donahue CJ, Sotiropoulos SN, Jbabdi S, Hernandez-Fernandez M, Behrens TE, Dyrby TB, Coalson T, Kennedy H, Knoblauch K, Van Essen DC, Glasser MF (2016) Using diffusion tractography to predict cortical connection strength and distance: a quantitative comparison with tracers in the monkey. J Neurosci 36(25):6758–6770. doi:10.1523/JNEUROSCI.0493-16.2016 CrossRefPubMedPubMedCentral

Eickhoff SB, Heim S, Zilles K, Amunts K (2006) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 32(2):570–582CrossRefPubMed

Fan L, Wang J, Zhang Y, Han W, Yu C, Jiang T (2014) Connectivity-based parcellation of the human temporal pole using diffusion tensor imaging. Cereb Cortex 24(12):3365–3378. doi:10.1093/cercor/bht196 CrossRefPubMed

Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47CrossRefPubMed

Frey S, Pandya DN, Chakravarty MM, Bailey L, Petrides M, Collins DL (2011) An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space). NeuroImage 55(4):1435–1442. doi:10.1016/j.neuroimage.2011.01.040 CrossRefPubMed

Gallay DS, Gallay MN, Jeanmonod D, Rouiller EM, Morel A (2012) The insula of Reil revisited: multiarchitectonic organization in macaque monkeys. Cereb Cortex 22(1):175–190. doi:10.1093/cercor/bhr104 CrossRefPubMed

Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8(1):30–52CrossRefPubMed

Gong G, Rosa-Neto P, Carbonell F, Chen ZJ, He Y, Evans AC (2009) Age- and gender-related differences in the cortical anatomical network. J Neurosci 29(50):15684–15693. doi:10.1523/JNEUROSCI.2308-09.2009 CrossRefPubMedPubMedCentral

Gregoriou GG, Rossi AF, Ungerleider LG, Desimone R (2014) Lesions of prefrontal cortex reduce attentional modulation of neuronal responses and synchrony in V4. Nat Neurosci 17(7):1003–1011. doi:10.1038/nn.3742 CrossRefPubMedPubMedCentral

Hagmann P, Jonasson L, Maeder P, Thiran JP, Wedeen VJ, Meuli R (2006) Understanding diffusion MR imaging techniques: from scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. Radiographics 26(Suppl 1):S205–S223. doi:10.1148/rg.26si065510 CrossRefPubMed

Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6(7):e159. doi:10.1371/journal.pbio.0060159 CrossRefPubMedPubMedCentral

Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ, Meuli R, Thiran JP, Grant PE (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci USA 107(44):19067–19072. doi:10.1073/pnas.1009073107 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

Hutchison RM, Everling S (2014) Broad intrinsic functional connectivity boundaries of the macaque prefrontal cortex. NeuroImage 88:202–211. doi:10.1016/j.neuroimage.2013.11.024 CrossRefPubMed

Hutchison RM, Gallivan JP, Culham JC, Gati JS, Menon RS, Everling S (2012a) Functional connectivity of the frontal eye fields in humans and macaque monkeys investigated with resting-state fMRI. J Neurophysiol 107(9):2463–2474. doi:10.1152/jn.00891.2011 CrossRefPubMed

Hutchison RM, Womelsdorf T, Gati JS, Leung LS, Menon RS, Everling S (2012b) Resting-state connectivity identifies distinct functional networks in macaque cingulate cortex. Cereb Cortex 22(6):1294–1308. doi:10.1093/cercor/bhr181 CrossRefPubMed

Hutchison RM, Culham JC, Flanagan JR, Everling S, Gallivan JP (2015) Functional subdivisions of medial parieto-occipital cortex in humans and nonhuman primates using resting-state fMRI. NeuroImage 116:10–29. doi:10.1016/j.neuroimage.2015.04.068 CrossRefPubMed

Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM (2004) Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci USA 101(36):13335–13340. doi:10.1073/pnas.0403743101 CrossRefPubMedPubMedCentral

Kaiser M, Hilgetag CC (2004) Edge vulnerability in neural and metabolic networks. Biol Cybern 90(5):311–317. doi:10.1007/s00422-004-0479-1 CrossRefPubMed

Krubitzer L, Clarey J, Tweedale R, Elston G, Calford M (1995) A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J Neurosci 15(5 Pt 2):3821–3839PubMed

Ku SP, Tolias AS, Logothetis NK, Goense J (2011) fMRI of the face-processing network in the ventral temporal lobe of awake and anesthetized macaques. Neuron 70(2):352–362. doi:10.1016/j.neuron.2011.02.048 CrossRefPubMed

Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701. doi:10.1103/PhysRevLett.87.198701 CrossRefPubMed

Lewis JW, Van Essen DC (2000a) Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol 428(1):112–137CrossRefPubMed

Lewis JW, Van Essen DC (2000b) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol 428(1):79–111CrossRefPubMed

Li W, Qin W, Liu H, Fan L, Wang J, Jiang T, Yu C (2013) Subregions of the human superior frontal gyrus and their connections. NeuroImage 78:46–58. doi:10.1016/j.neuroimage.2013.04.011 CrossRefPubMed

Liu H, Qin W, Li W, Fan L, Wang J, Jiang T, Yu C (2013) Connectivity-based parcellation of the human frontal pole with diffusion tensor imaging. J Neurosci 33(16):6782–6790. doi:10.1523/JNEUROSCI.4882-12.2013 CrossRefPubMed

Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106(47):20069–20074. doi:10.1073/pnas.0905314106 CrossRefPubMedPubMedCentral

Markov NT, Misery P, Falchier A, Lamy C, Vezoli J, Quilodran R, Gariel MA, Giroud P, Ercsey-Ravasz M, Pilaz LJ, Huissoud C, Barone P, Dehay C, Toroczkai Z, Van Essen DC, Kennedy H, Knoblauch K (2011) Weight consistency specifies regularities of macaque cortical networks. Cereb Cortex 21(6):1254–1272. doi:10.1093/cercor/bhq201 CrossRefPubMed

Mars RB, Jbabdi S, Sallet J, O’Reilly JX, Croxson PL, Olivier E, Noonan MP, Bergmann C, Mitchell AS, Baxter MG, Behrens TE, Johansen-Berg H, Tomassini V, Miller KL, Rushworth MF (2011) Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31(11):4087–4100. doi:10.1523/JNEUROSCI.5102-10.2011 CrossRefPubMedPubMedCentral

Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296(5569):910–913. doi:10.1126/science.1065103 CrossRefPubMed

Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U (2002) Network motifs: simple building blocks of complex networks. Science 298(5594):824–827. doi:10.1126/science.298.5594.824 CrossRefPubMed

Modha DS, Singh R (2010) Network architecture of the long-distance pathways in the macaque brain. Proc Natl Acad Sci USA 107(30):13485–13490. doi:10.1073/pnas.1008054107 CrossRefPubMedPubMedCentral

Morecraft RJ, Cipolloni PB, Stilwell-Morecraft KS, Gedney MT, Pandya DN (2004) Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey. J Comp Neurol 469(1):37–69. doi:10.1002/cne.10980 CrossRefPubMed

Morecraft RJ, Stilwell-Morecraft KS, Cipolloni PB, Ge J, McNeal DW, Pandya DN (2012) Cytoarchitecture and cortical connections of the anterior cingulate and adjacent somatomotor fields in the rhesus monkey. Brain Res Bull 87(4–5):457–497. doi:10.1016/j.brainresbull.2011.12.005 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

Newman ME (2003) The structure and function of complex networks. SIAM Rev 45(2):167–256CrossRef

Pandya DN, Sanides F (1973) Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern. Z Anat Entwicklungsgesch 139(2):127–161CrossRefPubMed

Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204(2):196–210. doi:10.1002/cne.902040208 CrossRefPubMed

Passingham RE, Stephan KE, Kotter R (2002) The anatomical basis of functional localization in the cortex. Nat Rev Neurosci 3(8):606–616. doi:10.1038/nrn893 pii]CrossRefPubMed

Paxinos G, Huang XF, Toga AW (2000) The rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego

Petrides M, Pandya DN (2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 16(2):291–310CrossRefPubMed

Preuss TM, Goldman-Rakic PS (1991) Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca. J Comp Neurol 310(4):475–506. doi:10.1002/cne.903100403 CrossRefPubMed

Rohlfing T, Kroenke CD, Sullivan EV, Dubach MF, Bowden DM, Grant KA, Pfefferbaum A (2012) The INIA19 Template and NeuroMaps Atlas for primate brain image parcellation and spatial normalization. Front Neuroinform 6:27. doi:10.3389/fninf.2012.00027 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

Seelke AM, Padberg JJ, Disbrow E, Purnell SM, Recanzone G, Krubitzer L (2012) Topographic Maps within Brodmann’s Area 5 of macaque monkeys. Cereb Cortex 22(8):1834–1850. doi:10.1093/cercor/bhr257 CrossRefPubMed

Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res 149(1):1–24CrossRefPubMed

Seltzer B, Pandya DN (1989) Intrinsic connections and architectonics of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 290(4):451–471. doi:10.1002/cne.902900402 CrossRefPubMed

Sporns O, Tononi G, Kotter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1(4):e42. doi:10.1371/journal.pcbi.0010042 CrossRefPubMedPubMedCentral

Styner M, Knickmeyer R, Joshi S, Coe C, Short SJ, Gilmore J (2007) Automatic brain segmentation in rhesus monkeys. In: Medical imaging, 2007. International Society for Optics and Photonics, pp 65122L–65128L

Wang J, Fan L, Zhang Y, Liu Y, Jiang D, Zhang Y, Yu C, Jiang T (2012) Tractography-based parcellation of the human left inferior parietal lobule. NeuroImage 63(2):641–652. doi:10.1016/j.neuroimage.2012.07.045 CrossRefPubMed

Wang J, Fan L, Wang Y, Xu W, Jiang T, Fox PT, Eickhoff SB, Yu C, Jiang T (2015a) Determination of the posterior boundary of Wernicke’s area based on multimodal connectivity profiles. Hum Brain Mapp 36(5):1908–1924. doi:10.1002/hbm.22745 CrossRefPubMedPubMedCentral

Wang J, Yang Y, Fan L, Xu J, Li C, Liu Y, Fox PT, Eickhoff SB, Yu C, Jiang T (2015b) Convergent functional architecture of the superior parietal lobule unraveled with multimodal neuroimaging approaches. Hum Brain Mapp 36:238–257. doi:10.1002/hbm.22626 CrossRefPubMed

Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393(6684):440–442. doi:10.1038/30918 CrossRefPubMed

Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M (2012) The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48(1):58–81. doi:10.1016/j.cortex.2011.03.004 CrossRefPubMed

Zhang Y, Fan L, Zhang Y, Wang J, Zhu M, Zhang Y, Yu C, Jiang T (2014) Connectivity-based parcellation of the human posteromedial cortex. Cereb Cortex 24(3):719–727. doi:10.1093/cercor/bhs353 CrossRefPubMed

Title: Parcellation of Macaque Cortex with Anatomical Connectivity Profiles
Authors: Jiaojian Wang
Zhentao Zuo
Sangma Xie
Yifan Miao
Yuanye Ma
Xudong Zhao
Tianzi Jiang
Publication date: 01-03-2018
Publisher: Springer US
Published in: Brain Topography / Issue 2/2018
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-017-0576-9

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Parcellation of Macaque Cortex with Anatomical Connectivity Profiles

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2018

Permutation Mutual Information: A Novel Approach for Measuring Neuronal Phase-Amplitude Coupling

EEG Frequency-Tagging and Input–Output Comparison in Rhythm Perception

A Preliminary Study on Precision Image Guidance for Electrode Placement in an EEG Study

Erratum to: The Callosal Relay Model of Interhemispheric Communication: New Evidence from Effective Connectivity Analysis

Mapping Slow Waves by EEG Topography and Source Localization: Effects of Sleep Deprivation

The Callosal Relay Model of Interhemispheric Communication: New Evidence from Effective Connectivity Analysis