Abstract
The foundation for understanding brain connections and related psychiatric diseases lies in human and animal circuitry studies. In rodents and nonhuman primates (NHPs), axonal tracing methods provide the ground-truth connectivity information of brain circuits, coupled with the ability to experimentally manipulate them when combined with other methods. In humans, neuroimaging approaches have taken the lead for studying connectivity patterns in vivo and the changes in network profiles associated with disease. To integrate knowledge from animal models and humans, a critical question is how similar the animal brains and circuits are to the humans’. In this review, we demonstrate the use of meso-circuitry information from tracing studies in NHPs to understand common network connections across species. We show that the meso-circuitry information help establish homologies of cortical and striatal regions and fiber pathways between rodents and NHPs, facilitate the translation of connections that are detailed in animal models to humans, and can locate critical hubs in large-scale brain networks. This review combines anatomic studies across animal models and imaging studies across NHPs and humans to provide a more comprehensive understanding of the hard-wired connectivity that underlies neuroimaging-derived brain networks.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akert K (1964) Comparative anatomy of frontal cortex and thalamo frontal connection. In: Warren JM, Akert K (eds) The frontal granular cortex and behavior. McGraw- Hill Book Co, New York, pp 372–396
Averbeck BB, Lehman J, Jacobson M, Haber SN (2014) Estimates of projection overlap and zones of convergence within frontal-striatal circuits. J Neurosci 34(29):9497–9505. https://doi.org/10.1523/JNEUROSCI.5806-12.2014
Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375
Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates [published erratum appears in Trends Neurosci 1991 Mar; 14(3):119]. Trends Neurosci 14(1):21–27
Beucke JC, Sepulcre J, Eldaief MC, Sebold M, Kathmann N, Kaufmann C (2014) Default mode network subsystem alterations in obsessive-compulsive disorder. Br J Psychiatry 205(5):376–382. https://doi.org/10.1192/bjp.bp.113.137380
Block SR, Liberzon I (2016) Attentional processes in posttraumatic stress disorder and the associated changes in neural functioning. Exp Neurol. https://doi.org/10.1016/j.expneurol.2016.05.009
Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde. Leipzig, J.A. Barth
Bryant RA, Felmingham K, Whitford TJ, Kemp A, Hughes G, Peduto A, Williams LM (2008) Rostral anterior cingulate volume predicts treatment response to cognitive-behavioural therapy for posttraumatic stress disorder. J Psychiatry Neurosci 33(2):142–146
Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease. J Neurosci 29(6):1860–1873. https://doi.org/10.1523/JNEUROSCI.5062-08.2009
Chakrabarty T, Ogrodniczuk J, Hadjipavlou G (2016) Predictive neuroimaging markers of psychotherapy response: a systematic review. Harv Rev Psychiatry 24(6):396–405. https://doi.org/10.1097/HRP.0000000000000132
Choi EY, Tanimura Y, Vage PR, Yates EH, Haber SN (2017) Convergence of prefrontal and parietal anatomical projections in a connectional hub in the striatum. Neuroimage 146:821–832
Choi EY, Yeo BT, Buckner RL (2012) The organization of the human striatum estimated by intrinsic functional connectivity. J Neurophysiol 108(8):2242–2263. https://doi.org/10.1152/jn.00270.2012
Coizet V, Heilbronner SR, Carcenac C, Mailly P, Lehman JF, Savasta M, David O, Deniau JM, Groenewegen HJ, Haber SN (2017) Organization of the anterior limb of the internal capsule in the rat. J Neurosci 37(10):2539–2554. https://doi.org/10.1523/JNEUROSCI.3304-16.2017
Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, McGuire P, Bullmore ET (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137(Pt 8):2382–2395. https://doi.org/10.1093/brain/awu132
Di Martino A, Scheres A, Margulies DS, Kelly AM, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18(12):2735–2747. https://doi.org/10.1093/cercor/bhn041
Field M, Cox WM (2008) Attentional bias in addictive behaviors: a review of its development, causes, and consequences. Drug Alcohol Depend 97(1–2):1–20. https://doi.org/10.1016/j.drugalcdep.2008.03.030
Flaherty A, Graybiel A (1993) Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey. J Neurosci 13(3):1120–1137. https://doi.org/10.1523/jneurosci.13-03-01120.1993
Fullana MA, Cardoner N, Alonso P, Subira M, Lopez-Sola C, Pujol J, Segalas C, Real E, Bossa M, Zacur E, Martinez-Zalacain I, Bulbena A, Menchon JM, Olmos S, Soriano-Mas C (2014) Brain regions related to fear extinction in obsessive-compulsive disorder and its relation to exposure therapy outcome: a morphometric study. Psychol Med 44(4):845–856. https://doi.org/10.1017/S0033291713001128
Gaspar P, Stepniewska I, Kaas JH (1992) Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys. J Comp Neurol 325:1–21
Gerbella M, Borra E, Mangiaracina C, Rozzi S, Luppino G (2015) Corticostriate projections from areas of the “lateral grasping network”: evidence for multiple hand-related input channels. Cereb Cortex. https://doi.org/10.1093/cercor/bhv135
Haber SN (2016) Corticostriatal circuitry. Dialog Clin Neurosci 18(1):7–21
Haber SN, Kim KS, Mailly P, Calzavara R (2006) Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26(32):8368–8376. https://doi.org/10.1523/JNEUROSCI.0271-06.2006
Haber SN, Tang W, Choi EY, Yendiki A, Liu H, Jbabdi S, Versace A, Phillips M (2020) Circuits, networks, and neuropsychiatric disease: transitioning from anatomy to imaging. Biol Psychiat 87(4):318–327. https://doi.org/10.1016/j.biopsych.2019.10.024
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. https://doi.org/10.1371/journal.pbio.0060159
Hayes JP, Vanelzakker MB, Shin LM (2012) Emotion and cognition interactions in PTSD: a review of neurocognitive and neuroimaging studies. Front Integr Neurosci 6:89. https://doi.org/10.3389/fnint.2012.00089
Heilbronner SR, Chafee MV (2019) Learning how neurons fail inside of networks: nonhuman primates provide critical data for psychiatry. Neuron 102(1):21–26. https://doi.org/10.1016/j.neuron.2019.02.030
Heilbronner SR, Rodriguez-Romaguera J, Quirk GJ, Groenewegen HJ, Haber SN (2016) Circuit-based corticostriatal homologies between rat and primate. Biol Psychiatry. https://doi.org/10.1016/j.biopsych.2016.05.012
Jbabdi S, Behrens TE, Smith SM (2010) Crossing fibres in tract-based spatial statistics. Neuroimage 49(1):249–256. https://doi.org/10.1016/j.neuroimage.2009.08.039
Jbabdi S, Lehman JF, Haber SN, Behrens TE (2013) Human and monkey ventral prefrontal fibers use the same organizational principles to reach their targets: tracing versus tractography. J Neurosci 33(7):3190–3201. https://doi.org/10.1523/JNEUROSCI.2457-12.2013
Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE (2015) Measuring macroscopic brain connections in vivo. Nat Neurosci 18(11):1546–1555. https://doi.org/10.1038/nn.4134
Kennis M, Rademaker AR, van Rooij SJ, Kahn RS, Geuze E (2015) Resting state functional connectivity of the anterior cingulate cortex in veterans with and without post-traumatic stress disorder. Hum Brain Mapp 36(1):99–109. https://doi.org/10.1002/hbm.22615
Künzle H (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res 88(2):195–209. https://doi.org/10.1016/0006-8993(75)90384-4
Lehman JF, Greenberg BD, McIntyre CC, Rasmussen SA, Haber SN (2011) Rules ventral prefrontal cortical axons use to reach their targets: implications for diffusion tensor imaging tractography and deep brain stimulation for psychiatric illness. J Neurosci 31(28):10392–10402. https://doi.org/10.1523/JNEUROSCI.0595-11.2011
Leonard CM (1969) The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res 12(2):321–343. https://doi.org/10.1016/0006-8993(69)90003-1
Maier-Hein KH, Neher PF, Houde JC, Cote MA, Garyfallidis E, Zhong J, Chamberland M, Yeh FC, Lin YC, Ji Q, Reddick WE, Glass JO, Chen DQ, Feng Y, Gao C, Wu Y, Ma J, Renjie H, Li Q, Westin CF, Deslauriers-Gauthier S, Gonzalez JOO, Paquette M, St-Jean S, Girard G, Rheault F, Sidhu J, Tax CMW, Guo F, Mesri HY, David S, Froeling M, Heemskerk AM, Leemans A, Bore A, Pinsard B, Bedetti C, Desrosiers M, Brambati S, Doyon J, Sarica A, Vasta R, Cerasa A, Quattrone A, Yeatman J, Khan AR, Hodges W, Alexander S, Romascano D, Barakovic M, Auria A, Esteban O, Lemkaddem A, Thiran JP, Cetingul HE, Odry BL, Mailhe B, Nadar MS, Pizzagalli F, Prasad G, Villalon-Reina JE, Galvis J, Thompson PM, Requejo FS, Laguna PL, Lacerda LM, Barrett R, Dell'Acqua F, Catani M, Petit L, Caruyer E, Daducci A, Dyrby TB, Holland-Letz T, Hilgetag CC, Stieltjes B, Descoteaux M (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8(1):1349. https://doi.org/10.1038/s41467-017-01285-x
Mayberg HS, Brannan SK, Mahurin RK, Jerabek PA, Brickman JS, Tekell JL, Silva JA, McGinnis S, Glass TG, Martin CC, Fox PT (1997) Cingulate function in depression: a potential predictor of treatment response. NeuroReport 8(4):1057–1061
McGeorge AJ, Faull RLM (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29(3):503–537. https://doi.org/10.1016/0306-4522(89)90128-0
Menon V (2011) Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci 15(10):483–506. https://doi.org/10.1016/j.tics.2011.08.003
Milad MR, Rauch SL (2012) Obsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends Cogn Sci 16(1):43–51
O'Neill M, Schultz W (2013) Risk prediction error coding in orbitofrontal neurons. J Neurosci 33(40):15810–15814. https://doi.org/10.1523/JNEUROSCI.4236-12.2013
Oldham S, Fornito A (2019) The development of brain network hubs. Dev Cogn Neurosci 36:100607. https://doi.org/10.1016/j.dcn.2018.12.005
Parthasarathy H, Schall J, Graybiel A (1992) Distributed but convergent ordering of corticostriatal projections: analysis of the frontal eye field and the supplementary eye field in the macaque monkey. J Neurosci 12(11):4468–4488. https://doi.org/10.1523/jneurosci.12-11-04468.1992
Patel R, Spreng RN, Shin LM, Girard TA (2012) Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 36(9):2130–2142. https://doi.org/10.1016/j.neubiorev.2012.06.003
Pizzagalli DA (2011) Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36(1):183–206. https://doi.org/10.1038/npp.2010.166
Preuss TM (1995) Do rats have prefrontal cortex? The rose-woolsey-akert program reconsidered. J Cogn Neurosci 7(1):1–24. https://doi.org/10.1162/jocn.1995.7.1.1
Preuss TM, Goldman-Rakic PS (1991) Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate galago, with comparative comments on anthropoid primates. J Comp Neurol 310(4):507–549
Reep R (1984) Relationship between prefrontal and limbic cortex: a comparative anatomical review. Brain Behav Evol 25(1):5–80. https://doi.org/10.1159/000118849
Reiner A (2010) Organization of corticostriatal projection neuron types. In: Steiner H, Tseng KY (eds) Handbook of behavioral neuroscience, vol 20. Academic Press-Elsevier, Cambridge, MA, pp 323–339
Reveley C, Seth AK, Pierpaoli C, Silva AC, Yu D, Saunders RC, Leopold DA, Ye FQ (2015) Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography. Proc Natl Acad Sci USA 112(21):E2820–2828. https://doi.org/10.1073/pnas.1418198112
Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 18(3):247–291
Rose JE, Woolsey CN (1948) Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat. J Comp Neurol 89(3):279–347
Rubinov M, Bullmore E (2013) Schizophrenia and abnormal brain network hubs. Dialogues Clin Neurosci 15(3):339–349
Safadi Z, Grisot G, Jbabdi S, Behrens TE, Heilbronner SR, McLaughlin NCR, Mandeville J, Versace A, Phillips ML, Lehman JF, Yendiki A, Haber SN (2018) Functional segmentation of the anterior limb of the internal capsule: linking white matter abnormalities to specific connections. J Neurosci 38(8):2106–2117. https://doi.org/10.1523/JNEUROSCI.2335-17.2017
Selemon LD, Goldman-Rakic PS (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5:776–794
Sporns O, Honey CJ, Kötter R (2007) Identification and classification of hubs in brain networks. PLoS ONE 2(10):e1049–e1049. https://doi.org/10.1371/journal.pone.0001049
Tadayonnejad R, Deshpande R, Ajilore O, Moody T, Morfini F, Ly R, O'Neill J, Feusner JD (2017) Pregenual anterior cingulate dysfunction associated with depression in OCD: an integrated multimodal fMRI/(1)H MRS study. Neuropsychopharmacology. https://doi.org/10.1038/npp.2017.249
Tang W, Jbabdi S, Zhu Z, Cottaar M, Grisot G, Lehman JF, Yendiki A, Haber SN (2019) A connectional hub in the rostral anterior cingulate cortex links areas of emotion and cognitive control. Elife 8:e43761
Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, Pierpaoli C (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci USA 111(46):16574–16579. https://doi.org/10.1073/pnas.1405672111
Tomasi D, Volkow ND (2012) Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71(5):443–450. https://doi.org/10.1016/j.biopsych.2011.11.003
van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17(12):683–696. https://doi.org/10.1016/j.tics.2013.09.012
Versace A, Graur S, Greenberg T, Lima Santos JP, Chase HW, Bonar L, Stiffler RS, Hudak R, Kim T, Yendiki A, Greenberg B, Rasmussen S, Liu H, Haber S, Phillips ML (2019) Reduced focal fiber collinearity in the cingulum bundle in adults with obsessive-compulsive disorder. Neuropsychopharmacology. https://doi.org/10.1038/s41386-019-0353-4
Walker AE (1940) A cytoarchitectural study of the prefronal area of the macaque monkey. J Comp Neurol 73:59–86
Yendiki A, Panneck P, Srinivasan P, Stevens A, Zollei L, Augustinack J, Wang R, Salat D, Ehrlich S, Behrens T, Jbabdi S, Gollub R, Fischl B (2011) Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front Neuroinformatics 5:23. https://doi.org/10.3389/fninf.2011.00023
Yeterian EH, Van Hoesen GW (1978) Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res 139:43–63
Acknowledgements
The authors would like to acknowledge the funding from NIH (NIMH PO106435, R01045573, R01MH118257; NINDS UH3NS095554) and University of Minnesota (MnDrive Brain Conditions).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
This is a review paper on existing studies. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committees and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tang, W., Choi, E.Y., Heilbronner, S.R. et al. Nonhuman primate meso-circuitry data: a translational tool to understand brain networks across species. Brain Struct Funct 226, 1–11 (2021). https://doi.org/10.1007/s00429-020-02133-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-020-02133-3