Skip to main content
Log in

A metric survey on the sagittal and coronal morphology of the precuneus in adult humans

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The size, cortical surface area, length and height of the precuneus vary greatly in adult humans. The precuneus is also proportionally much larger in humans than in other primates, and its dorsal region is larger in our species compared with extinct hominids. Its longitudinal and vertical proportions can depend on a real cortical expansion, or on a deformation of the whole brain form due to cranial constraints. In this study, we analyse the correlation between its sagittal and coronal morphology to study the variation of its proportions along the three dimensions. Shape analysis was performed on magnetic resonance scans of 50 adult humans, through both traditional and geometric morphometrics. Results suggest that the degrees of longitudinal, vertical and lateral extension are independent, pointing at different factors involved, and concerning different cortical areas or specific connectivity pathways. This absence of correlation suggests that the individual and evolutionary morphological variations are probably due to actual brain changes, and not to general volume deformation constrained by cranial architecture. These results are discussed in the wider frame of homology and phylogenetic differences, and provide indications for further studies and more targeted surveys.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen JS, Damasio H, Grabowski TJ (2002) Normal neuroanatomical variation in the human brain: an MRI-volumetric study. Am J Phys Anthropol 118:341–358

    Article  PubMed  Google Scholar 

  • Ardesch DJ, Scholtens LH, Li L, Preuss TM, Rilling JK, Van den Heuvel MP (2019) Evolutionary expansion of connectivity between multimodal association areas in the human brain compared with chimpanzees. Proc Natl Acad Sci USA 116:7101–7106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baars BJ (2002) The conscious access hypothesis: origins and recent evidence. Trends Cogn Sci 6:47–52

    Article  PubMed  Google Scholar 

  • Barks SK, Parr LA, Rilling JL (2015) The default mode network in chimpanzees (Pan troglodytes) is similar to that of humans. Cereb Cortex 25:538–544

    Article  PubMed  Google Scholar 

  • Bruner E (2018a) Human paleoneurology and the evolution of the parietal cortex. Brain Behav Evol 91:136–147

    Article  PubMed  Google Scholar 

  • Bruner E (2018b) The brain, the braincase, and the morphospace. In: Bruner E, Ogihara N, Tanabe HC (eds) Digital endocasts—from skulls to brains. Springer, Tokyo, pp 93–114

    Chapter  Google Scholar 

  • Bruner E, Iriki A (2016) Extending mind, visuospatial integration, and the evolution of the parietal lobes in the human genus. Quat Int 405:98–110

    Article  Google Scholar 

  • Bruner E, Rangel de Lázaro G, de la Cuétara JM, Martín-Loeches M, Colom R, Jacobs HIL (2014) Midsagittal brain variation and MRI shape analysis of the precuneus in adult individuals. J Anat 224:367–376

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruner E, Román FJ, de la Cuétara JM, Martin-Loeches M, Colom R (2015a) Cortical surface area and cortical thickness in the precuneus of adult humans. Neuroscience 286:345–352

    Article  CAS  PubMed  Google Scholar 

  • Bruner E, Amano H, de la Cuétara JM, Ogihara N (2015b) The brain and the braincase: a spatial analysis on the midsagittal profile in adult humans. J Anat 227:268–276

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruner E, Preuss T, Chen X, Rilling J (2017a) Evidence for expansion of the precuneus in human evolution. Brain Struct Funct 222:1053–1060

    Article  PubMed  Google Scholar 

  • Bruner E, Pereira-Pedro AS, Chen X, Rilling JK (2017b) Precuneus proportions and cortical folding: a morphometric evaluation on a racially diverse human sample. Ann Anat 211:120–128

    Article  PubMed  Google Scholar 

  • Bruner E, Esteve-Altava B, Rasskin-Gutman D (2018a) Networking brains: modeling spatial relationships of the cerebral cortex. In: Bruner E, Ogihara N, Tanabe HC (eds) Digital endocasts—from skulls to brains. Springer, Tokyo, pp 191–204

    Chapter  Google Scholar 

  • Bruner E, Fedato AP, Silva-Gago M, Alonso-Alcalde R, Terradillos-Bernal M, Fernández-Durantes MA, Martín-Guerra E (2018b) Cognitive archaeology, body cognition, and hand–tool interaction. Progr Brain Res 238:325–345

    Article  Google Scholar 

  • Bruner E, Esteve-Altava B, Rasskin-Gutman D (2019) A network approach to brain form, cortical topology and human evolution. Brain Struct Funct 224:2231–2245

    Article  PubMed  Google Scholar 

  • Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38

    Article  PubMed  Google Scholar 

  • Bzdok D, Heeger A, Langner R, Laird AR, Fox PT, Palomero-Gallagher N, Vogt BA, Zilles K, Eickhoff SB (2015) Subspecialization in the human posterior medial cortex. Neuroimage 106:55–71

    Article  PubMed  Google Scholar 

  • Caminiti R, Innocenti GM, Battaglia-Mayer A (2015) Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans. Neurosci Biobehav Rev 56:73–96

    Article  PubMed  Google Scholar 

  • Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583

    Article  PubMed  Google Scholar 

  • Chamberlain R, McManus IC, Brunswick N, Rankin Q, Riley H, Kanai R (2014) Drawing on the right side of the brain: a voxel-based morphometry analysis of observational drawing. Neuroimage 96:167–173

    Article  PubMed  Google Scholar 

  • Cunningham SI, Tomasi D, Volkow ND (2017) Structural and functional connectivity of the precuneus and thalamus to the default mode network. Hum Brain Map 38:938–956

    Article  Google Scholar 

  • Fransson P, Marrelec G (2008) The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage 42:1178–1184

    Article  PubMed  Google Scholar 

  • Gamberini M, Passarelli L, Fattori P, Galletti C (2020a) Structural connectivity and functional properties of the macaque superior parietal lobule. Brain Struct Funct 225:1349–1367

    Article  PubMed  Google Scholar 

  • Gamberini M, Passarelli L, Impieri D, Worthy KH, Burman KJ, Fattori P, Galletti C, Rosa MGP, Bakola S (2020b) Thalamic afferents emphasize the different functions of macaque precuneate areas. Brain Struct Funct 225:853–870

    Article  PubMed  Google Scholar 

  • Goldring AB, Krubitzer LA (2017) Evolution of the parietal cortex in mammals: from manipulation to tool use. In: Kaas J (ed) Evolution of nervous systems, vol 3, 2nd edn. Elsevier, Oxford, pp 259–286

    Chapter  Google Scholar 

  • Gómez-Robles A, Reyes LD, Sherwood CC (2018) Landmarking brains. In: Bruner E, Ogihara N, Tanabe HC (eds) Digital endocasts—from skulls to brains. Springer, Tokyo, pp 115–126

    Chapter  Google Scholar 

  • Goulas A, Bastiani M, Bezgin G, Uylings HB, Roebroeck A, Stiers P (2014) Comparative analysis of the macroscale structural connectivity in the macaque and human brain. PLoS Comput Biol 10:e1003529

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gray JR, Chabris CF, Braver TS (2003) Neural mechanisms of general fluid intelligence. Nat Neurosci 6:316–322

    Article  CAS  PubMed  Google Scholar 

  • Gunz P, Harvati K (2007) The Neanderthal “chignon”: variation, integration, and homology. J Hum Evol 52:262–274

    Article  PubMed  Google Scholar 

  • 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:e159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaentol Electron 4:1–9

    Google Scholar 

  • Heed T, Buchholz VN, Engel AK, Röder B (2015) Tactile remapping: from coordinate transformation to integration in sensorimotor processing. Trends Cogn Sci 19:251–258

    Article  PubMed  Google Scholar 

  • Huang Y, Hullfish J, De Ridder D, Vanneste S (2019) Meta-analysis of functional subdivisions within human posteromedial cortex. Brain Struct Funct 224:435–452

    Article  CAS  PubMed  Google Scholar 

  • Huntenburg JM, Bazin PL, Margulies DS (2017) Large-scale gradients in human cortical organization. Trends Cogn Sci 22:21–31

    Article  PubMed  Google Scholar 

  • Impieri D, Zilles K, Niu M, Rapan L, Schubert N, Galletti C, Palomero-Gallagher N (2019) Receptor density pattern confirms and enhances the anatomic–functional features of the macaque superior parietal lobule areas. Brain Struct Funct 224:2733–2756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung RE, Haier RJ (2007) The parieto-frontal integration theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 30:135–154

    Article  PubMed  Google Scholar 

  • Kaas JH, Qi HX, Stepniewska I (2017) Evolution of the parietal-frontal networks in primates. In: Kaas J (ed) Evolution of nervous systems, vol 3, 2nd edn. Elsevier, Oxford, pp 287–297

    Chapter  Google Scholar 

  • Kastner S, Chen Q, Jeong SK, Mruczek REB (2017) A brief comparative review of primate posterior parietal cortex: a novel hypothesis on the human toolmaker. Neuropsychology 105:123–134

    Article  CAS  Google Scholar 

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • Koch G, Bonnì S, Pellicciari MC et al (2018) Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal Alzheimer’s disease. Neuroimage 169:302–311

    Article  PubMed  Google Scholar 

  • Lee KH, Choi YY, Gray JR, Cho SH, Chae JH, Lee S, Kim K (2006) Neural correlates of superior intelligence: stronger recruitment of posterior parietal cortex. Neuroimage 29:578–586

    Article  PubMed  Google Scholar 

  • Lieberman DE, Ross C, Ravosa M (2000) The primate cranial base: ontogeny function and integration. Yrb Phys Anthropol 43:117–169

    Article  Google Scholar 

  • Malafouris L (2010) The brain-artefact interface (BAI): a challenge for archaeology and cultural neuroscience. Soc Cogn Affect Neurosci 5:264–273

    Article  PubMed  PubMed Central  Google Scholar 

  • Maldonado IL, Mandonnet E, Duffau H (2012) Dorsal fronto-parietal connections of the human brain: a fiber dissection study of their composition and anatomical relationships. Anat Rec 295:187–195

    Article  Google Scholar 

  • Marcus DS, Wang TH, Parker J, Csernansky JG, Morris JC, Buckner RL (2007) Open access series of imaging studies (OASIS): cross-sectional MRI data in young, middle aged, nondemented, and demented older adults. J Cogn Neurosci 19:1498–1507

    Article  PubMed  Google Scholar 

  • 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 106:20069–20074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meunier D, Lambiotte R, Formito A, Ersche KD, Bullmore ET (2009) Hierarchical modularità in human brain functional networks. Front Neuroinform 3:37

    Article  PubMed  PubMed Central  Google Scholar 

  • Meunier D, Lambiotte R, Bullmore ET (2010) Modular and hierarchically modular organization of brain networks. Front Neurosci 4:200

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller LE, Montroni L, Koun E, Salemme R, Hayward V, Farnè A (2018) Sensing with tools extends somatosensory processing beyond the body. Nature 561:239

    Article  CAS  PubMed  Google Scholar 

  • Miller LE, Fabio C, Ravenda V, Bahmad S, Koun E, Salemme R, Luauté J, Bolognini N, Hayward V, Farnè A (2019) Somatosensory cortex efficiently processes touch located beyond the body. Curr Biol 29:4276–4283

    Article  CAS  PubMed  Google Scholar 

  • Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18:281–292

    Article  CAS  PubMed  Google Scholar 

  • Parvizi J, Van Hoesen GW, Buckwalter J, Damasio A (2006) Neural connections of the posteromedial cortex in the macaque. Proc Natl Acad Sci USA 103:1563–1568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Passarelli L, Rosa MG, Bakola S, Gamberini M, Worthy KH, Fattori P, Galletti C (2018) Uniformity and diversity of cortical projections to precuneate areas in the macaque monkey: what defines area PGm? Cereb Cortex 28:1700–1717

    Article  PubMed  Google Scholar 

  • Pereira-Pedro AS, Bruner E (2016) Sulcal pattern, extension, and morphology of the precuneus in adult humans. Ann Anat 208:85–93

    Article  PubMed  Google Scholar 

  • Pereira-Pedro AS, Rilling JL, Chen X, Preuss TM, Bruner E (2017) Midsagittal brain variation among non-human primates: insights into evolutionary expansion of the human precuneus. Brain Behav Evol 90:255–263

    Article  PubMed  Google Scholar 

  • Pereira-Pedro AS, Bruner E, Gunz P, Neubauer S (2020) A morphometric comparison of the parietal lobe in modern humans and Neanderthals. J Hum Evol 142:102770

    Article  PubMed  Google Scholar 

  • Richtsmeier JT, Flaherty K (2013) Hand in glove: brain and skull in development and dysmorphogenesis. Acta Neuropathol 125:469–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheperjans F, Eickhoff SB, Hömke L, Mohlberg H, Hermann K, Amunts K, Zilles K (2008) Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. Cereb Cortex 18:2141–2157

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to Image J: 25 years of image analysis. Nat Meth 9:671–675

    Article  CAS  Google Scholar 

  • Sereno MI, Huang RS (2014) Multisensory maps in parietal cortex. Curr Opin Neurobiol 24:39–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka S, Kirino E (2017) Reorganization of the thalamocortical network in musicians. Brain Res 1664:48–54

    Article  CAS  PubMed  Google Scholar 

  • Utevsky AV, Smith DV, Huettel SA (2014) Precuneus is a functional core of the default-mode network. J Neurosci 34:932–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaishnavi SN, Vlassenko AG, Rundle MM, Snyder AZ, Mintun MA, Raichle ME (2010) Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci USA 107:17757–17762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenderoth N, Debaere F, Sunaert S, Swinnen SP (2005) The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour. Eur J Neurosci 22:235–246

    Article  PubMed  Google Scholar 

  • Wu Y, Sun D, Wang Y, Ou WY, S, (2016) Segmentation of the cingulum bundle in the human brain: a new perspective based on DSI tractography and fiber dissection study. Front Neuroanat 10:84

    PubMed  PubMed Central  Google Scholar 

  • Yang Z, Chang C, Xu T, Jiang L, Handwerker DA, Castellanos FX, Milham MP, Bandettini PA, Zuo XN (2014) Connectivity trajectory across lifespan differentiates the precuneus from the default network. Neuroimage 89:45–56

    Article  PubMed  Google Scholar 

  • Zelditch ML, Swidersky DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. Elsevier, San Diego

    Google Scholar 

  • Zhang S, Li CR (2012) Functional connectivity mapping of the human precuneus by resting state fMRI. Neuroimage 59:3548–3562

    Article  PubMed  Google Scholar 

  • Zhou Y, Freedman DJ (2019) Posterior parietal cortex plays a causal role in perceptual and categorical decisions. Science 365:180–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zilles K, Palomero-Gallagher N (2001) Cyto-, myelo-, and receptor architectonics of the human parietal cortex. Neuroimage 14:S8–S20

    Article  CAS  PubMed  Google Scholar 

  • Zollikofer CPE, Ponce de León M (2002) Visualizing patterns of craniofacial shape variation in Homo sapiens. Proc R Soc B 269:801–807

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank two anonymous reviewers for their comments and suggestions.

Funding

Spanish Government, Ministerio de Ciencia, Innovación y Universidades (PGC2018-093925-B-C31) (EB); Fundación Atapuerca (SPP).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emiliano Bruner.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Availability of data

Data are available upon request.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bruner, E., Pereira-Pedro, S. A metric survey on the sagittal and coronal morphology of the precuneus in adult humans. Brain Struct Funct 225, 2747–2755 (2020). https://doi.org/10.1007/s00429-020-02152-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-020-02152-0

Keywords

Navigation