Abstract
Many structural brain asymmetries accompany left hemisphere language dominance. For example, the cingulate sulcus is larger in the medial cortex of the right hemisphere, while the more dorsal paracingulate sulcus is larger on the left. The functional significance of these asymmetries is unknown because fMRI studies rarely attempt to localize activation to specific sulci, possibly due to difficulties in consistent sulcal identification. In medial cortex, for example, there are many regions of partial sulcal overlap where MRI images do not provide sufficient information to unambiguously distinguish a paracingulate sulcus from a displaced anterior cingulate segment. As large samples of postmortem material are rarely available for cytoarchitectural studies of sulcal variation, we have investigated the effect of variation in boundary and sulcal definition on paracingulate asymmetry in the MRI scans of 200 healthy adults (100 men, 100 women). Although women displayed a reliable asymmetry in the size of the paracingulate sulcus, regardless of boundary definition or technique, asymmetry was greatest when (1) the measurement was limited to the midcingulate region between the genu and the anterior commissure; and (2) the more dorsal of two overlapping sulci was always classified as a paracingulate sulcus (rather than as a displaced cingulate segment). The fact that paracingulate asymmetry is maximal in the midcingulate region suggests that this region may play a particular role in hemispheric specialization for language. Future work should investigate the structural and functional correlates of sulcal variation in this region.
Similar content being viewed by others
References
Amunts K, Schleicher A, Ditterich A, Zilles K (2003) Broca’s region: cytoarchitectonic asymmetry and developmental changes. J Comp Neurol 465:72–89
Artiges E, Martelli C, Naccache L, Bartres-Faz D, Leprovost JB, Viard A, Paillere-Martinot ML, Dehaene S, Martinot JL (2006) Paracingulate sulcus morphology and fMRI activation detection in schizophrenia patients. Schizophr Res 82:143–151
Blonder LX, Bowers D, Heilman KM (1991) The role of the right hemisphere in emotional communication. Brain 114:1115–1127
Bryden MP (1982) Laterality: functional asymmetry in the normal brain. Academic Press, New York
Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222
Cannon TD, Rosso IM, Bearden CE, Sanchez LE, Hadley T (1999) A prospective cohort study of neurodevelopmental processes in the genesis and epigenesis of schizophrenia. Dev Psychopathol 11:467–485
Carter CS, Botvinick MM, Cohen JD (1999) The contribution of the anterior cingulate cortex to executive processes in cognition. Rev Neurosci 10:49–57
Chen WK, Swartz JD, Rush LJ, Alvarez CE (2009) Mapping DNA structural variation in dogs. Genome Res 19:500–509
Chiarello C, Kacinik N, Manowitz B, Otto R, Leonard C (2004) Cerebral asymmetries for language: evidence for structural-behavioral correlations. Neuropsychology 18:219–231
Chiarello C, Lombardino LJ, Kacinik NA, Otto R, Leonard CM (2006) Neuroanatomical and behavioral asymmetry in an adult compensated dyslexic. Brain Lang 98:169–181
Chiarello C, Welcome SE, Halderman LK, Towler S, Julagay J, Otto R, Leonard CM (2009a) A large-scale investigation of lateralization in cortical anatomy and word reading: are there sex differences? Neuropsychology (in press)
Chiarello C, Welcome SE, Halderman LK, Leonard CM (2009b) Does degree of asymmetry relate to performance? An investigation of word recognition and reading in consistent and mixed handers. Brain Cogn 69:521–530
Cohen J (1977) Statistical power for the behavioral sciences (revised edition). Academic Press, New York
Crosson B, Sadek JR, Bobholz JA, Gokcay D, Mohr CM, Leonard CM, Maron L, Auerbach EJ, Browd SR, Freeman AJ, Briggs RW (1999) Activity in the paracingulate and cingulate sulci during word generation: an fMRI study of functional anatomy. Cereb Cortex 9:307–316
Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306
Devlin JT, Poldrack RA (2007) In praise of tedious anatomy. Neuroimage 37:1033–1041 (discussion 1050–1038)
Dubois J, Benders M, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Borradori-Tolsa C, Mangin JF, Huppi PS (2008) Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex 18:1444–1454
Eckert MA, Lombardino LJ, Leonard CM (2001) Planar asymmetry tips the phonological playground and environment raises the bar. Child Dev 72:988–1002
Eckert MA, Leonard CM, Molloy EA, Blumenthal J, Zijdenbos AP, Giedd JN (2002) The epigenesis of planum temporale asymmetry in twins. Cereb Cortex 12:749–755
Eckert MA, Leonard CM, Possing ET, Binder JR (2006) Uncoupled leftward asymmetries for planum morphology and functional language processing. Brain Lang 98:102–111
Fink GR, Frackowiak RS, Pietrzyk U, Passingham RE (1997) Multiple nonprimary motor areas in the human cortex. J Neurophysiol 77:2164–2174
Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BT, Mohlberg H, Amunts K, Zilles K (2008) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18:1973–1980
Fornito A, Yucel M, Wood S, Stuart GW, Buchanan JA, Proffitt T, Anderson V, Velakoulis D, Pantelis C (2004) Individual differences in anterior cingulate/paracingulate morphology are related to executive functions in healthy males. Cereb Cortex 14:424–431
Fornito A, Whittle S, Wood SJ, Velakoulis D, Pantelis C, Yucel M (2006a) The influence of sulcal variability on morphometry of the human anterior cingulate and paracingulate cortex. Neuroimage 33:843–854
Fornito A, Yucel M, Wood SJ, Proffitt T, McGorry PD, Velakoulis D, Pantelis C (2006b) Morphology of the paracingulate sulcus and executive cognition in schizophrenia. Schizophr Res 88:192–197
Fukuchi-Shimogori T, Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071–1074
Goldman PS, Galkin T (1978) Prenatal removal of frontal association cortex in the fetal rhesus monkey: anatomical and functional consequences in postnatal life. Brain Res 152:451–485
Grove EA, Fukuchi-Shimogori T (2003) Generating the cerebral cortical area map. Annu Rev Neurosci 26:355–380
Halpern DR, Benbow CP, Geary DC, Gur RC, Shibley Hyde J, Gernsbacher MA (2007) The science of sex differences in science and mathematics. Psychol Sci Pub Interest 8:1–51
Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2:e22
Huster RJ, Westerhausen R, Kreuder F, Schweiger E, Wittling W (2007) Morphologic asymmetry of the human anterior cingulate cortex. Neuroimage 34:888–895
Ide A, Dolezal C, Fernandez M, Labbe E, Mandujano R, Montes S, Segura P, Verschae G, Yarmuch P, Aboitiz F (1999) Hemispheric differences in variability of fissural patterns in parasylvian and cingulate regions of human brains. J Comp Neurol 410:235–242
Isaacs EB, Gadian DG, Sabatini S, Chong WK, Quinn BT, Fischl BR, Lucas A (2008) The effect of early human diet on caudate volumes and IQ. Pediatr Res 63:308–314
Jenkinson M, Smith SM (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156
Johnson-Frey SH, Newman-Norlund R, Grafton ST (2005) A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex 15:681–695
Karlsson EK, Lindblad-Toh K (2008) Leader of the pack: gene mapping in dogs and other model organisms. Nat Rev Genet 9:713–725
Le Provost JB, Bartres-Faz D, Paillere-Martinot ML, Artiges E, Pappata S, Recasens C, Perez-Gomez M, Bernardo M, Baeza I, Bayle F, Martinot JL (2003) Paracingulate sulcus morphology in men with early-onset schizophrenia. Br J Psychiatry 182:228–232
Leonard CM, Voeller KS, Lombardino LJ, Morris MK, Alexander AW, Andersen HG, Garofalakis MA, Hynd GW, Honeyman JC, Mao J, Agee OF, Staab EV (1993) Anomalous cerebral structure in dyslexia revealed with magnetic resonance imaging. Arch Neurol 50:461–469
Leonard CM, Eckert MA, Lombardino LJ, Oakland T, Kranzler J, Mohr CM, King WM, Freeman AJ (2001) Anatomical risk factors for phonological dyslexia. Cereb Cortex 11:148–157
Leonard C, Eckert M, Givens B, Berninger V, Eden G (2006a) Individual differences in anatomy predict reading and oral language impairments in children. Brain 129:3329–3342
Leonard CM, Eckert MA, Kuldau JM (2006b) Exploiting human anatomical variability as a link between genome and cognome. Genes Brain Behav 5(Suppl 1):64–77
Leonard CM, Towler S, Welcome S, Halderman LK, Otto R, Eckert MA, Chiarello C (2008) Size matters: cerebral volume influences sex differences in neuroanatomy. Cereb Cortex 18:2920–2931
Lohmann G, von Cramon DY, Steinmetz H (1999) Sulcal variability of twins. Cereb Cortex 9:754–763
Mangin JF, Riviere D, Cachia A, Duchesnay E, Cointepas Y, Papadopoulos-Orfanos D, Scifo P, Ochiai T, Brunelle F, Regis J (2004) A framework to study the cortical folding patterns. Neuroimage 23(Suppl 1):S129–138
Morecraft RJ, Van Hoesen GW (1998) Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Res Bull 45:209–232
Ono M, Jubik S, Abernathy CD (1990) Atlas of the cerebral sulci. Thieme, New York
Palomero-Gallagher N, Mohlberg H, Zilles K, Vogt B (2008a) Cytology and receptor architecture of human anterior cingulate cortex. J Comp Neurol 508:906–926
Palomero-Gallagher N, Vogt BA, Schleicher A, Mayberg HS, Zilles K (2008b) Receptor architecture of human cingulate cortex: evaluation of the four-region neurobiological model. Hum Brain Mapp. 23:210–222
Parker HG, Kim LV, Sutter NB, Carlson S, Lorentzen TD, Malek TB, Johnson GS, DeFrance HB, Ostrander EA, Kruglyak L (2004) Genetic structure of the purebred domestic dog. Science 304:1160–1164
Passingham RE (1996) Attention to action. Philos Trans R Soc Lond B 351:1473–1479
Paus T, Otaky N, Caramanos Z, MacDonald D, Zijdenbos A, D’Avirro D, Gutmans D, Holmes C, Tomaiuolo F, Evans AC (1996a) In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior-rostral sulci: hemispheric asymmetries, gender differences and probability maps. J Comp Neurol 376:664–673
Paus T, Tomaiuolo F, Otaky N, MacDonald D, Petrides M, Atlas J, Morris R, Evans AC (1996b) Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map. Cereb Cortex 6:207–214
Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342–353
Price JL (2005) Free will versus survival: brain systems that underlie intrinsic constraints on behavior. J Comp Neurol 493:132–139
Pujol J, Lopez A, Deus J, Cardoner N, Vallejo J, Capdevila A, Paus T (2002) Anatomical variability of the anterior cingulate gyrus and basic dimensions of human personality. Neuroimage 15:847–855
Rivera SM, Reiss AL, Eckert MA, Menon V (2005) Developmental changes in mental arithmetic: evidence for increased functional specialization in the left inferior parietal cortex. Cereb Cortex 15:1779–1790
Rushworth MF, Behrens TE (2008) Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci 11:389–397
Rushworth MF, Nixon PD, Wade DT, Renowden S, Passingham RE (1998) The left hemisphere and the selection of learned actions. Neuropsychologia 36:11–24
Rushworth MF, Buckley MJ, Behrens TE, Walton ME, Bannerman DM (2007) Functional organization of the medial frontal cortex. Curr Opin Neurobiol 17:220–227
SAS (2007) SAS/STAT guide for personal computers, version 8. SAS Institute, Cary, NC
Scheperjans F, Eickhoff SB, Homke 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
Shapleske J, Rossell SL, Woodruff PW, David AS (1999) The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Rev 29:26–49
Smart IH, McSherry GM (1986) Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes. J Anat 146:141–152
Smith GE (1907) A new topographical survey of the human cerebral cortex, being an account of the distribution of the anatomically distinct cortical areas and their relationship to the cerebral sulci. J Anat 41:237–258
Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–219
Sutter NB, Mosher DS, Gray MM, Ostrander EA (2008) Morphometrics within dog breeds are highly reproducible and dispute Rensch’s rule. Mamm Genome 19:713–723
Toro R, Burnod Y (2005) A morphogenetic model for the development of cortical convolutions. Cereb Cortex 15:1900–1913
Van Essen D (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318
Van Essen DC, Dierker DL (2007) Surface-based and probabilistic atlases of primate cerebral cortex. Neuron 56:209–225
Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR (1995) Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 359:490–506
Vogt BA, Berger GR, Derbyshire SW (2003) Structural and functional dichotomy of human midcingulate cortex. Eur J Neurosci 18:3134–3144
Wechsler D (1997) WAIS-III: manual: Wechsler Adult intelligence scale, 3rd edn. Psychological Corporation, New York
White T, Andreasen NC, Nopoulos P (2002) Brain volumes and surface morphology in monozygotic twins. Cereb Cortex 12:486–493
Woodcock RW (1987) Woodcock reading mastery tests, revised. American Guidance Service, Circle Pines, MN
Yucel M, Stuart GW, Maruff P, Velakoulis D, Crowe SF, Savage G, Pantelis C (2001) Hemispheric and gender-related differences in the gross morphology of the anterior cingulate/paracingulate cortex in normal volunteers: an MRI morphometric study. Cereb Cortex 11:17–25
Yucel M, Stuart GW, Maruff P, Wood SJ, Savage GR, Smith DJ, Crowe SF, Copolov DL, Velakoulis D, Pantelis C (2002) Paracingulate morphologic differences in males with established schizophrenia: a magnetic resonance imaging morphometric study. Biol Psychiatry 52:15–23
Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45–57
Acknowledgments
This work was supported by NIH grant DC006957 and the McKnight Brain Institute. We are grateful to Ron Otto for arranging for the scans and examining them for neuropathology and to Alex Fornito for advice on cingulate categorization. We thank the student participants and Caroline Anderson, Dawn Joseph, and Kaitlyn Schmutz for their painstaking measurement efforts.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Leonard, C.M., Towler, S., Welcome, S. et al. Paracingulate asymmetry in anterior and midcingulate cortex: sex differences and the effect of measurement technique. Brain Struct Funct 213, 553–569 (2009). https://doi.org/10.1007/s00429-009-0210-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-009-0210-z