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Published in: Brain Structure and Function 1/2017

01-01-2017 | Original Article

Vertex- and atlas-based comparisons in measures of cortical thickness, gyrification and white matter volume between humans and chimpanzees

Authors: William D. Hopkins, Xiang Li, Tim Crow, Neil Roberts

Published in: Brain Structure and Function | Issue 1/2017

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Abstract

What changes in cortical organisation characterise global and localised variation between humans and chimpanzees remains a topic of considerable interest in evolutionary neuroscience. Here, we examined regional variation in cortical thickness, gyrification and white matter in samples of human and chimpanzee brains. Both species were MRI scanned on the same platform using identical procedures. The images were processed and segmented by FSL and FreeSurfer and the relative changes in cortical thickness, gyrification and white matter across the entire cortex were compared between species. In general, relative to chimpanzees, humans had significantly greater gyrification and significantly thinner cortex, particularly in the frontal lobe. Human brains also had disproportionately higher white matter volumes in the frontal lobe, particularly in prefrontal regions. Collectively, the findings suggest that after the split from the common ancestor, white matter expansion and subsequently increasing gyrification occurred in the frontal lobe possibly due to increased selection for human cognitive and motor specialisations.
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Literature
go back to reference Amunts K, Zilles K (2006) A multimodal analysis of structure and function in Broca’s area. In: Grodzinsky Y, Amunts K (eds) Broca’s region. Oxford University Press, Oxford Amunts K, Zilles K (2006) A multimodal analysis of structure and function in Broca’s area. In: Grodzinsky Y, Amunts K (eds) Broca’s region. Oxford University Press, Oxford
go back to reference Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings HB, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412(2):319–341CrossRefPubMed Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings HB, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412(2):319–341CrossRefPubMed
go back to reference Armstrong E, Zilles K, Schleicher A (1993) Cortical folding and the evolution of the human brain. J Hum Evol 20:341–348CrossRef Armstrong E, Zilles K, Schleicher A (1993) Cortical folding and the evolution of the human brain. J Hum Evol 20:341–348CrossRef
go back to reference Bogart SL, Mangin JF, Schapiro SJ, Reamer L, Bennett AJ, Pierre PJ, Hopkins WD (2012) Cortical sulci asymmetries in chimpanzees and macaques: a new look at an old idea. Neuroimage 61:533–541CrossRefPubMedPubMedCentral Bogart SL, Mangin JF, Schapiro SJ, Reamer L, Bennett AJ, Pierre PJ, Hopkins WD (2012) Cortical sulci asymmetries in chimpanzees and macaques: a new look at an old idea. Neuroimage 61:533–541CrossRefPubMedPubMedCentral
go back to reference Brodmann K (1912) Neue Ergebnisse über die vergleichende histologische localisation der grosshirnrinde mit besonderer berücksichtigung des stirnhirns. Anatomischer Anzeiger Supplement 41:157–216 Brodmann K (1912) Neue Ergebnisse über die vergleichende histologische localisation der grosshirnrinde mit besonderer berücksichtigung des stirnhirns. Anatomischer Anzeiger Supplement 41:157–216
go back to reference Dale AM, Fischl B, Sereno MI (1999a) Cortical surface-based analysis: I. Segementation and surface reconstruction. Neuroimage 9(2):179–194CrossRefPubMed Dale AM, Fischl B, Sereno MI (1999a) Cortical surface-based analysis: I. Segementation and surface reconstruction. Neuroimage 9(2):179–194CrossRefPubMed
go back to reference Dale AM, Fischl B, Sereno MI (1999b) Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system. Neuroimage 9(2):195–207CrossRefPubMed Dale AM, Fischl B, Sereno MI (1999b) Cortical surface-based analysis: II. Inflation, flattening, and a surface-based coordinate system. Neuroimage 9(2):195–207CrossRefPubMed
go back to reference De Felipe J (2011) The evolution of the brain, the human nature of cortical curcuits and intellectual creativity. Front Neuroanat 5(29):1–17 De Felipe J (2011) The evolution of the brain, the human nature of cortical curcuits and intellectual creativity. Front Neuroanat 5(29):1–17
go back to reference Deacon TW (1997) The symbolic species: the coevolution of language and the brain. W. W. Norton and Company, New York Deacon TW (1997) The symbolic species: the coevolution of language and the brain. W. W. Norton and Company, New York
go back to reference Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRi scans into gyral based regions of interest. Neuroimage 31:968–980CrossRefPubMed Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRi scans into gyral based regions of interest. Neuroimage 31:968–980CrossRefPubMed
go back to reference Fischl B, Sereno MI, Tootell RB, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8(4):272–284CrossRefPubMed Fischl B, Sereno MI, Tootell RB, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8(4):272–284CrossRefPubMed
go back to reference Fischl B, Salat DH, Busa E, Albert M, Dietrich M, Haselgrove C, Avd Kouwe, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355CrossRefPubMed Fischl B, Salat DH, Busa E, Albert M, Dietrich M, Haselgrove C, Avd Kouwe, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355CrossRefPubMed
go back to reference Fischl B, Van Der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D (2004a) Auomatically parcellating the human cerebral cortex. Cereb Cortex 14(1):11–22CrossRefPubMed Fischl B, Van Der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D (2004a) Auomatically parcellating the human cerebral cortex. Cereb Cortex 14(1):11–22CrossRefPubMed
go back to reference Fischl B, van der Kuwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004b) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22CrossRefPubMed Fischl B, van der Kuwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004b) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22CrossRefPubMed
go back to reference Gomez-Robles A, Hopkins WD, Sherwood CC (2013) Increased morphological asymmetry, evolvability, and plasticity in human brain evolution. Proc R Soc B Biol Sci 280(1761):20130575CrossRef Gomez-Robles A, Hopkins WD, Sherwood CC (2013) Increased morphological asymmetry, evolvability, and plasticity in human brain evolution. Proc R Soc B Biol Sci 280(1761):20130575CrossRef
go back to reference Holloway RL (2002) Brief communication: how much larger Is the relative volume of area ten of the prefrontal cortex in humans? Am J Phys Anthropol 118:389–401CrossRef Holloway RL (2002) Brief communication: how much larger Is the relative volume of area ten of the prefrontal cortex in humans? Am J Phys Anthropol 118:389–401CrossRef
go back to reference Hopkins WD (2013) Behavioral and brain asymmetries in chimpanzees: a case for continuity. Ann N Y Acad Sci 1288:27–35CrossRef Hopkins WD (2013) Behavioral and brain asymmetries in chimpanzees: a case for continuity. Ann N Y Acad Sci 1288:27–35CrossRef
go back to reference Hopkins WD, Nir T (2010) Planum temporale surface area and grey matter asymmetries in chimpanzees (Pan troglodytes): the effect of handedness and comparison within findings in humans. Behav Brain Res 208(2):436–443CrossRefPubMed Hopkins WD, Nir T (2010) Planum temporale surface area and grey matter asymmetries in chimpanzees (Pan troglodytes): the effect of handedness and comparison within findings in humans. Behav Brain Res 208(2):436–443CrossRefPubMed
go back to reference Im K, Lee JM, Shin YW, Kim IY, Kwon JS, Kim SI (2006) Gender difference analysis of cortical thickness in healthy young adults with surface-based methods. Neuroimage 31:31–38CrossRefPubMed Im K, Lee JM, Shin YW, Kim IY, Kwon JS, Kim SI (2006) Gender difference analysis of cortical thickness in healthy young adults with surface-based methods. Neuroimage 31:31–38CrossRefPubMed
go back to reference Kazu RS, Maldonado J, Mota B, Manger PR, Herculano-Houzel S (2014) Cellular scaling rules for the brain of Artiodactyla include a highly folded cortex with few neurons. Front Neuroanat 12(8):128 Kazu RS, Maldonado J, Mota B, Manger PR, Herculano-Houzel S (2014) Cellular scaling rules for the brain of Artiodactyla include a highly folded cortex with few neurons. Front Neuroanat 12(8):128
go back to reference Keller SS, Highley JR, Garcia-Finana M, Sluming V, Rezaie R, Roberts N (2007) Sulcal variability, stereological measurement and asymmetry of Broca’s area on MR images. J Anat 211:534–555PubMedPubMedCentral Keller SS, Highley JR, Garcia-Finana M, Sluming V, Rezaie R, Roberts N (2007) Sulcal variability, stereological measurement and asymmetry of Broca’s area on MR images. J Anat 211:534–555PubMedPubMedCentral
go back to reference Keller SS, Crow TJ, Foundas AL, Amunts K, Roberts N (2009a) Broca’s area: nomenclature, anatomy, typology and asymmetry. Brain Lang 109:29–48CrossRefPubMed Keller SS, Crow TJ, Foundas AL, Amunts K, Roberts N (2009a) Broca’s area: nomenclature, anatomy, typology and asymmetry. Brain Lang 109:29–48CrossRefPubMed
go back to reference Keller SS, Roberts N, Hopkins WD (2009b) A comparative magnetic resonance imaging study of the anatomy, variability and asymmetry of Broca’s area in the human and chimpanzee brain. J Neurosci 29:14607–14616CrossRefPubMedPubMedCentral Keller SS, Roberts N, Hopkins WD (2009b) A comparative magnetic resonance imaging study of the anatomy, variability and asymmetry of Broca’s area in the human and chimpanzee brain. J Neurosci 29:14607–14616CrossRefPubMedPubMedCentral
go back to reference Keller SS, Deppe M, Herbin M, Gilissen E (2012) Variability and asymmetry of the suclal contours defining Broca’s area homologue in the chimpanzee brain. J Comp Neurol 520:1165–1180CrossRefPubMed Keller SS, Deppe M, Herbin M, Gilissen E (2012) Variability and asymmetry of the suclal contours defining Broca’s area homologue in the chimpanzee brain. J Comp Neurol 520:1165–1180CrossRefPubMed
go back to reference Kevala I, Lewitus E, Huttner WB (2013) The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal. Front Anat 7(16):1–9 Kevala I, Lewitus E, Huttner WB (2013) The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal. Front Anat 7(16):1–9
go back to reference Kochunov PV, Glahn DC, Fox PT, Lancaster JL, Saleem KS, Shelledy W, Zilles K, Thompson PM, Coulon O, Mangin JF, Blangero J, Rogers J (2010) Genetics of primary cerebral gyrification: heritability of length, depth and area of primary sulci in an extended pedigree of Papio baboons. Neuroimage 53(3):1126–1134CrossRefPubMed Kochunov PV, Glahn DC, Fox PT, Lancaster JL, Saleem KS, Shelledy W, Zilles K, Thompson PM, Coulon O, Mangin JF, Blangero J, Rogers J (2010) Genetics of primary cerebral gyrification: heritability of length, depth and area of primary sulci in an extended pedigree of Papio baboons. Neuroimage 53(3):1126–1134CrossRefPubMed
go back to reference LeRoy F, Cai Q, Bogart SL, Dubois J, Coulon O, Monzalvo K, Fischer C, Glasel H, Van der Haegen L, Benezit A, Lin CP, Kennedy DN, Ihara AS, Hertz-Pannier L, Moutard ML, Poupon C, Brysbaert M, Roberts N, Hopkins WD, Mangin JF, Dehaene-Lambertz G (2015) New human-specific brain landmark: the depth asymmetry of superior temporal sulcus. Proc Natl Acad Sci LeRoy F, Cai Q, Bogart SL, Dubois J, Coulon O, Monzalvo K, Fischer C, Glasel H, Van der Haegen L, Benezit A, Lin CP, Kennedy DN, Ihara AS, Hertz-Pannier L, Moutard ML, Poupon C, Brysbaert M, Roberts N, Hopkins WD, Mangin JF, Dehaene-Lambertz G (2015) New human-specific brain landmark: the depth asymmetry of superior temporal sulcus. Proc Natl Acad Sci
go back to reference Luders E, Narr KL, Thompson PM, Rex DE, Woods RP, DeLuca H, Jancke L, Toga AW (2006) Gender effects on cortial thickness and the influence of scaling. Hum Brain Mapp 27:314–324CrossRefPubMed Luders E, Narr KL, Thompson PM, Rex DE, Woods RP, DeLuca H, Jancke L, Toga AW (2006) Gender effects on cortial thickness and the influence of scaling. Hum Brain Mapp 27:314–324CrossRefPubMed
go back to reference McBride T, Arnold SE, Gur RC (1999) A comparative volumetric analysis of the prefrontal cortex in human and baboon MRI. Brain Behav Evol 54:159–166CrossRefPubMed McBride T, Arnold SE, Gur RC (1999) A comparative volumetric analysis of the prefrontal cortex in human and baboon MRI. Brain Behav Evol 54:159–166CrossRefPubMed
go back to reference Rabinowicz T, Dean DE, McFDonald-Comber J, Courten-Myers GM (1999) Gender differences in the human cerebral cortex: more neurons in males, more processes in females. J Child Neurol 14:98–107CrossRefPubMed Rabinowicz T, Dean DE, McFDonald-Comber J, Courten-Myers GM (1999) Gender differences in the human cerebral cortex: more neurons in males, more processes in females. J Child Neurol 14:98–107CrossRefPubMed
go back to reference Rilling JK (2006) Human and non-human primate brains: are they allometrically scaled versions of the same design? Evol Anthropol 15(2):65–77CrossRef Rilling JK (2006) Human and non-human primate brains: are they allometrically scaled versions of the same design? Evol Anthropol 15(2):65–77CrossRef
go back to reference Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223CrossRefPubMed Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223CrossRefPubMed
go back to reference Rilling JK, Seligman RA (2002) A quantitative morphometric comparative analysis of the primate temporal lobe. J Hum Evol 42:505–533CrossRefPubMed Rilling JK, Seligman RA (2002) A quantitative morphometric comparative analysis of the primate temporal lobe. J Hum Evol 42:505–533CrossRefPubMed
go back to reference Rogers J, Kochunov PV, Zilles K, Shelledy W, Lancaster JL, Thompson P, Duggirala R, Blangero J, Fox PT, Glahn DC (2010) On the genetic architecture of cortical folding and brain volume in primates. Neuroimage 53:1103–1108CrossRefPubMedPubMedCentral Rogers J, Kochunov PV, Zilles K, Shelledy W, Lancaster JL, Thompson P, Duggirala R, Blangero J, Fox PT, Glahn DC (2010) On the genetic architecture of cortical folding and brain volume in primates. Neuroimage 53:1103–1108CrossRefPubMedPubMedCentral
go back to reference Schaer M, Cuadra M, Tamarit L, Lazeyras F, Eliez S, Thiran J (2008) A surface based approach to quantify local cortical gyrification. IEEE Trans Med Imaging 27(2):161–170CrossRefPubMed Schaer M, Cuadra M, Tamarit L, Lazeyras F, Eliez S, Thiran J (2008) A surface based approach to quantify local cortical gyrification. IEEE Trans Med Imaging 27(2):161–170CrossRefPubMed
go back to reference Schenker NM, Hopkins WD, Spocter MA, Garrison A, Stimpson CD, Erwin JM, Hof PR, Sherwood CC (2010) Broca’s area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry and comparison to humans. Cereb Cortex 20(3) :730–742CrossRefPubMed Schenker NM, Hopkins WD, Spocter MA, Garrison A, Stimpson CD, Erwin JM, Hof PR, Sherwood CC (2010) Broca’s area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry and comparison to humans. Cereb Cortex 20(3) :730–742CrossRefPubMed
go back to reference Schoenemann PT (2006) Evolution of size and functional areas of the human brain. Annu Rev Anthropol 35:379–406CrossRef Schoenemann PT (2006) Evolution of size and functional areas of the human brain. Annu Rev Anthropol 35:379–406CrossRef
go back to reference Schoenemann PT, Sheehan MJ, Glotzer LD (2005) Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 8(2):242–252CrossRefPubMed Schoenemann PT, Sheehan MJ, Glotzer LD (2005) Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 8(2):242–252CrossRefPubMed
go back to reference Seldon SH (2005) Does brain white matter growth expand the cortex like a balloon? Hypothesis and consequences. Laterality 10(1):81–95PubMed Seldon SH (2005) Does brain white matter growth expand the cortex like a balloon? Hypothesis and consequences. Laterality 10(1):81–95PubMed
go back to reference Semendeferi K, Damasio H (2000) The brain and its main anatomical subdivisions in living hominids using magnetic resonance imaging. J Hum Evol 38:317–332CrossRefPubMed Semendeferi K, Damasio H (2000) The brain and its main anatomical subdivisions in living hominids using magnetic resonance imaging. J Hum Evol 38:317–332CrossRefPubMed
go back to reference Semendeferi K, Damasio H, Frank R, Van Hoesen GW (1997) The evolution of the frontal lobes: a volumetric analysis based on three dimensional reconstructions of the magnetic resonance scans of human and ape brains. J Hum Evol 32:375–388CrossRefPubMed Semendeferi K, Damasio H, Frank R, Van Hoesen GW (1997) The evolution of the frontal lobes: a volumetric analysis based on three dimensional reconstructions of the magnetic resonance scans of human and ape brains. J Hum Evol 32:375–388CrossRefPubMed
go back to reference Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (2001) Prefrontal cortex in humans and apes: a comparative study of area 10. Am J Phys Anthropol 114:224–241CrossRefPubMed Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW (2001) Prefrontal cortex in humans and apes: a comparative study of area 10. Am J Phys Anthropol 114:224–241CrossRefPubMed
go back to reference Semendeferi K, Lu A, Schenker NM, Damasio H (2002) Humans and great apes share a large frontal cortex. Nat Neurosci 5(3):272–276CrossRefPubMed Semendeferi K, Lu A, Schenker NM, Damasio H (2002) Humans and great apes share a large frontal cortex. Nat Neurosci 5(3):272–276CrossRefPubMed
go back to reference Sherwood CC, Broadfield DC, Holloway RL, Gannon PJ, Hof PR (2003) Variability of Broca’s area homologue in great apes: implication for language evolution. Anat Rec 217A:276–285CrossRef Sherwood CC, Broadfield DC, Holloway RL, Gannon PJ, Hof PR (2003) Variability of Broca’s area homologue in great apes: implication for language evolution. Anat Rec 217A:276–285CrossRef
go back to reference Sherwood CC, Holloway RL, Semendeferi K, Hof PR (2005) Is prefrontal white matter enlargement a human evolutionary specialization? Nat Neurosci 8(5):537–538CrossRefPubMed Sherwood CC, Holloway RL, Semendeferi K, Hof PR (2005) Is prefrontal white matter enlargement a human evolutionary specialization? Nat Neurosci 8(5):537–538CrossRefPubMed
go back to reference Sherwood CC, Baurernfeind AL, Bianchi S, Raghanti MA, Hof PR (2012) Human brain evolution writ large and small. In: Hofman MA, Falk D (eds) Progress in brain research. Elsevier, Oxford Sherwood CC, Baurernfeind AL, Bianchi S, Raghanti MA, Hof PR (2012) Human brain evolution writ large and small. In: Hofman MA, Falk D (eds) Progress in brain research. Elsevier, Oxford
go back to reference Stout D, Chaminade T (2012) Stone tools, language and the brain in human evolution. Philos Trans R Soc B Biol Sci 367:75–87CrossRef Stout D, Chaminade T (2012) Stone tools, language and the brain in human evolution. Philos Trans R Soc B Biol Sci 367:75–87CrossRef
go back to reference Uylings H, Jacobsen A, Zilles K, Amunts K (2006) Left–right asymmetry in volume and number of neurons in adult Broca’s area. Cortex 42(4):652–658CrossRefPubMed Uylings H, Jacobsen A, Zilles K, Amunts K (2006) Left–right asymmetry in volume and number of neurons in adult Broca’s area. Cortex 42(4):652–658CrossRefPubMed
go back to reference Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318CrossRefPubMed Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318CrossRefPubMed
go back to reference Zilles K, Armstrong E, Moser KH, Schleicher A, Stephan H (1989) Gyrification in the cerebral cortex of primates. Brain Behav Evol 34:143–150CrossRefPubMed Zilles K, Armstrong E, Moser KH, Schleicher A, Stephan H (1989) Gyrification in the cerebral cortex of primates. Brain Behav Evol 34:143–150CrossRefPubMed
go back to reference Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36(5):275–284CrossRefPubMed Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36(5):275–284CrossRefPubMed
Metadata
Title
Vertex- and atlas-based comparisons in measures of cortical thickness, gyrification and white matter volume between humans and chimpanzees
Authors
William D. Hopkins
Xiang Li
Tim Crow
Neil Roberts
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1213-1

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