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Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans.

Wilson B, Kikuchi Y, Sun L, Hunter D, Dick F, Smith K, Thiele A, Griffiths TD, Marslen-Wilson WD, Petkov CI - Nat Commun (2015)

Bottom Line: An evolutionary account of human language as a neurobiological system must distinguish between human-unique neurocognitive processes supporting language and evolutionarily conserved, domain-general processes that can be traced back to our primate ancestors.Neuroimaging studies across species may determine whether candidate neural processes are supported by homologous, functionally conserved brain areas or by different neurobiological substrates.These regions are also known to be associated with initial stages of human syntactic processing.

View Article: PubMed Central - PubMed

Affiliation: Institute of Neuroscience, Henry Wellcome Building, Newcastle University, Framlington Place, Newcastle upon Tyne, NE2 4HH, UK.

ABSTRACT
An evolutionary account of human language as a neurobiological system must distinguish between human-unique neurocognitive processes supporting language and evolutionarily conserved, domain-general processes that can be traced back to our primate ancestors. Neuroimaging studies across species may determine whether candidate neural processes are supported by homologous, functionally conserved brain areas or by different neurobiological substrates. Here we use functional magnetic resonance imaging in Rhesus macaques and humans to examine the brain regions involved in processing the ordering relationships between auditory nonsense words in rule-based sequences. We find that key regions in the human ventral frontal and opercular cortex have functional counterparts in the monkey brain. These regions are also known to be associated with initial stages of human syntactic processing. This study raises the possibility that certain ventral frontal neural systems, which play a significant role in language function in modern humans, originally evolved to support domain-general abilities involved in sequence processing.

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Related in: MedlinePlus

Macaque ROI results.(a) Bilateral anatomically defined ROIs used for analyses: blue comprises anatomical areas 44 and 45; green comprises adjacent vFOC areas, including anatomical areas PrCO, dysgranular insula and area 6v (Methods). Somatosensory and gustatory regions, and area 12 (orbital frontal cortex) were excluded. (b–g) Normalized mean fMRI response differences (violation versus consistent) in the vFOC and Areas 44/45 regions-of-interest shown by hemisphere in each of the macaques. Details of statistical analyses: One-sample t-tests with Bonferroni correction, in Monkey 1, left vFOC: t366=3.827, P<0.001; right vFOC: t404=4.155, P<0.001; Monkey 2, left vFOC: t658=2.401, P=0.034; right vFOC: t702=12.052, P<0.001; Monkey 3, left vFOC: t632=1.523, P=0.256; right vFOC: t658=3.818, P<0.001. Two-sample t-tests, between hemispheres in vFOC, in Monkey 1: t770=1.279, P=0.201; Monkey 2: t1360=5.771, P<0.001; Monkey 3: t1290=1.839, P=0.066. One-sample t-tests with Bonferroni correction, in Monkey 1, left areas 44/45: t192=8.000, P<0.001; right areas 44/45: t181=2.438, P=0.032; Monkey 2, left areas 44/45: t276=0.05, P=1.0; right areas 44/45: t282=2.372, P=0.036; Monkey 3, left areas 44/45: t265=0.583, P=0.561; right areas 44/45: t270=0.331, P=0.741. Two-sample t-tests, between hemispheres in areas 44/45, in Monkey 1: t373=0.977, P=0.329; Monkey 2: t558=1.556, P<0.120; Monkey 3: t535=0.653, P=0.514, see also Supplementary Figs 5 and 6. Symbols: n.s.,not significant; *P<0.05; **P<0.01; ***P<0.001.
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f3: Macaque ROI results.(a) Bilateral anatomically defined ROIs used for analyses: blue comprises anatomical areas 44 and 45; green comprises adjacent vFOC areas, including anatomical areas PrCO, dysgranular insula and area 6v (Methods). Somatosensory and gustatory regions, and area 12 (orbital frontal cortex) were excluded. (b–g) Normalized mean fMRI response differences (violation versus consistent) in the vFOC and Areas 44/45 regions-of-interest shown by hemisphere in each of the macaques. Details of statistical analyses: One-sample t-tests with Bonferroni correction, in Monkey 1, left vFOC: t366=3.827, P<0.001; right vFOC: t404=4.155, P<0.001; Monkey 2, left vFOC: t658=2.401, P=0.034; right vFOC: t702=12.052, P<0.001; Monkey 3, left vFOC: t632=1.523, P=0.256; right vFOC: t658=3.818, P<0.001. Two-sample t-tests, between hemispheres in vFOC, in Monkey 1: t770=1.279, P=0.201; Monkey 2: t1360=5.771, P<0.001; Monkey 3: t1290=1.839, P=0.066. One-sample t-tests with Bonferroni correction, in Monkey 1, left areas 44/45: t192=8.000, P<0.001; right areas 44/45: t181=2.438, P=0.032; Monkey 2, left areas 44/45: t276=0.05, P=1.0; right areas 44/45: t282=2.372, P=0.036; Monkey 3, left areas 44/45: t265=0.583, P=0.561; right areas 44/45: t270=0.331, P=0.741. Two-sample t-tests, between hemispheres in areas 44/45, in Monkey 1: t373=0.977, P=0.329; Monkey 2: t558=1.556, P<0.120; Monkey 3: t535=0.653, P=0.514, see also Supplementary Figs 5 and 6. Symbols: n.s.,not significant; *P<0.05; **P<0.01; ***P<0.001.

Mentions: These effects were further evaluated using planned region of interest (ROI) analyses. First, separate ROIs for the vFOC (vFOC, green ROI in Fig. 3a) and the adjacent areas 44/45 (blue ROI in Fig. 3a) were defined using accepted stereotactic coordinates for these regions in a macaque anatomical atlase (Methods). The vFOC ROI included ventral frontal cortical areas adjacent and inferior to areas 44/45, including the frontal operculum, ventral BA6v and dysgranular insular cortex, but excluding areas 44/45, much of area 47/12c (ref. 40) and all of area 49. A voxel-based repeated measures (RM) analysis of variance (ANOVA) was used to evaluate effects in the ROIs with the factors: Condition (consistent and violation sequences); ROI (vFOC, areas 44/45); Hemisphere (left, right); and Monkey (three levels). A significant main effect of condition (F1,4886=108.1, P<0.001) showed increased activation to violation relative to consistent sequences in these ROIs. There was no significant interaction between condition and ROI (F1,4886=1.149, P=0.284), suggesting that although macaque vFOC is strongly sensitive to sequence violations, and consistently so across the three animals, areas 44/45 are also involved to some extent. Regarding the lateralization of results, there was no significant interaction between Condition and Hemisphere (F1,4886=3.37, P=0.07), suggesting that the effects in these areas are not significantly lateralized to either hemisphere (see Supplementary Note 3 for a summary of lateralisation results). These analyses were complemented with analyses of the results in each of the animals individually (Fig. 3b–g). The individual animal results recapitulated the overall findings, showing significant activation to violation sequences relative to consistent sequences in the vFOC in all of the animals, and that statistically significant activation was also observed in areas 44/45 in two of the three macaques.


Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans.

Wilson B, Kikuchi Y, Sun L, Hunter D, Dick F, Smith K, Thiele A, Griffiths TD, Marslen-Wilson WD, Petkov CI - Nat Commun (2015)

Macaque ROI results.(a) Bilateral anatomically defined ROIs used for analyses: blue comprises anatomical areas 44 and 45; green comprises adjacent vFOC areas, including anatomical areas PrCO, dysgranular insula and area 6v (Methods). Somatosensory and gustatory regions, and area 12 (orbital frontal cortex) were excluded. (b–g) Normalized mean fMRI response differences (violation versus consistent) in the vFOC and Areas 44/45 regions-of-interest shown by hemisphere in each of the macaques. Details of statistical analyses: One-sample t-tests with Bonferroni correction, in Monkey 1, left vFOC: t366=3.827, P<0.001; right vFOC: t404=4.155, P<0.001; Monkey 2, left vFOC: t658=2.401, P=0.034; right vFOC: t702=12.052, P<0.001; Monkey 3, left vFOC: t632=1.523, P=0.256; right vFOC: t658=3.818, P<0.001. Two-sample t-tests, between hemispheres in vFOC, in Monkey 1: t770=1.279, P=0.201; Monkey 2: t1360=5.771, P<0.001; Monkey 3: t1290=1.839, P=0.066. One-sample t-tests with Bonferroni correction, in Monkey 1, left areas 44/45: t192=8.000, P<0.001; right areas 44/45: t181=2.438, P=0.032; Monkey 2, left areas 44/45: t276=0.05, P=1.0; right areas 44/45: t282=2.372, P=0.036; Monkey 3, left areas 44/45: t265=0.583, P=0.561; right areas 44/45: t270=0.331, P=0.741. Two-sample t-tests, between hemispheres in areas 44/45, in Monkey 1: t373=0.977, P=0.329; Monkey 2: t558=1.556, P<0.120; Monkey 3: t535=0.653, P=0.514, see also Supplementary Figs 5 and 6. Symbols: n.s.,not significant; *P<0.05; **P<0.01; ***P<0.001.
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f3: Macaque ROI results.(a) Bilateral anatomically defined ROIs used for analyses: blue comprises anatomical areas 44 and 45; green comprises adjacent vFOC areas, including anatomical areas PrCO, dysgranular insula and area 6v (Methods). Somatosensory and gustatory regions, and area 12 (orbital frontal cortex) were excluded. (b–g) Normalized mean fMRI response differences (violation versus consistent) in the vFOC and Areas 44/45 regions-of-interest shown by hemisphere in each of the macaques. Details of statistical analyses: One-sample t-tests with Bonferroni correction, in Monkey 1, left vFOC: t366=3.827, P<0.001; right vFOC: t404=4.155, P<0.001; Monkey 2, left vFOC: t658=2.401, P=0.034; right vFOC: t702=12.052, P<0.001; Monkey 3, left vFOC: t632=1.523, P=0.256; right vFOC: t658=3.818, P<0.001. Two-sample t-tests, between hemispheres in vFOC, in Monkey 1: t770=1.279, P=0.201; Monkey 2: t1360=5.771, P<0.001; Monkey 3: t1290=1.839, P=0.066. One-sample t-tests with Bonferroni correction, in Monkey 1, left areas 44/45: t192=8.000, P<0.001; right areas 44/45: t181=2.438, P=0.032; Monkey 2, left areas 44/45: t276=0.05, P=1.0; right areas 44/45: t282=2.372, P=0.036; Monkey 3, left areas 44/45: t265=0.583, P=0.561; right areas 44/45: t270=0.331, P=0.741. Two-sample t-tests, between hemispheres in areas 44/45, in Monkey 1: t373=0.977, P=0.329; Monkey 2: t558=1.556, P<0.120; Monkey 3: t535=0.653, P=0.514, see also Supplementary Figs 5 and 6. Symbols: n.s.,not significant; *P<0.05; **P<0.01; ***P<0.001.
Mentions: These effects were further evaluated using planned region of interest (ROI) analyses. First, separate ROIs for the vFOC (vFOC, green ROI in Fig. 3a) and the adjacent areas 44/45 (blue ROI in Fig. 3a) were defined using accepted stereotactic coordinates for these regions in a macaque anatomical atlase (Methods). The vFOC ROI included ventral frontal cortical areas adjacent and inferior to areas 44/45, including the frontal operculum, ventral BA6v and dysgranular insular cortex, but excluding areas 44/45, much of area 47/12c (ref. 40) and all of area 49. A voxel-based repeated measures (RM) analysis of variance (ANOVA) was used to evaluate effects in the ROIs with the factors: Condition (consistent and violation sequences); ROI (vFOC, areas 44/45); Hemisphere (left, right); and Monkey (three levels). A significant main effect of condition (F1,4886=108.1, P<0.001) showed increased activation to violation relative to consistent sequences in these ROIs. There was no significant interaction between condition and ROI (F1,4886=1.149, P=0.284), suggesting that although macaque vFOC is strongly sensitive to sequence violations, and consistently so across the three animals, areas 44/45 are also involved to some extent. Regarding the lateralization of results, there was no significant interaction between Condition and Hemisphere (F1,4886=3.37, P=0.07), suggesting that the effects in these areas are not significantly lateralized to either hemisphere (see Supplementary Note 3 for a summary of lateralisation results). These analyses were complemented with analyses of the results in each of the animals individually (Fig. 3b–g). The individual animal results recapitulated the overall findings, showing significant activation to violation sequences relative to consistent sequences in the vFOC in all of the animals, and that statistically significant activation was also observed in areas 44/45 in two of the three macaques.

Bottom Line: An evolutionary account of human language as a neurobiological system must distinguish between human-unique neurocognitive processes supporting language and evolutionarily conserved, domain-general processes that can be traced back to our primate ancestors.Neuroimaging studies across species may determine whether candidate neural processes are supported by homologous, functionally conserved brain areas or by different neurobiological substrates.These regions are also known to be associated with initial stages of human syntactic processing.

View Article: PubMed Central - PubMed

Affiliation: Institute of Neuroscience, Henry Wellcome Building, Newcastle University, Framlington Place, Newcastle upon Tyne, NE2 4HH, UK.

ABSTRACT
An evolutionary account of human language as a neurobiological system must distinguish between human-unique neurocognitive processes supporting language and evolutionarily conserved, domain-general processes that can be traced back to our primate ancestors. Neuroimaging studies across species may determine whether candidate neural processes are supported by homologous, functionally conserved brain areas or by different neurobiological substrates. Here we use functional magnetic resonance imaging in Rhesus macaques and humans to examine the brain regions involved in processing the ordering relationships between auditory nonsense words in rule-based sequences. We find that key regions in the human ventral frontal and opercular cortex have functional counterparts in the monkey brain. These regions are also known to be associated with initial stages of human syntactic processing. This study raises the possibility that certain ventral frontal neural systems, which play a significant role in language function in modern humans, originally evolved to support domain-general abilities involved in sequence processing.

Show MeSH
Related in: MedlinePlus