Limits...
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.

Show MeSH

Related in: MedlinePlus

Macaque brain regions sensitive to sequence ordering violations.Statistical parametric maps of sensitivity to sequence violations (contrast: violation versus consistent) displayed in each of the three macaques (a–c) and in a majority consensus voxel-overlap map (d), all P<0.05 cluster corrected (see Methods). Results are displayed on rendered lateral and medial surface representations transformed to a standard monkey brain in register with a macaque stereotactic atlas (Methods); light grey: gyri; dark grey: sulci. A, anterior; D, dorsal; P, posterior; V, ventral, see also Supplementary Figs 5 and 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4660034&req=5

f2: Macaque brain regions sensitive to sequence ordering violations.Statistical parametric maps of sensitivity to sequence violations (contrast: violation versus consistent) displayed in each of the three macaques (a–c) and in a majority consensus voxel-overlap map (d), all P<0.05 cluster corrected (see Methods). Results are displayed on rendered lateral and medial surface representations transformed to a standard monkey brain in register with a macaque stereotactic atlas (Methods); light grey: gyri; dark grey: sulci. A, anterior; D, dorsal; P, posterior; V, ventral, see also Supplementary Figs 5 and 6.

Mentions: Functional MRI was used to reveal the brain regions associated with detecting sequence ordering violations in macaques and humans. Three rhesus macaques were first exposed to a representative set of consistent sequences (Fig. 1a), allowing them to implicitly learn the statistical properties of those sequences1416 (Supplementary Figs 2 and 3). After the exposure phase, the macaques were then scanned with fMRI as they listened to testing sequences that were consistent with or that violated the rule-based ordering relationships (Fig. 1a; Methods). Figure 2 shows the brain regions sensitive to the violation sequences for each animal (contrast: violation versus consistent, see Methods and Supplementary Note 2) mapped onto a surface-rendered standard macaque template brain. Several significant clusters (P<0.05, cluster corrected) occurred in corresponding anatomical regions across the animals. Regions sensitive to sequence violations in all three animals included right ventral frontal cortex, involving opercular and dysgranular insular cortex, ventral to Areas 44/45 (Fig. 2). Even in monkey 3 (M3), who shows the more restricted pattern of activation of the three monkeys (Fig. 2c), there is clear engagement of the dysgranular insula in the frontal operculum (Supplementary Fig. 4). In a majority of the animals significant clusters of activation were also observed in additional ventral frontal regions (surrounding and including ventral area 6v), the anterior temporal lobe (for example, area TS2), and posterior parietal cortex area 7 (see Table 1 for a list of all the significantly activated brain areas).


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 brain regions sensitive to sequence ordering violations.Statistical parametric maps of sensitivity to sequence violations (contrast: violation versus consistent) displayed in each of the three macaques (a–c) and in a majority consensus voxel-overlap map (d), all P<0.05 cluster corrected (see Methods). Results are displayed on rendered lateral and medial surface representations transformed to a standard monkey brain in register with a macaque stereotactic atlas (Methods); light grey: gyri; dark grey: sulci. A, anterior; D, dorsal; P, posterior; V, ventral, see also Supplementary Figs 5 and 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4660034&req=5

f2: Macaque brain regions sensitive to sequence ordering violations.Statistical parametric maps of sensitivity to sequence violations (contrast: violation versus consistent) displayed in each of the three macaques (a–c) and in a majority consensus voxel-overlap map (d), all P<0.05 cluster corrected (see Methods). Results are displayed on rendered lateral and medial surface representations transformed to a standard monkey brain in register with a macaque stereotactic atlas (Methods); light grey: gyri; dark grey: sulci. A, anterior; D, dorsal; P, posterior; V, ventral, see also Supplementary Figs 5 and 6.
Mentions: Functional MRI was used to reveal the brain regions associated with detecting sequence ordering violations in macaques and humans. Three rhesus macaques were first exposed to a representative set of consistent sequences (Fig. 1a), allowing them to implicitly learn the statistical properties of those sequences1416 (Supplementary Figs 2 and 3). After the exposure phase, the macaques were then scanned with fMRI as they listened to testing sequences that were consistent with or that violated the rule-based ordering relationships (Fig. 1a; Methods). Figure 2 shows the brain regions sensitive to the violation sequences for each animal (contrast: violation versus consistent, see Methods and Supplementary Note 2) mapped onto a surface-rendered standard macaque template brain. Several significant clusters (P<0.05, cluster corrected) occurred in corresponding anatomical regions across the animals. Regions sensitive to sequence violations in all three animals included right ventral frontal cortex, involving opercular and dysgranular insular cortex, ventral to Areas 44/45 (Fig. 2). Even in monkey 3 (M3), who shows the more restricted pattern of activation of the three monkeys (Fig. 2c), there is clear engagement of the dysgranular insula in the frontal operculum (Supplementary Fig. 4). In a majority of the animals significant clusters of activation were also observed in additional ventral frontal regions (surrounding and including ventral area 6v), the anterior temporal lobe (for example, area TS2), and posterior parietal cortex area 7 (see Table 1 for a list of all the significantly activated brain areas).

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