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Neubert et al., Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas in Monkey Frontal Cortex

Neubert et al., Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas in Monkey Frontal Cortex

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Published by Angel Martorell
Neuron (2014), http://dx.doi.org/10.1016/j.neuron.2013.11.012

This new study from Oxford University researchers suggests a surprising degree of similarity in the organization of brain regions that control language and complex thought processes in humans and monkeys, as well as key differences. The team’s finding demonstrate valuable insights into the evolutionary processes that established the link between humans and other primates and what made humans distinctly different.
Neuron (2014), http://dx.doi.org/10.1016/j.neuron.2013.11.012

This new study from Oxford University researchers suggests a surprising degree of similarity in the organization of brain regions that control language and complex thought processes in humans and monkeys, as well as key differences. The team’s finding demonstrate valuable insights into the evolutionary processes that established the link between humans and other primates and what made humans distinctly different.

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Published by: Angel Martorell on Jan 29, 2014
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01/30/2014

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Neuron
 Article
Comparison of Human Ventral Frontal Cortex Areasfor Cognitive Control and Languagewith Areas in Monkey Frontal Cortex
Franz-Xaver Neubert,
* Rogier B. Mars,
1,2
 Adam G. Thomas,
2,3
Jerome Sallet,
1
and Matthew F.S. Rushworth
1,2
1
Department of Experimental Psychology, University of Oxford, 9 South Parks Road, Oxford OX1 3UD, UK
2
Oxford Centre for Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, Headington,Oxford OX3 9DU, UK
3
Functional MRI Facility, NIMH, National Institutes of Health, Bethesda, MD 20892-1148, USA *Correspondence: franz-xaver.neubert@psy.ox.ac.ukhttp://dx.doi.org/10.1016/j.neuron.2013.11.012
SUMMARY 
Human ventrolateral frontal cortex (vlFC) is identifiedwith cognitive processes such as language andcognitive flexibility. The relationship between it andthevlFCofotherprimateshasthereforebeenthesub- jectofparticularspeculation.Weusedacombinationof structural and functional neuroimaging methodsto identify key components of human vlFC. WecomparedhowvlFCareasinteractedwithotherbrainareasin25humansand25macaquesusingthesamemethods. We identified a core set of 11 vlFC compo-nents that interacted in similar ways with similar distributed circuits in both species and, in addition,one distinctively human component in ventrolateralfrontal pole. Fundamental differences in interactionswith posterior auditory association areas in the twospecies were also present—these were ubiquitousthroughout posterior human vlFC but channeledto different frontal regions in monkeys. Finally, therewere some differences in interregional interactionswithin vlFC in the two species.
INTRODUCTION
The vlFC is identified with cognitive processes pre-eminentin humans such as language and cognitive flexibility. Broca’sarea is a part of left vlFC and is associated with language ( Frie-derici and Gierhan, 2013 ), while other vlFC areas, sometimes inthe right hemisphere, have been linked to cognitive control—high-level top-down control of behavior—by influencing pro-cessing in other brain regions (  Aron, 2007; Brass et al., 2005;Dosenbach et al., 2006; Higo et al., 2011; Neubert et al., 2010 ).Despite vlFC’s identification with such aspects of humancognition, key features of its neuroanatomy, such as cytoarchi-tecture, seem homologous in human and nonhuman primatessuch as the macaque ( Petrides and Pandya, 2002 ). Apparenthomology in neuroanatomy is puzzling when macaques lackcognitive skills that humans possess. There is evidence thatmacaque vlFC is involved in auditory processing ( Romanski,2012 ),orofacial motor control ( Petrideset al.,2005 ), and gesture recognition ( Rizzolatti and Sinigaglia, 2010 ), which might relateto processes necessary for language. However, emphasis hasalso been placed on macaque vlFC’s role in multimodal sensoryintegration ( Passingham and Wise, 2012; Romanski, 2012 ), theselection of environmental features for attention, and theirsubsequent use to guide flexible decision making and actionselection Passingham and Wise, 2012 ). How the macaquebrain areas responsible for these processes relate to areasin human vlFC areas implicated in attention and task controlremains uncertain. An alternative hypothesis is that there are new areas in humanvlFC that support uniquely human cognitive abilities. A recentcytoarchitectonic and receptor-density-based investigationidentifiedpreviouslyunreportedvlFCregionsinlocationsassoci-ated with language and cognitive control (  Amunts et al., 2010 ).It is possible that no corresponding regions exist in monkeysbut no test has been conducted. Alternatively, another aspectof vlFC may differ between species—the interactions that re-gions have with each other and with the rest of the brain. Suchinterconnections and interactions determine the informationthat brain regions have access to and the influence they exert.In the current study we used diffusion-weighted MRI (DW-MRI) parcellation techniques to test the former hypothesis: thepotential existence of new areas in humans. DW-MRI identifiesareas corresponding in position and extent to those identifiedby histological examination ( Mars et al., 2011 ). Another noninva-sive MRI-based technique, resting-state fMRI, was used toexplore the latter hypothesis—that there are interspecies differ-ences in the functional networks vlFC participates in(‘‘functionalconnectivity’[Bullmore and Sporns, 2009]). Functionally con-nected networks observed at rest often overlap with networksobserved during performance of cognitive tasks ( Power et al.,2011 ). Such interregional coupling patterns often partly reflectanatomical connectivity ( O’Reilly et al., 2013 ). Previous studieshave shown that dorsal prefrontal and parietal cortex participatein similar networks in macaques and humans ( Margulies et al.,2009; Mars et al., 2011; Sallet et al., 2013; Vincent et al., 2007 ).Here we tested whether this is true in vlFC.
RESULTS
The first goal was to identify component parts of the entirehuman ventrolateral prefrontal cortex Figure 1 A). There has
Neuron
 81
, 1–14, February 5, 2014
ª
2014 Elsevier Inc.
 1
Please cite this article in press as: Neubert et al., Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas inMonkey Frontal Cortex, Neuron (2014), http://dx.doi.org/10.1016/j.neuron.2013.11.012
 
recently been interest in the existence of specialized brainareas near the border between ventrolateral prefrontal andventral premotor cortex (PMv). To ensure the possibility of investigating them in our study, we took care to include PMvas well as ventrolateral prefrontal cortex within the vlFC regionof interest (ROI; see Figure 2 A). Posteriorly, we delimited theROI by the posterior end of the precentral gyrus to includethe crown of the precentral gyrus but not the rostral bank of the central sulcus. Posterior to the posterior end of the inferiorfrontal sulcus, the ROI was dorsally delimited by what had pre-viously been established to be the border between PMv anddorsal premotor cortex (PMd) ( Tomassini et al., 2007 ). In addi-tion to PMv, we also examined all areas in the pars opercularis,pars trianguris, and pars orbitalis of the inferior frontal gyrus,the whole of the inferior frontal sulcus, and the deep frontaloperculum. Hence our ROI was delimited dorsally by the fusionof the middle frontal gyrus and the inferior frontal sulcus toinclude the whole inferior frontal sulcus. More anteriorly, weincluded all the tissue ventral to a line extending anteriorlyfrom the anterior tip of the inferior frontal sulcus to the mostanterior point in the brain. This line ran along the surface of the brain approximately in the axial plane in the standard Mon-treal Neurological Institute (MNI) coordinate system. Thereby,we probably included part of the frontal pole in this most ante-rior area, and for reasons of completeness we also included amore dorsal region into our ROI identified as frontal pole bySallet et al. (2013). The ROI included both medial and lateralfrontal pole and was medially delimited by the paracingulatesulcus. Ventromedially, the ROI was delimited by the lateralorbital sulcus and more posteriorly at the level of the deep fron-tal operculum by the circular sulcus. The ROI could be definedin an unbiased and easily reproducible way in all subjectsby using the automated gray matter-white matter segmenta-tion tool FAST v4.1 (FMRIB’s Automated Segmentation Tool)Zhang et al., 2001 ) on the MNI standard brain template(MNI_152 template) in combination with these gross anatomical
Figure 1. Overall Approach of the Study 
We used DW-MRI-based tractography in 25 human participants to divide vlFC ROI (A) into regions with consistent connectivity profiles with the rest of the brain.Probabilistic tractography was performed from each voxel in the ROI and yielded a connectivity matrix between all VLFC voxels and each brain voxel for eachparticipant (25 connectivity matrices, four example connectivity matrices in B). These matrices were then used to generate a symmetric cross-correlation matrix,which was then permuted using k-means segmentation for automated clustering to define different clusters (yielding 25 clustered cross-correlation matrices, C).Theseclusterswereprojectedbackontotheindividualparticipant’sbrainandoverlayedontotheMNI152standardbrain(D).fMRIanalysesinthesame25participantsdeterminedfunctionalconnectivitybetweenthesedistinctvlFCregionsandtherestofthebrain(examplefunctionalconnectivitypatternforIFJinblueinE).Werelatedthefunctionalconnectivityfingerprints(F)ofthedifferentvlFCregionstotheresting-statefMRI-basedconnectivityprofilesfromdifferentcytoarchitectonicallydefinedareas in vlFC in 25 macaques (cytoarchitectonically defined macaque’s area 44, D
0
, and respective functional connectivity pattern, E
0
 ).
Neuron
Human and Monkey Ventrolateral Frontal Cortex
2
 Neuron
 81
, 1–14, February 5, 2014
ª
2014 Elsevier Inc.
Please cite this article in press as: Neubert et al., Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas inMonkey Frontal Cortex, Neuron (2014), http://dx.doi.org/10.1016/j.neuron.2013.11.012
 
landmarks. This standard-space ROI was then registered toeach individual brain using nonlinear registration (FMRIB’sNonlinear Image Registration Tool [FNIRT]).Because of potential differences between right and left vlFC,we carried out parallel investigations of both regions definedby the same anatomical criteria. However, we judged results tobe similar enough to focus on right vlFC and to present leftvlFC results only in the Supplemental Information.To identify component vlFC regions, we used DW-MRI-basedtractographyin25healthyhumanparticipants.Weestimatedtheconnections of every vlFC voxel in each subject ( Behrens et al.,2007 ) Figure 1B). The parcellation approach identifies voxels within vlFC ( Figure 1 A) with similar estimated profiles of connec-tivitywiththerestofthebrain.TheconnectivitymatrixFigure1B)isusedtogenerateasymmetriccross-correlationmatrixJohan-sen-Berg et al., 2004 ) reflecting the correlation in connectivitypattern between all vlFC voxels. This cross-correlation matrixis then regrouped using K-means clustering ( Figure 1C) to iden-tify voxels sharing connectivity profiles ( Beckmann et al., 2009;Mars et al., 2011 ). The spatial locations of the voxels in eachparcel are then established; voxels cluster into anatomicallycoherent parcels ( Figure 1D).With the correct number of regions in human vlFC being un-known, we carried out a series of parcellations into two to 25 re-gions. The parcellation into ten distinct regions was particularlyconsistent across subjects and showed the smallest varianceof the average cross-correlation, suggesting that it is the mostcoherent clustering into similarly correlated clusters Supple-mental Experimental Procedures 2 discusses determination of regions). Similar ten-cluster parcellations were obtained in bothleft and right hemispheres. This specific parcellation solution of ten different regions was further corroborated with a second se-ries of parcellations using an iterative procedure ( SupplementalExperimental Procedures 4) similar to the approach used byBeckmann et al. (2009). This iterative parcellation procedureyielded similar ten cluster results. Each of these ten regionswas subsequently subjected to further subparcellation to testwhether a more detailed parcellation of vlFC could be obtained.Two of the ten vlFC regions could reliably be parcellated furtherinto two regions. Therefore, in summary, we identified 12 similarvlFC regions in all our human subjects.The names given to each vlFC region need to be consideredwith caution. One strategy is to avoid naming areas, but wefound this approach renders our findings difficult to communi-cate. Instead, we used names largely based on cross-speciessimilarities in the areas’ connectivity profiles. In several, but notall cases, they can be related to previous cytoarchitectonicand receptor-density-based parcellation schemes  Amuntset al., 2010 ). After parcellation, we used fMRI from the same 25 humans todetermine functional connectivity profiles for each vlFC region.We took the BOLD signal from each area and established whichother voxels had correlated BOLD time courses Figure 1Eshows the example case of areas where the BOLD signal wascorrelated with the inferior frontal junction [IFJ] BOLD signal).We then summarized each vlFC area’s pattern of coupling in aspider plot ( Figure 1F). The spider plot shows the relative degreeof coupling between each vlFC area and a set of target regions.These target regions were chosen because they are thought, onthe basis of anatomical and functional evidence, to correspondbetween humans and macaques and because different vlFCareas were expected to have diagnostically different couplingpatterns with different sets of these target regions. Similarspider plots were calculated for a set of macaque vlFC regionsFigure 1D
0
 ) and the corresponding target areas in other partsof the brain ( Figure 1E
0
 ). Finally Figure 1F), we compared thedissimilarity or ‘‘distance’’ between each human frontal area’scoupling fingerprint and the coupling fingerprint associatedwith each frontal area of the macaque ( Mars et al., 2013; Salletet al., 2013 ).
Figure2. HumanvlFCRegionofInterestandParcellation Solution
(A) The right vlFC ROI. Dorsally it included theinferior frontal sulcus and, more posteriorly, itincluded PMv; anteriorly it was bound by the par-acingulatesulcusandventrallybythelateralorbitalsulcus and the border between the dorsal insulaand the opercular cortex.(B) A schematic depiction of the result of the 12cluster parcellation solution using an iterativeparcellation approach. We subdivided PMv intoventral and dorsal regions (6v and 6r, purple andblack). We delineated the IFJ area (blue) and areas44d (gray) and 44v (red) in lateral pars opercularis.More anteriorly,we delineated areas 45 (orange) inthe pars triangularis and adjacent operculum andIFS (green) in the inferior frontal sulcus and dorsalpars triangularis. We found area 12/47 in the parsorbitalis (light blue) and area Op (yellow) in thedeep frontal operculum. We also identified area 46(bright yellow), and lateral and medial frontal poleregions (FPl and FPm, ruby colored and pink). Seealso Figures S1–S3 and S5.
Neuron
Human and Monkey Ventrolateral Frontal Cortex
Neuron
 81
, 1–14, February 5, 2014
ª
2014 Elsevier Inc.
 3
Please cite this article in press as: Neubert et al., Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas inMonkey Frontal Cortex, Neuron (2014), http://dx.doi.org/10.1016/j.neuron.2013.11.012

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