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Architectonic Identification of the Core Region in Auditory Cortex Of THEJOURNALOFCOMPARATIVENEUROLOGY441:197–222(2001) ArchitectonicIdentificationoftheCore RegioninAuditoryCortexofMacaques, Chimpanzees,andHumans TROYA.HACKETT,1,3* TODDM.PREUSS,2 ANDJONH.KAAS3 1DepartmentofHearingandSpeechSciences,VanderbiltUniversity, Nashville,Tennessee37203 2CognitiveEvolutionGroup,UniversityofLouisianaatLafayette, NewIberia,Louisiana70560 3DepartmentofPsychology,VanderbiltUniversity,Nashville,Tennessee37203 ABSTRACT Thegoalofthepresentstudywastodeterminewhetherthearchitectoniccriteriausedto identifythecoreregioninmacaquemonkeys(Macacamulatta,M.nemestrina)couldbeusedto identifyahomologousregioninchimpanzees(Pantroglodytes)andhumans(Homosapiens). Currentmodelsofauditorycorticalorganizationinprimatesdescribeacentrallylocatedcore regioncontainingtwoorthreesubdivisionsincludingtheprimaryauditoryarea(AI),asurround- ingbeltofcortexwithperhapssevendivisions,andalateralparabeltregioncomprisedofatleast twofields.Inmonkeysthecoreregioncanbeidentifiedonthebasisofspecificanatomicaland physiologicalfeatures.Inthisstudy,thecorewasidentifiedfromserialsetsofadjacentsections processedforcytoarchitecture,myeloarchitecture,acetylcholinesterase,andcytochromeoxidase. Qualitativeandquantitativecriteriawereusedtoidentifythebordersofthecoreregionin individualsections.Serialreconstructionsofeachbrainweremadeshowingthelocationofthe corewithrespecttogrossanatomicallandmarks.Thepositionofthecorewithrespecttomajor sulciandgyriinthesuperiortemporalregionvariedmostinthechimpanzeeandhuman specimens.Althoughthearchitectonicappearanceofthecoreareasdidvaryincertainrespects acrosstaxonomicgroups,thenumeroussimilaritiesmadeitpossibletoidentifyunambiguously ahomologouscorticalregioninmacaques,chimpanzees,andhumans.J.Comp.Neurol.441: 197–222,2001. ©2001Wiley-Liss,Inc. Indexingterms:comparative;primate;neuroanatomy;neurolinguistics;language;imaging; evolution;acetylcholinesterase;myelin Thesearchforcorticalregionsthatarelargelyorwholly animalstohumansisespeciallyproblematicbecauseex- devotedtoauditoryprocessinghasbeenthesubjectof perimentalconstraintslimitdirectcomparisonsbetween numerousinvestigationsforover125years,leadingtothe species.Oneconsequenceisthatbothbodiesofknowledge identificationofmultipleauditorycorticalfieldsinmost expand,butlittleconnectionismadebetweenthem.As mammalsstudied.Thenumberoffieldsidentifiedranges from1(inmarsupials)toover12(inprimates).Incats,a singleprimaryauditoryfield(AI)issurroundedbyseveral nonprimaryauditoryfields.Inmonkeystwoorthreepri- GrantSponsor:NationalInstitutesofHealth,NIDCDgrantsDC00249 maryfields,includingAI,areenvelopedbyaneven andDC04318;Grantsponsor:theMcDonnell-PewPrograminCognitive greaternumberofnonprimaryfields(forreviews,see Neuroscience;Grantnumber:JSMF98-45;Grantsponsor:theJamesS. McDonnellFoundation;Grantnumber:JSMF20002029;Grantsponsor: WoolseyandWalzl,1982;BruggeandReale,1985;Aitkin, NINDS;Grantnumber:NS16446;Grantsponsor:theNationalInstituteon 1990;Schreiner,1992,1998;Ehret,1997;deRibaupierre, Aging;Grantnumber:NS1P30AG-13854-01. 1997;Rouiller,1997;Kaasetal.,1999;KaasandHackett, *Correspondenceto:TroyA.Hackett,Ph.D.,VanderbiltUniversity,301 st 2000).Currently,onlythehomologyofAIhasbeenwell WilsonHall,11121 AvenueSouth,Nashville,TN37203. E-mail:[email protected] establishedacrossmajortaxonomicgroups.Thus,theex- Received9March2001;Revised17July2001;Accepted17September tenttowhichfindingsinonespeciescanbegeneralizedto 2001 anotherisuncertain.Extendingfindingsfromresearch PublishedonlinetheweekofNovember12,2001 ©2001WILEY-LISS,INC. DOI10.1002/cne.1407 198 T. HACKETT ET AL Fig. 1. Schematic view of the macaque left hemisphere showing region (RP, CP; no shading) occupies the exposed surface of the the location and intrinsic connections of auditory cortex. The dorsal superior temporal gyrus (STG). The core fields project to surrounding bank of the lateral sulcus has been removed (cut) to expose the belt areas (arrows). Inputs to the parabelt arise from the lateral and superior temporal plane (LS ventral bank). The floor and outer bank medial belt subdivisions. Connections between the parabelt and me- of the circular sulcus (CiS) have been flattened to show the medial dial belt fields are not illustrated to improve clarity. Tonotopic gradi- auditory fields. The core region (dark shading) contains three subdi- ents in the core and lateral belt fields are indicated by the letters H visions (AI, R, RT). In the belt region (light shading) seven subdivi- (high frequency) and L (low frequency). For abbreviations, see list. sions are proposed (CM, CL, ML, AL, RTL, RTM, RM). The parabelt this trend continues, the need for studies that attempt to link these findings also grows. Toward this end, we have initiated comparative architectonic studies of auditory Abbreviations cortex in macaque monkeys, chimpanzees, and humans. Our goal is to identify features of auditory cortical orga- AChE acetylcholinesterase AI auditory area I (core) nization that are common, and unique, to each taxonomic AL anterior lateral auditory belt group. AS arcuate sulcus In recent years we have developed a model of auditory ASC caudal CiS circular sulcus cortical organization in nonhuman primates based on a CL caudolateral auditory belt wide range of anatomical and physiological findings CM caudomedial auditory belt (Hackett et al., 1998a; Kaas et al., 1999; Kaas and Hack- CPB caudal parabelt ett, 2000). According to the model, primate auditory cortex CS circular sulcus CSHG Heschl’s gyrus consists of three major regions containing as many as 12 HG1 first (anterior) gyrus of Heschl different fields (Fig. 1). Two or three cochleotopically or- HG2 second (posterior) gyrus of Heschl ganized primary or primary-like auditory areas (AI, R, HSa Heschl’s sulcus (anterior) RT) with independent parallel inputs from the ventral HSp Heschl’s sulcus (posterior) IPS intraparietal sulcus division of the medial geniculate complex (MGv) comprise LS lateral sulcus the core region at a first level of processing. The core fields LuS lunate sulcus are surrounded by a belt region of possibly seven fields LuSMF myelinated fibers (CL, CM, RM, RTM, RTL, AL, ML) at a second level of ML middle lateral auditory belt N Nissl substance processing, with major inputs from the core and the dorsal PS principal sulcus division of the medial geniculate complex (MGd). Co- R rostral area (core) chleotopic organization is preserved in at least some of the RM rostromedial auditory belt belt fields (Rauschecker et al., 1995; Kosaki et al., 1997). RMRPB rostral parabelt RT rostrotemporal area (core) The belt region is bordered laterally on the superior tem- RTL rostrotemporolateral auditory belt poral gyrus by a parabelt region of two or more divisions RTM rostrotemporomedial auditory belt (CP, RP) that are activated by inputs from the belt areas RTLRTMSI sulcus intermedius and the MGd, but not MGv or the core. Neurons in the belt STG superior temporal gyrus STS superior temporal sulcus and parabelt project to auditory-related fields in the tem- TTG transverse temporal gyrus (of Heschl) poral, parietal, and frontal lobes. Experimental evidence IDENTIFICATION OF THE AUDITORY CORE 199 supporting this model is derived from numerous studies of TABLE 1. Histologic Treatment of Macaque, Chimpanzee, and monkeys and chimpanzees (Campbell, 1905; Beck, 1929; Human Brain Specimens1 Walker, 1937; von Bonin, 1938; Ades and Felder, 1942; Postmortem Plane of Bailey et al., 1943; Walzl and Woolsey, 1943; Walzl, 1947; Case Fixation procedure delay section von Bonin and Bailey, 1947; Bailey et al., 1950; Akert et M1–M4 P 4% PBPF 0 Off-coronal A al., 1959; Merzenich and Brugge, 1973; Jones and Burton, M5–M6 P 4% PBPF 0 Coronal Ch1 I 4% PBPF Ͻ12 hr Off-coronal A 1976; Imig et al., 1977; Fitzpatrick and Imig, 1980; Gala- Ch2 P 4% PBPF ϩ 0.1% GA 0 Off-coronal A burda and Pandya, 1983; Aitkin et al., 1988; Luethke et Ch3 P 10% formalin 20 min Off-coronal A Ch4 I 10% formalin 12 hr Off-coronal A al., 1989; Morel and Kaas, 1992; Morel et al., 1993; Jones Hu1 I 4% PBPF 6 hr Off-coronal A et al., 1995; Kosaki et al., 1997; Rauschecker et al., 1997; Hu2 I 2% PBPF Ͻ24 hr Off-coronal A Hackett et al., 1998a,b; Recanzone et al., 2000). Hu3 I 2% PBPF 23 hr Off-coronal B Extension of this model to human auditory cortex can be 1M, macaque; Ch, chimpanzee, Hu, human; P, perfusion; I, immersion; PBPF, done in a limited way by comparing anatomical features. phosphate-buffered paraformaldehyde; GA, glutaraldehyde; off-coronal A, perpendicu- lar to the superior temporal plane and midline; off-coronal B, perpendicular to the Detailed architectonic parcellations of the human audi- superior temporal plane and long axis of the first transverse temporal gyrus. All cortical tory cortex have appeared regularly for nearly a century blocks are left hemisphere. (Campbell, 1905; Brodmann, 1909; Vogt and Vogt, 1919; Flechsig, 1920; von Economo and Koskinas, 1925; Beck, 1928; von Economo, 1929; von Economo and Horn, 1930; Poljak, 1932; Hopf, 1954; Blinkov, 1955; Braak, 1978; tify the core region in monkeys could be used to identify a Galaburda and Sanides, 1980; Seldon 1981a,b, 1982; Ong homologous region in chimpanzees and humans. A prelim- and Garey, 1990; Rademacher et al., 1993; Rivier and inary report of these findings was previously published in Clarke, 1997; Clarke and Rivier, 1998; Morosan et al., abstract form (Hackett et al., 1998c). 2001). Although these parcellations differ from one an- other in many respects, including nomenclature, common MATERIALS AND METHODS features include a centrally located region with anatomi- cal features
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