The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI

232 Pages·2005·20.49 MB·English

by  Henri M. Duvernoy (auth.)

HenriM.Duvernoy,TheHumanHippocampus
Henri M. Duvernoy
The Human
Hippocampus
Functional Anatomy, Vascularization
and Serial Sections with MRI
ThirdEdition
In collaboration with F. Cattin, G. Fatterpekar, Th. Naidich,
Ch.Raybaud,P.Y.Risold,U.SalvoliniandT.Scarabino
DrawingsbyJ.L.Vannson
With260Figures
H. Duvernoy
Anatomie,Universite´deFranche-Comte´
Personaladdress:
ChemindesRelanc¸ons
25000Besanc¸on,France
email:[email protected]
F.Cattin
ServicedeNeuroradiologie,CentreHospitalierUniversitaireJ.Minjoz
25000Besanc¸on,France
Th.NaidichandG.Fatterpekar
TheMountSinaiMedicalCenter
OneGustaveL.LevyPlace,New-York,USA
Ch.Raybaud
HopitaldelaTimone,264rueSaint-Pierre
13385MarseilleCedex05,France
P.Y.Risold
Laboratoired’Histologie,Faculte´deMe´decine
25000Besanc¸on,France
U.Salvolini
InstitutodiRadiologia,Faculta´diMedicina,Universita`Polytecnica
dellaMarche,Ancona,Italia
T.Scarabino
Neurologia,CasaSollevodellaSofferenza
71013SanGiovanniRotondo(FG),Italia
ISBN3-540-23191-9Springer-VerlagBerlinHeidelbergNewYork
LibraryofCongressControlNumber:2004112752
Thisworkissubjecttocopyright.Allrightsarereserved,whetherthewholeorpartofthe
materialisconcerned,specificallytherightsoftranslation,reprinting,reuseofillustrations,
recitation,broadcasting,reproductiononmicrofilmorinanyotherway,andstorageindata
banks.Duplicationofthispublicationorpartsthereofispermittedonlyundertheprovisions
oftheGermanCopyrightLawofSeptember9,1965,initscurrentversion,andpermissionfor
usemustalwaysbeobtainedfromSpringer-Verlag.Violationsareliabletoprosecutionunder
theGermanCopyrightLaw.
Springer-VerlagBerlinHeidelbergNewYork
SpringerisapartofSpringerScience+BusinessMedia
http://www.springeronline.com
©Springer-VerlagBerlinHeidelberg2005
PrintedinGermany
Theuseofgeneraldescriptivenames,registerednames,trademarks,etc.inthispublication
doesnotimply,evenintheabsenceofaspecificstatement,thatsuchnamesareexemptfrom
therelevantprotectivelawsandregulationsandthereforefreeforgeneraluse.
Productliability:Thepublisherscannotguaranteetheaccuracyofanyinformationaboutthe
applicationofoperativetechniquesandmedicationscontainedinthisbook.Ineveryindivid-
ualcasetheusermustchecksuchinformationbyconsultingtherelevantliterature.
CoverDesign:eStudioCalamar,Spain
Typesetting:FotoSatzPfeiferGmbH,D-82166Gräfelfing
Printedonacid-freepaper–24/3150–54 3210
Preface
Sincethefirsteditionofthisbookwaspublished(Duvernoy1988),considerable
advanceshavebeenmade.Theneweditionthereforeincludescurrentconcepts
aboutfunctionsofthehippocampusandastudyofitsexternalandinternalvas-
cularization.Headsectionsandmagneticresonanceimaging(MRI)viewshave
alsobeenaddedtothepreviousatlasofsections.
Thebookisdividedintofivesections,precededbyanintroduction(Chap.1)
andashortcommentonthematerialandmethods(Chap.2).Thefirstsection
(Chap.3)dealsbrieflywiththestructure,functions,andconnectionsofthehip-
pocampus. Thisisfollowed in Chap. 4bya description of the anatomyof the
hippocampusanditsrelationswithadjacentstructures.Thenextsection(Chap.
5)isconcernedwiththevascularizationofthehippocampus,andthefinalsec-
tions(Chap.6and7)aredevotedtosectionalanatomyandMRI.
Thisworkhasbenefittedfromtheinvaluablehelpofmanyofmycolleagues.
Firstofall,IwouldliketoexpressmygratitudetothelateProfessorRogerWar-
wick,whohelpedmeclarifythedifficultdescriptionofhippocampalanatomy.
IwillalsoacknowledgethehelpofDr.F.Cattin,Prof.Ch.Raybaud,Dr.P.Y.Ri-
sold,andthemembersoftheDepartmentofAnatomyinBesanc¸on.
My thanks go to Prof. T. Naidich, Dr. G. Fatterpekar, Prof. U. Salvolini and
Prof.T.Scarabinowhoprovideuswith9.4Tand3.TMRIviews.
MydeepestthankstoMichelGaudronforhissupportaswellasMs.Franc¸oise
GilletandMs.AnneRichard.
ThanksarealsoduetoMs.S.Benko,Ms.G.Schröder,andMr.J.W.Schmidt
(Springer-Verlag,Heidelberg)fortheirsupport.
ThisbookisdedicatedtomywifeOdileandtomysonsCharlesandDavid.
HenriDuvernoy
Contents
1 Introduction ................................................ 1
2 MaterialandMethods ........................................ 3
3 Structure,Functions,andConnections
3.1 PreliminaryRemarks ......................................... 5
3.2 Structure ................................................... 6
3.2.1 CornuAmmonis(HippocampusProper) ........................ 7
3.2.2 GyrusDentatus(FasciaDentata,GyrusInvolutus)................. 8
3.2.3 StructuresJoinedtotheHippocampus .......................... 9
3.3 FunctionsandConnections.................................... 26
3.3.1 LearningandMemory ........................................ 26
3.3.2 EmotionalBehavior .......................................... 32
3.3.3 MotorControl ............................................... 33
3.3.4 Hypothalamus............................................... 33
3.3.5 ComparativeStudies.......................................... 33
4 Anatomy
4.1 PreliminaryRemarks ......................................... 39
4.2 HippocampalBody........................................... 39
4.2.1 IntraventricularPart.......................................... 39
4.2.2 ExtraventricularorSuperficialPart ............................. 40
4.2.3 RelationswithAdjacentStructures.............................. 40
4.3 HippocampalHead........................................... 41
4.3.1 IntraventricularPart.......................................... 41
4.3.2 ExtraventricularorUncalPart ................................. 41
4.3.3 RelationsoftheUncuswithAdjacentStructures................... 42
4.4 HippocampalTail ............................................ 43
4.4.1 IntraventricularPart.......................................... 43
4.4.2 ExtraventricularPart ......................................... 43
4.4.3 RelationswithAdjacentStructures.............................. 44
4.5 GeneralFeatures ............................................. 45
5 Vascularization
5.1 Superficial(Leptomeningeal)BloodVessels ...................... 73
5.1.1 SuperficialHippocampalArteries .............................. 73
5.1.2 SuperficialHippocampalVeins ................................. 74
5.2 Intrahippocampal(Deep)BloodVessels ......................... 75
5.2.1 IntrahippocampalArteries .................................... 75
5.2.2 IntrahippocampalVeins....................................... 76
5.2.3 HippocampalHead........................................... 76
5.2.4 VascularNetwork ............................................ 76
VIII Contents
6 Coronal,SagittalandAxialSectionsoftheHippocampus
ShowingitsRelationshipswiththeSurroundingStructures
(afterintravascularIndiainkinjection) .......................... 109
7 SectionalAnatomyandMagneticResonanceImaging
7.1 CoronalSections ............................................. 129
7.2 SagittalSections .............................................. 165
7.3 AxialSections................................................ 193
References ...................................................... 219
Index .......................................................... 226
CHAPTER 1
Introduction
Theaimofthisstudyistogiveaprecisedescription Thiscuriousterminologymayderivefromacom-
of human hippocampal anatomy in view of neuro- parison between the sea horse and the mythical
surgicalprogressandthewealthofmedicalimaging animalthatissupposedtohavedrawnPoseidon’s
methodsavailable.Twomajorproblemsrenderthis chariotoverthesea.Theposteriorpartofthisan-
study more difficult: (1)thecomplexityof thehip- imal is shaped like a fish, and the anterior part,
pocampalstructure,makingitoneofthemostmys- which is like a horse, has two feet folded back;
terious regions in the central nervous system, and each foot was compared to the intraventricular
(2)thegreatconfusionwhichplaguesitsterminolo- reliefofthetemporalhorn,hencetheappearance
gy, a confusion which appeared in the earliest de- oftheterm“peshippocampi.”Theendofthisfoot
scriptions. waswebbed,liketheenlargedanteriorendofthe
Fromamongthosewhohavestudiedthehistory intraventricular hippocampus or “digitationes
ofhippocampalterminology(e.g.,Tilney1939;Ben- hippocampi.”
ninghoff 1940; Klinger 1948; Clara 1959; Meyer
1971),theviewsofLewis(1923)havebeenchosento To complicate matters, the hippocampus was then
besummarizedhere. describedashavingtwofeet:peshippocampimajor
The first description of the hippocampus was forthehippocampusandpeshippocampiminorfor
written by Arantius in 1587 (cited in Lewis 1923), the calcar avis, a bulge in the occipital horn. The
who compared the protrusion on the floor of the terms “large hippocampus” and “small hippocam-
temporalhorntoahippocampus,orseahorse(see pus”havesometimesbeenusedforthesetwostruc-
Fig.3).Itshouldbenoted,however,thathehesitated tures.
between the terms “sea horse” and “silkworm.” In In current usage, the terms “cornu Ammonis”
1729,J.G.Duvernoy(citedinLewis1923)firstillus- and“peshippocampi”areoftenregardedassynony-
trated the hippocampus and he, too, hesitated be- mous (Kopsch 1940), although the latter is some-
tween “hippocampus” and “silkworm.” In 1732, times reserved for the digitationes hippocampi,
Winslow suggested the term “ram’s horn” (see which raise the anterior end of the hippocampus
Winslow 1752). Hippocampus, silkworm, and ram’s (Williams1995).
hornwerethusthetermsusedattheendofthisini- Aftertheseperiodsofconfusion,theterminology
tialperiod,allbasedontheintraventricularappear- that is currently most commonly used needs to be
anceofthehippocampus. clarified.Thenamehippocampusappliestotheen-
A second period was characterized by an exces- tire ventricular protrusion. Thus the hippocampus
siveimageryamonganatomists,whocomparedthe comprisestwocorticallaminaerolleduponeinside
hippocampustomythologicalsymbols: theother:thecornuAmmonisandthegyrusdenta-
tus(seeFig.5).Thesubiculum,ortransitionalcor-
– The“ram’shorn”becamethecornuAmmonis,af-
texbetweenthecornuAmmonisandtherestofthe
ter the Egyptian god Ammon (Ammun Kneph).
temporal lobe, is sometimes viewed as part of the
This name, probably first used by De Garengeot
hippocampus,constitutingafunctionalunit(Chro-
(1742;citedbyLewis1923),hasremainedinuse.
nister and White 1975). However, since the hippo-
– Thetermpeshippocampiwasintroducednext,al-
campusandsubiculumdonotformadistincttopo-
though it is not known who added “foot” to the
graphicalunit,thesubiculumisnotincludedinthis
hippocampus. Lewis (1923) cites Diemerbroeck
study.
(1672), while others have challenged this claim.
CHAPTER 2
Material and Methods
Sixtyhippocampiwereexamined,theaverageageof ion,thismethodoftotalvascularinjectionofthe
the brains being 57 years (range, 19–85 years). To brainthroughthemainarterialtrunksisthebest
simplifythisaccount,thehemispherestudied(right waytoobtainagoodviewnotonlyofthearteries,
orleft)andthesexofthesubjectitwastakenfrom but also of the capillaries and, in particular, the
were omitted; previous studies have shown no dif- veins.Intheliterature,thecerebralveinshaveal-
ferences stemming from the particular techniques waysbeenstudiedbyspecificretrogradevenous
used(Manietal.1986). injections. Using this last method, however, it is
Thebrainswereremovedbetween5and12hafter rarelypossibletoobtaingoodfillingofthevenous
death and were fixed in a 10% formalin solution. tree.ThemethodofintravascularIndiainkinjec-
Mosthadalreadyreceivedanintravascularinjection tionpermitsthevascularanatomytobeobserved
ofIndiaink.Inthefollowing,thespecificmethods inthreedifferentways:
usedineachchapteraredescribed. a)Observation of the superficial (leptomeningeal)
InChaps.3and4onthestructureandanatomyof vessels. The superficial vessels were dissected
thehippocampus,twomethodswereused: withthehelpofanoperatingmicroscope.Arter-
ies and veins were identified, and the point of
1.Dissectionofthehippocampus.Withthehelpofan
penetration of arteries and emergence of veins
operatingmicroscope, the hippocampus was ex-
noted(16hemisphereswereusedforthisstudy).
aminedafterablationofbloodvesselsandlepto-
Thepreparationswerethenphotographedwhile
meninges. The temporal horn was opened, and
immersedindistilledwatertopreventreflection
thechoroidplexusesremovedtoinspecttheven-
andbubbles.
tricularaspectofthehippocampus.
b)Identificationofthedeeppathofintrahippocam-
2.Bodian’smethodofsilverimpregnation.Afterfix-
palarteriesandveins.Blocks3–4mmthickwere
ationinformalin,thehippocampuswascutinto
cutandclearedusingtheSpalteholztechnique(a
sections of 10–20 µm and then impregnated by
mixture of methyl salicylate and benzyl benzo-
thesilverproteinatemethod.Thismethodisap-
ate).Thesuperficialarteriesandveinsidentified
plicableafterintravascularinjection,andacorre-
duringtheprecedingstepwerefollowedintothe
lationcanthusbeestablishedbetweentheneural
hippocampaltissue.Bythismethod,itispossible
architectureandthevascularnetwork.Compared
to recognize the intrahippocampal arteries and
with the usualstaining by cresyl violet, Bodian’s
veinsandtofollowthemalongtheirentirecourse.
techniquehastheadvantageofshowingnotonly
c)Thicksections.Afterfixation,thebrainswerecut
neuronal somata, but also their processes. Con-
intocoronal,sagittal,oraxialsectionsinrelation
versely,andduetodensityofimpregnation,pho-
to the bicommissural plane linking the middle
tographsoflargeareasshowinsufficientcontrast
part of the anterior and posterior commissures.
andareoflittleuse.
Sections(500µmthick)weremadeafterdehydra-
tion, immersion in toluene, and embedding in
InChap.5onthehippocampalvascularization,two
paraffin.Toobtainthicksectionswithoutcracks,
methodswereapplied:
theblockwasheatedbetweeneachcut.Sections
1.Intravascular injection of India ink. Once the werethenmountedonslidesingelatinanddried
brainhadbeenremoved,400ccIndiainksolution under pressure. This method provides a picture
dilutedbydistilledwaterto50%wasinjectedinto of the total cerebral vascular pattern (Chap. 6)
the carotid and vertebral arteries. Gelatin and allows the intrahippocampal vascular net-
(5%–10%)wasaddedtothemixture.Inouropin- worktobestudied.However,thepossibledefor-
4 Chapter2 MaterialandMethods
mationofthenervoustissueduetoconsiderable InChap.7onsectionalanatomy,eachplateincludes
shrinkage following immersion in alcohols and severalfigures:
toluenemustbetakeninaccount.Thicksections
1.A three-dimensional section of the hippocampus.
facilitatetheidentificationofcerebralstructures
Theprincipleofthismethodistograduallyerode
according to differences in the vascular density.
thehemispherebysectioningitfromanteriorto
Whiteandgreysubstancesareclearlydifferenti-
posteriorforcoronalsections,frommedialtolat-
ated. In addition, the grey matter nuclei do not
eralforsagittalsections,andfromsuperiortoin-
have a vascular network of equal density. This
ferior for axial sections. Eroded tissue is dis-
technique has already been used to study the
carded, and the newly exposed surface of the
vascularizationofcircumventricularorgansand
hemisphere is observed for the purpose of ana-
brain stem, cerebral, cerebellar cortices and pi-
tomicalanalysis.
neal gland (Duvernoy 1972, 1975, 1978, 1995a,
2.Aheadsection
1999a,b; Duvernoy and Koritke 1964, 1965; Du-
3.OneorseveralMRIviews
vernoyetal.1969,1971,1972,1981,1983,2000).
Thebicommissuralplaneactedasareferenceforall
2.Intravascular injection with low-viscosity resin
thesesections.The3TMRIviewswereprovidedby
(Mercox). This technique was used to complete
Prof.U.SalvoliniandProf.T.Scarabino.Prof.T.Nai-
theobservationofthevesselscarriedoutbyintra-
dich and Dr. G. Fatterpekar supplied us with the
vascularinjectionofIndiaink.Aftertotalvascu-
9.4Tviewsobtainedfromanatomicalpreparation.
larinjectionofthebrainwiththeresin(Mercox),
thetissuesweredestroyed,andthecastofthevas-
cular network was examined with a scanning
electronmicroscope.Thusaccurateobservations
ofthefinevascularnetworkanditsspatialorga-
nizationbecamepossible.