Stereotaxic brain atlas of the prosimian primate Galago senegalensis

Stereotaxic brain atlasof the prosimian primate Galago senegalensis*

by

J. C. ORSINI 0), A. CHRISTOLOMME (2), M. DUPE-GODETand D. RICHE (3)

Get atlas comporte trente et une sections frontales du cerveau anterieur, situees entreles colliculus inferieurs et les bulbes olfactifs. Son utilisation est prSvue pour des animauxadultes, males et femeiles, presentant un poids de 190 a 240 g et une distance bregma-lambda de 17,0 a 17,5 mm.

Un dispositif adaptable a un appareil storootaxique pour Rat et permettant de fixerle cräne de Galago senegalensis, est decrit dans Introduction. Les reperes osseux utilisessont les rebords inferieurs des orbites et les conduits auditifs externes. Le zero de refe-rence est situe dans le plan sagittal, 5 mm au-dessus de la ligne interauriculaire.

INTRODUCTION

Galago senegalensis, commonly called "the lesser bushbaby", is a pro-simian primate (infra-order of Lorisiformes, family of Lorisidae, according toNapier and Napier, 1967). This nocturnal animal inhabits the African continentand is widely distributed across the savannah from Senegal eastward toEthiopia and also in austral Africa within an area symmetric with regard tothe equator (Dorst and Dandelot, 1972).

For the adult, the total length, without tail, measures about 20 cm andthe weight is rarely more than 300 g.

It can be purchased and maintained at a lower cost than anthropoidprimates and it is possible to keep it several years in a laboratory room (forpractical details see Doyle and Bekker, 1967).

Because of its ethology and its phylogenetic position, the Galago presentsspecial advantages for Neurophysiologists and Psychophysiologists and hasrecently formed the subject of numerous articles (e.g. Atencio et al.9 1975 ;Dobler, 1976 ; Glendenning et al., 1975 ; Goode and Haines, 1975 ; Haines,

(*) Published with the help of the Centre National de la Recherche Scientifique andthe Fondation Marcel Merieux.

(1) Laboratoire de Neurophysiologie, F.S.T., Universite de Nice, Pare Valrose,F-06034 Nice Cedex.

(2) Service d'Histologie, I.N.P., C.N.R.S., 31 chemin Joseph-Aiguier, F-13274 Mar-seille Cedex 2.

(3) Departement de Neurophysiologie Appliquee, L.P.N., C.N.R.S., F-91190 Gif-sur-Yvette.

Mammalia, t. 41, n° 4, 1977.

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Fig. 1. — Perspective-view of the head-holder.(1) Main part. (2) Mouthpiece holder. (3) Articulation screw. (4) Mouthpiece.

(5) Slope screw. (6) Locking nut. (7) Eye rod. (8) Fixing nut. (9) Fixing screw.

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STEREOTAXIC BRAIN ATLAS OF GALAGO 447

1975 ; Hiley, 1976 ; Murray and Haines, 1975). Now the physiological studiesshould be completed by methods which need a more precise knowledge ofsubcortical structures. The present stereotaxic atlas answers this need.

To date, there has been no such atlas for animals situated in the phylo-genetic classification between insectivores and anthropoid primates, except forTupaia (Tigges and Shantha, 1969) whose phylogenetic status is yet unclear.

The brain weighs 4 g to 5 g and is lissencephalic : the external surface ofthe hemisphere is smooth except for the Sylvian and the pre-calcarine fissures(Kanagasuntheram and Mahran, 1960).

STEREOTAXIC TECHNIQUE

A stereotaxic instrument for the rat («La Precision Cinematographique »ref. M) has been used but with a head-holder modified to fit the Galago sene-galensis' skull. This device replaces accessories Me and Op and is describedbelow.

1) Skull landmarks and reference planes.The plane passing through the centres of the external auditory meati and

the lower margins of the orbital openings is usually called the Frankfurtplane or basi-horizontal plane.

The horizontal zero plane (H 0.0) was chosen 5 mm dor sally and parallelto the Frankfurt plane.

The vertical zero plane (A P 0.0) is taken perpendicularly to the Frankfurtplane and these two planes cross along the interaural line.

The lateral zero plane (L 0.0), at right angles with both the H 0.0 andA P 0.0 planes, is the mid-sagittal one.

2) Pieces of the head-holder.The tips of the two eye rods (Fig. 1, No. 7 and Fig. 2 b) are notched to

fit over the inferior orbital ridge. When the rods are positioned on the mainpart of the device, the tops of these notches are situated in the Frankfurtplane.

The skull being fixed by the ear bars, when its forepart is raised, it pivotsabout the interaural line and the lower orbital margin comes into contactwith the eye rods. Then the mouthpiece (Fig. 1, No. 4 and Fig. 2 c) allows theskull to be firmly maintained in this position. Its tip is placed between theupper canine teeth. By turning a slope screw (Fig. 1, No. 5) the mouthpiececant pivot on an articulation screw (Fig. 1, No. 3).

Once the skull is correctly positioned, the mouthpiece is fixed by a lockingnut (Fig. 1, No. 6).

3) The whole head-holder.The pieces are made of duralumin, except the screws and nuts which are

made of brass. The main part of the device (Fig. 2 a) can be displaced longi-tudinally on the stereotaxic instrument. Likewise, the mouthpiece holder(Fig. 1, No. 2) can be displaced longitudinally with respect to the main part



448 MAMMALIA

of the device. Finally the lateral adjustement of the eye rods is provided bya fixing nut and a screw (Fig. 1, No. 8 and 9).

Thus, this headholder is adjustable for use with young galagos havingvarious skull sizes, and perhaps with other small mammals.

MATERIAL

Ten animals (Galago senegalensis senegalensis, six females and four males)weighing from 150 g to 255 g were used. Each of them was anesthetized by anintraperitoneal injection of alpha-chloralose (5 mg / 100 g) and fixed in thestereotaxic holder. Some vertical and horizontal electrodes were implanted atvarious levels. Then an intracardiac perfusion with 10% formol saline wascarried out. After a few hours, the brain was removed from the skull.

HlSTOLOGICAL PROCEDURES

The ten brains were sectioned in frontal planes. All of these sections wereused and stained alternatively with cresyl-violet, Weil and Kluver-Barreratechniques (for cell bodies, fibers and both respectively).

One brain was embedded in paraffin and sectioned every 15 μπι for a moreprecise study of the structures.

The remainders were sectioned on a freezing microtome every 50 μιη.Four of them (three females and one male) presented a remarkably slight inter-individual variation of their stereotaxic coordinates ; the corresponding animalswere characterized by a total weight from 190 g to 240 g and a lambda-bregmadistance from 17.0 to 17.5 mm (the bregma and the lambda are the two pointson the median suture where frontal and parietal bones, and parietal and inter-parietal bones, respectively, meet). The present atlas is valid within theselimits.

DISPOSITION OF THE CHARTS

Thirty-one frontal planes are presented at a magnification of 7.5 χ. Theinterval between two successive planes is not constant but varies dependingon the complexity of the structures encountered. Each level is identified byits A P ordinate, i.e. the distance in mm anterior ( + ) or posterior (—) to theA P 0.0 plane. It is illustrated by two photographs of sections stained withKl ver-Barrera (on the left) and cresyl-violet (on the right) techniques, andfacing them, an explanatory drawing. The structures' outlines are drawn infull lines if well determined and in broken lines when there is some uncertainty.The frame of the photographs and drawings shows millimetric divisions. Theselection of the photographs was made from only one brain.

For recognizing and labeling the nuclei and fiber systems, some comparisonswere made with the stereotaxic atlases of Tupaia (Tigges and Shantha, 1969)and of some primates (Gergen and Mac Lean, 1962 ; Manocha et σ/., 1968;Olszewski, 1952 ; Riche et al, 1968 ; Shantha et α/., 1968; Snider and Lee,




1961), as well as other atlases (Albe-Fessard et /., 1966 ; Herman, 1968 ;Bleier, 1961 ; De Groot, 1959; Jasper and Ajmone-Marsan, 1954; Lehmann,1974 ; Sherwood and Timiras, 1970). We also consulted the available literatureon the diencephalon of Galago (Atencio et al.9 1975 ; Bauchot, 1963 ; Glenden-ning et al.9 1975 ; Kanagasuntheram et /., 1968).

ACKNOWLEDGEMENTS

The publication of this study was made possible by the financial help of the CentreNational de la Recherche Scientifique and of the Fondation MSrieux.

We are deeply grateful to Dr P. Mac Leod for his advice and to Dr J. Bert, Dr J. J.Fetter and Dr. A. Calas who encouraged us during this work.

We are pleased to acknowledge the assistance of MM. Huguenin, Yvinec and Creuzet(photography), Miss Eugene (secretary) and all staff members of I.N.P. 31 (histology).

Our thanks are also due to Mr Baldi, who made the headholder, and to the Laboratoirede Physiologie Animale, University of Dakar (Senegal), and Prof. R. Godet who providedthe animals.

SUMMARY

The present study shows thirty-one frontal sections of the forebrain, extending fromthe inferior colliculus to the olfactory bulb. It can be used for adult males and femaleswith a body weight between 190 and 240 g and a bregma-lambda distance from 17.0 to17.5 mm.

A device is described which fits a stereotaxic apparatus for the rat and allows a Galagosenegalensis' skull to be fixed. The skull landmarks are the lower orbital margins and theexternal auditory meati. The zero point is taken in the mid-sagittal plane, 5 mm abovethe interaural line.

BIBLIOGRAPHY

ALBE-FESSARD, D., F. STUTINSKY and S. LIBOUBAN, 1966. — Atlas stereotaxiqüe du dienci-phale da Rat blanc. Editions du Centre National de la Recherche Scientifique,Paris.

ATENCIO, F. W., I. T. DIAMOND and J. P. WARD, 1975. — Behavorial study of the visualcortex of Galago senegalensis. J. comp. physiol. Psychol., 89 : 1109-1135.

BAUCHOT, R., 1963. — These. Mammalia, 27, suppl. 1 : 1-400.BERMAN, A. L., 1968. — The brain stem of the cat. The University of Wisconsin Press,

Madison, Milwaukee, and London.BLEI ER, R., 1961. — The hypothalamus of the cat. The Johns Hopkins Press, Baltimore.DE GROOT, J., 1959. — The rat forebrain in stereotaxic coordinates. North-Holland Publish-

ing Company, Amsterdam, London.DOBLER, H. J., 1976. — Development of thermoregulation in the newborn lesser bushbaby

(Galago senegalensis moholi Smith 1839). Experientia, 32 : 194-195.DORST, J., and P. DANDELOT, 1972. — Guide des grands mammiferes d'Afrique. Ed. Dela-

chaux et Niestlo, Neuchätel.DOYLE, G. A., and T. BEKKER, 1967. — A facility for naturalistic studies of the lesser

bushbaby (Galago senegalensis moholi). Folia Primat., 7 : 161-168.



450 MAMMALIA

GERGEN, J. Α., and P. D. MAC LEAN, 1962. — A stereotaxic atlas of the squirrel monkey'sbrain (Saimiri sciureus). Public Health Service Publication, Bethesda.

GLENDENNING, K. K., J. A. HALL, I. T. DIAMOND and W. C. HALL, 1975. — The pulvinarnucleus of Galago senegalensis. J. Comp. Neur., 161 : 419-458.

GOODE, G. E., and D. E. HAINES, 1975. — Origin, course and termination of cortico-spinal fibers in a prosimian primate (Galago). Brain Behav. EvoL, 12 : 334-361.

HAINES, D. E., 1975. — Cerebellar cortical efferents of the posterior lobe vermis in aprosimian primate (Galago) and the tree shrew (Tupaia). J. Comp. Neurol.,163 : 21-39.

HILEY, P. G., 1976. — The thermoregulatory responses of the galago (Galago crassi-caudatus), the baboon (Papio cynocephalas) and the chimpanzee (Pan satyrus)to heat stress. J. Physiol. (Lond.), 254 : 657-671.

JASPER, H. H., and C. AJMONE-MARSAN, 1954. — A stereotaxic atlas of the diencephalonof the cat. The National Research Council of Canada, Ottawa.

KANAGASUNTHERAM, R., and Z. Y. MAHRAN, 1960. — Observations on the nervous systemof the lesser bushbaby (Galago senegalensis senegalensis). J. Anat., 94 :512-527.

KANAGASUNTHERAM, R., W. C. WONG and A. KRISHNAMURTI, 1968. — Nuclear confi-guration of the diencephalon in some lorisoid. J. Comp. Neur., 133 : 241-268.

LEHMANN, A., 1974. — Atlas stereotaxique du cerveau de la Souris. Editions du CentreNational de la Recherche Scientifique, Paris.

MANOCHA, S. L., T. R. SHANTHA and G. H. BOURNE, 1968. — A stereotaxic atlas of thebrain of the cebus monkey (Cebus apella). Oxford University Press, London.

MURRAY, H. M., and D. E. HAINES, 1975. — The rubrospinal tract in a prosimian primate(Galago senegalensis). Brain Behav. EvoL, 12 : 311-333.

NAPIER, J. R., and P. H. NAPIER, 1967. — A handbook of living primates. Academic Press,London.

OLSZEWSKI, J., 1952. — The thalamus of the Macaca mulatta. S. Karger, Basel, New York.RICHE, D., A. CHRISTOLOMME, J. BERT and R. NAQUET, 1968. — Atlas stlreotaxique du

cerveau. de Babouin (Papio papio). Editions du Centre National de la RechercheScientifique, Paris.

SHANTHA, T. R., S. L. MANOCHA, and G. H. BOURNE, 1968. — A stereotaxic atlas of the Javamonkey brain (Macaca irus). S. Karger, Basel, New York.

SHERWOOD, N. M., and P. S. TIMIRAS, 1970. — A stereotaxic atlas of the developing ratbrain. University of California Press, Berkeley, Los Angeles, London.

SNIDER, R. S., and J. C. LEE, 1961. — A stereotaxic atlas of the monkey brain (Macacamulatta). The University of Chicago Press, Chicago.

TIGGES, J., and T. R. SHANTHA, 1969. — A stereotaxic brain atlas of the tree shrew (Tupaiaglis). The Williams and Wilkins Company, Baltimore.



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INDEX OF ΒΠΛΙΧ STRUCTURES

Structure Abbreviation

Aquaeductus Sylvii ASArea anterior hypothalami AAHArea dorsalis hypothalami ADHArea latcralis hypothalami ALHArea ])raeoplica laleralis API-Area praetectalis APArea tegmenti ventral is (Tsai) TV

Brachium eoll icul i inferioris HCllirachium eoll iculi superioris BCS

Campus foreli . pars dorsalis H iCampus foreli., pars venlralis H 2Capsula externa CKCapsula exlrema CKTCapsula interna CICentrum median um thalami CMChiasma opticum CHClauslrum CLCollieulus inferior CIRColliculus sii])crior CSRColumna fornicis CFCommissura anterior CACommissura eolliculi inferioris CCICommissura eolliculi superioris CCSCommissura posterior CPCommissura supramamillaris CSMCommissura supraoptica dorsalis CS1)Corpus amygdalae CAMCorpus callosum CCCortex pirifonnis CPF

Decussatio pedunculorum ecrebellarium superiorum DPC

Epiphysis eercbri KP

Fasciculus longitudinalis im-dialis FLMFibrac pontis transvcrsae FPTFimbria hippocampi FHFissura sylvii (Fissura lateralis eercbri) FSFormalio retieularis pontis FRPFormalio retieularis tegmenti mesencephali FRMFornix FFossa interpeduneularis FI

Globus pallidus GPGriseum periventrieulare hypothalami GPHGriscum periventrieulare mesencephali GPMGriseum pontis GPOGyrus cinguli CGyrus dentalus (Fascia dentata hippocampi) . . . . GDGyrus parahippocampalis (Area entorhinalis) GHGyrus uncinatus GUHippocam])us H

StereotaxicA I> levels

1.65 to ~5.8Γ)5.55 to —3.45 to -r6.15 to -f0.75 to -

5.855.55(UM)

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9.008.558.103. (10(U59.000.150.30I). 45

10.50

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3.90 to +2.55 to -f-1.95 to -ί-0.60 to 4-8.10 to -τ-0.15 to -40.30 to -f2.551.05 to -r

1.051.1)52.256.150.301.955.25

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Structure

STEREOTAXIC BRAIN ATLAS OF GALAGO

Abbreviation

513

StereotaxicA P levels

Insula callejae 1C

Laminae bulbi olfactorii LBOLamina medullaris externa lhalami LMKLamina mcdullaris interna thalami LMILcmniscus lateralis LLLemniscus meclialis LM

Xervus oculomotorius n3Xervus trigcminus n5Xervus trochlearis n ,Xucleus accumbcns sepli (Area parolfactoria late-

ralis) ASTXucleus annularis AXXucleus anterior amygdalae AAXucleus anterior dorsalis thalami AI)Xucleus anterior hypothalami AHXucleus anterior medialis thalami AMNucleus anterior ventralis thalami AYNucleus arcuatus hypothalami AHHNucleus basalis accessorius amygdalae BAANucleus basalis lateralis amygdalae BLANucleus basalis medialis amygdalae BMANucleus caudatus XCNucleus centralis amygdalae CKANucleus centralis lateralis thalami XCLNucleus centralis meclialis thalami XCMNucleus centralis superior raphae CSNucleus centralis superior thalami XCSNucleus corticalis amygdalae CO ANucleus Durkschcwitsch DKNucleus dorsalis raphae 1>RNucleus dorsalis septi DSNucleus dorsalis tegmenti (Guddcn) 1)GNucleus dorsolatcralis hypothalami DLHXucleus dorsomedialis hypothalami DMHXucleus Edinger-\Vestj)hal (Xucleus accessorius

nervi oculomotor!i) K\VXucleus fasciculi diagonal is Brocae NFDXucleus geniculatus lateralis GLXucleus geniculalus medialis GMXucleus hahenularis lateralis epilhalami HLXucleus habenularis medialis epithalami HMXucleus inlcrpcduncularis IPXucleus interst i t ial is (Cajal) ISXucleus lateralis amygdalae LAXucleus lateralis corpus mamillaris MLXucleus lateralis septi LSXucleus lateralis lhalami LXucleus lemnisci lateralis NLLXucleus limitans LIMNucleus medialis amygdalae MAXucleus medialis corpus mamillaris MMXucleus medialis dorsalis lhalami MI)Nucleus medialis septi MSNucleus nervi oculomotorii NOXucleus nervi trochlearis TXucleus olfactorius anterior NOA

-f 0.90 lo 4- 8.10

4- 10.50 lo4 3.00 lo 4-4 4.20- 1.05 lo -- 1.05 lo -f

4- 1.35 to 4-- 0.00— 1.05 to —

0.15 to 41.05 to -5.553.905.854.20 to 4-3.90 to -f3.45 to 4-4.50 to 4-4.50 to 4-4.50 to -ί-0. 75 to 4-4.802.55 to 43.00 to 4-1.05 to -3.90 to 4-4.20 to 4-1.95 to 4-1 .054.20 to 4-1 .054.20 to 4-1.50 to 4-

11.104.50

0.152.25

4-

4-

4-

4-

1 .050.15 to 4-0.75 lo 4-0.30 to +1.35 to 4-1.35 to -Ι-Ο. 15 to +1.05 to 44.50 lo 4-3.005.25 to 41.35 to 4-0.00 to -0.75 to 4-4.50 to 4-2.55 to 4-2.25 to 4-5.85 to 40.15 to 40.00

10.50 lo 4-

8.550.00

4.804.805.255.255.555.559.00

3.904.500.004.505.552.25

0.45

4.504.80

0.903.452.252.552.552.252.255.55

7.503.900.151.055.553.004.200.901.35

11.10



514 MAMMALIA

Structure Abbreviation SlereotaxicΛ Ρ levels

Xucleus parabigcirinalis PG — 0.00 to — 0.1.5Nucleus paraeenlralis lhalami PCT -f- 3.90 to -f 4.2«0Xuclcus parafuscicularis lhalami PF — 2.25 to -j- 2.5-5Xuclcus paratacnial is thalami PT — 4.80Xucleus paravenlricularis hypolhalr.mi PH -~ 4.80 to — 5.55Xuclcus paravcntricularis t ha l smi PY --- 3.00 to — 4.80Xuclcus peri vent r icularis hypothalami PIH -f·· 3.90 to — 4.50Xuclcus posterior hypothalami 1 IP -·- 2.55 to — 3.45Xuclcus posterior lha lami PC - 0.30 to - 2.25Xuclcus pracmamillaris PM -·· 3.45Xucleus praeopticus in ters t i l ia l i s POI -r 0.15 to -- 0.45Xuclcus praeopticus magnocellularis POMC — 0.15 to -f 0.45Xuclcus praeopticus medianus POM :- 0.15 to — 0.45Xucleus praeopticus prineipalis POP -f- 0.15 to -f- 0.90Xucleus pulvinaris inferior thalami PL'I -!- 0.30 to -f 1.35Xuclcus pulvinaris superior lha lami PI'S -:- 0.75 to ^- 2.25Xucleus reticularis lhalami H -·- 1.95 to -f 5.25Xuclcus rcuniens lhalami RV -f 3.90Xucleus ruher XH -r 1 -05 to -r l .35Xucleus ruher pars magnocellularis XHM -f 1.05 to -f- 1.95Xucleus ruber pars parvocellulcris XRP -f 1.05 lo -f 1.95Xucleus striae terminal is XST -f 5.25 to -f 5.85Xucleus suhmedius lhalami SMT -\- 4.80Xucleus suhparaccntralis lhalami SPC -}- 3.45 to -f- 3.90Xucleus subthalamicus STH -l- 3.00 to 4- 3.45Xucleus supraehiasmatieus hypothalami SH -r 5.55 to -~ (>,45Xucleus supramamillaris hyi)Othalami SMH 4- 2.55 to -f- 3.00Nucleus supraopticus hypolhalami SOU -f- 5.25 l o -f- 0.15Xucleus supratroehelaris ST — O.(>0Xucleus traclus olfaclorii laleralis Oi. -*- 5.85 to -.· (>.15Nucleus tr iangularis Fcp t i TR -{- 5.25Nucleus vcntralis anterior t ha l ami VA -f- 3.45 to -f -1-80Xucleus ventral is lateral is tha lami VL -f 2.25 to -f 4.50Xucleus ventralis posterior lhalami VP -f 1.95 lo -f 3.90Xucleus ventralis legmenli (Gudden) VG — 0.00Xucleus venlromcdialis hypothalami VMH -\- 4.20 to -}- 4.80

Pedunculus cerebellaris medius (Brachium pontis) I-'CM — 1.G5 lo -f 1.05Pedunculus cerebellaris superior (Brachium con-

junct ivum) PCS - 1.05 to + 0.30Pedunculus cerebri PC -L- 0.75 to 4- 3.45Pons PS -f 1.95Putamcn P -h 2.55 to -f- 8.10

Radiatio geniculocalcir i ra RGC -f- 1.05 lo -f 2.55

Stria medullaris thalami SM 4- 2.25 to + 5.55Subiculum S -|- 0.30 lo + 3.90Subslantia grisea cenlralis GC — 1.05 lo + 1.65Substantia nigra SX + 1.05 to + 1.35Substantia nigra, j>ars compacta SXC. + 1·^>5 to + 2.55Substantia nigra, pars cliiTusa SXD -|- 1.05 lo -f 2.55Sulcus hippocampi SHI -f- 1.05 to + 3.00

Tract us habenulo-interpeduncularis THP -h 1.95 to + 2.55Tractus mamillolhalamicus MT + 3.00 to + 4.50Tractus mesencephalicus nervi trigemini TM — 1.05Tractus olfactorius lateralis LOT + 0.45 l o -f 11.10




Structure Abbreviation StcreolaxicA P levels

-j- 2.25 to -f δ.55- (UK) to + 1.05- 1.05- 1.05 to + 0.30-|- 7.50 to + 8.55

- 1.155 to -1- 9.00+ 9.60 to -f 10.50+ 0.30 to -f 6.45

-f 2.55 t o -{- 3.90

ERRATA

ΛΡ — -1.50 : suppress LA above ALH (on the drawing).Λ I* H- 9.(»0 : add to the legend : CPF = cortex i)iriformis.

Tract us oplicusTract us ])vrainidalisTrad us tectoponl inus'I'ractus lectospinalisTuherculum olfactoriuni

\*enlr iculus lateralis\*entricuhis olfiictorius . . .λ entr iculus tcrlius . . .

Xona incer ta

. . . . TOPYTTPTSTOF

IVOI I I

7Λ





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