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Brain and Behavior of Dromiciops gliroides

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Abstract

We have analyzed the internal structure of the brain of the microbiotherian marsupial Dromiciops gliroides and compared it with the brains of American and Australian marsupials. Dromiciops does not have a fasciculus aberrans, but does exhibit other features of brain structure that are similar to diprotodontid metatherians (e.g., lamination of the lateral geniculate nucleus of the dorsal thalamus). Cortical organization in Dromiciops shows some similarities with that in Australian marsupial carnivores in that the proportional areas of isocortex devoted to somatosensory and visual function are similar in size to each other, and greater in area than that devoted to olfactory or auditory function. This points to similar sensory requirements for the foraging lifestyle of Dromiciops and small Australian marsupial carnivores, with isocortical specialization for somatosensation and vision. We also examined phylogenetic relationships of Dromiciops with extant marsupials based on maximum parsimony analysis using a soft body brain morphology-only matrix, representing 93 extant marsupial taxa. The results recovered Dromiciops as a sister group to the Australasian marsupial clade Diprotodontia.

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Abbreviations

2Cb:

lobule 2 of cerebellar vermis

2n:

optic nerve

3n:

oculomotor nerve

3V:

third ventricle

4Cb:

lobule 4 of cerebellar vermis

4N:

trochlear nucleus

4V:

fourth ventricle

5Cb:

lobule 5 of cerebellar vermis

5n:

trigeminal nerve

5N:

motor trigeminal nucleus

7Cb:

lobule 7 of cerebellar vermis

7n:

facial nerve

8Cb:

lobule 8 of cerebellar vermis

8cn:

cochlear division of vestibulocochlear nerve

9Cb:

lobule 9 of cerebellar vermis

10Cb:

lobule 10 of cerebellar vermis

10 N:

vagal motor nucleus

12 N:

hypoglossal nucleus

α:

α sulcus

ac:

anterior commissure

aca:

anterior commissure, anterior limb

AcbC:

nucleus accumbens core

AcbSh:

nucleus accumbens shell

aci:

anterior commissure, intrabulbar part

ACo:

amygdalocortical area

AD:

anterodorsal thalamic nucleus

AHA:

anterior hypothalamic area

AHi:

amygdalohippocampal area

AID:

agranular insular cortex, dorsal

AIP:

agranular insular cortex, posterior

AIV:

agranular insular cortex, ventral

AM:

anteromedial thalamic nucleus

Ant:

anterior lobe of cerebellum

AOB:

accessory olfactory bulb

AOD:

anterior olfactory nucleus, dorsal part

AOE:

anterior olfactory nucleus, external part

AOL:

anterior olfactory nucleus, lateral part

AOV:

anterior olfactory nucleus, ventral part

AP:

area postrema

APT:

anterior pretectal nucleus

APTD:

anterior pretectal nucleus, dorsal part

APTV:

anterior pretectal nucleus, ventral part

Aq:

cerebral aqueduct

Arc:

arcuate nucleus

ArcLP:

arcuate hypothalamic nucleus, lateral posterior part

ArcMP:

arcuate hypothalamic nucleus, medial posterior part

ASt:

amygdalostriatal area

Au:

auditory cortex

AV:

anteroventral thalamic nucleus

bic:

brachium of inferior colliculus

BIC:

nucleus of brachium of inferior colliculus

BLA:

basolateral nucleus of amygdala, anterior part

BMA:

basomedial nucleus of amygdala, anterior part

BMP:

basomedial nucleus of amygdala, posterior part

bsc:

brachium of superior colliculus

CA:

cornu Ammonis

CA1:

cornu Ammonis, zone 1

CA2:

cornu Ammonis, zone 2

CA3:

cornu Ammonis, zone 3

Cb:

cerebellum

Cd:

caudate nucleus

Ce:

central nucleus of amygdala

cef:

cervical flexure

Cg:

cingulate gyrus

Cg1:

cingulate area 1

Cg2:

cingulate area 2

CIC:

central nucleus of inferior colliculus

Cl:

claustrum

CL:

central lateral thalamic nucleus

CM:

central medial thalamic nucleus

CnF:

cuneiform nucleus

Com:

commissural nucleus of inferior colliculus

cp:

cerebral peduncle

Cu:

cuneate nucleus

Cx:

cortex (region unspecified)

CxA:

cortex amygdala

DA:

dorsal hypothalamic area

das:

dorsal acoustic stria

dc:

dorsal columns

DC:

dorsal cochlear nucleus

DCDp:

dorsal cochlear nucleus, deep layer

DCFu:

dorsal cochlear nucleus, fusiform layer

DCGr:

dorsal cochlear nucleus, granular layer

DCIC:

dorsal cortex of inferior colliculus

DCMo:

dorsal cochlear nucleus, molecular layer

DEn:

dorsal endopiriform cortex

DG:

dentate gyrus of hippocampal formation

DLGa:

dorsal lateral geniculate thalamic nucleus, alpha segment

DLGb:

dorsal lateral geniculate thalamic nucleus, beta segment

DLL:

dorsal nucleus of lateral lemniscus

dlo:

dorsolateral olfactory tract

DMTg:

dorsomedial tegmental nucleus

DpG:

deep gray layer of superior colliculus

DR:

dorsal raphe nucleus

DRL:

dorsal raphe nucleus, lateral part

DS:

dorsal subiculum

DT:

dorsal terminal nucleus

EAC:

extended amygdala, caudal part

ec:

external capsule

ECIC:

external cortex of inferior colliculus

Ect:

ectorhinal cortex

ECu:

external cuneate nucleus

eml:

external medullary lamina

Ent:

entorhinal cortex

EP:

entopeduncular nucleus

EPl:

external plexiform layer, main olfactory bulb

f:

fornix

fi:

fimbria of hippocampal formation

Fl:

flocculus of cerebellum

fr:

fasciculus retroflexus

FrA:

frontal association cortex

GCCM:

granule cell cluster magna

GI:

glomerular layer of main olfactory bulb

GP:

globus pallidus

Gr:

nucleus gracilis

GrO:

granule cell layer of main olfactory bulb

HDB:

nucleus of horizontal limb of diagonal band

Hy:

hypothalamus

ic:

internal capsule

icp:

inferior cerebellar peduncle

IG:

indusium griseum

ILL:

intermediate nucleus of lateral lemniscus

IMD:

intermediodorsal thalamic nucleus

iml:

internal medullary lamina

InG:

intermediate gray layer of superior colliculus

Int:

interposed cerebellar nucleus

IOA:

inferior olive, subnucleus A of ventral accessory nucleus

IOA’:

inferior olive, subnucleus A’ of ventral accessory nucleus

IOB:

inferior olive, subnucleus B of ventral accessory nucleus

IOBe:

inferior olive, beta subnucleus of ventral accessory nucleus

IOC:

inferior olive, subnucleus C of ventral accessory nucleus

IOC’:

inferior olive, subnucleus C′ of ventral accessory nucleus

IOD:

inferior olive, dorsal accessory nucleus

IODl:

inferior olive, dorsal accessory nucleus, lateral part

IODm:

inferior olive, dorsal accessory nucleus, medial part

IOK:

inferior olive, cap of Kooy of ventral accessory nucleus

IOmd:

inferior olive, mediodorsal part of ventral accessory nucleus

IOPr(dl):

inferior olive, principal nucleus, dorsal lamina

IOPr(vl):

inferior olive, principal nucleus, ventral lamina

IP:

interpeduncular nucleus

IPAC:

interstitial nucleus of posterior limb of anterior commissure

IPl:

internal plexiform layer of the olfactory bulb

isRt:

isthmic reticular formation

LA:

lateral anterior hypothalamic nucleus

LACbSh:

lateral accumbens shell

Lat:

lateral deep cerebellar nucleus

LD:

laterodorsal thalamic nucleus

LEnt:

lateral entorhinal cortex

LHb:

lateral habenular nucleus

ll:

lateral lemniscus

LM:

lateral mammillary nucleus

lo:

lateral olfactory tract

LO:

lateral orbital cortex

LP:

lateral posterior thalamic nucleus

LPB:

lateral parabrachial nucleus

LPGi:

lateral paragigantocellular nucleus

LPO:

lateral preoptic nucleus

LRt:

lateral reticular nucleus

LS:

lateral septal nucleus

LSD:

lateral septal nucleus, dorsal part

LSI:

lateral septal nucleus, intermediate part

LSO:

lateral superior olivary nucleus

LSV:

lateral septal nucleus, ventral part

LV:

lateral ventricle

LVe:

lateral vestibular nucleus

LVPO:

lateroventral preoptic nucleus

M:

motor cortex

mcp:

middle cerebellar peduncle

MCPC:

magnocellular nucleus of posterior commissure

MCPO:

magnocellular nucleus of preoptic area

Md:

medulla oblongata

MD:

mediodorsal thalamic nucleus

MDC:

mediodorsal thalamic nucleus, central part

MDL:

mediodorsal thalamic nucleus, lateral part

MDM:

mediodorsal thalamic nucleus, medial part

Med:

medial deep cerebellar nucleus

MEnt:

medial entorhinal cortex

mfb:

medial forebrain bundle

MGD:

medial geniculate nucleus of thalamus, dorsal part

MGM:

medial geniculate nucleus of thalamus, medial part

MGV:

medial geniculate nucleus of thalamus, ventral part

MHb:

medial habenular nucleus

Mi:

mitral cell layer of main olfactory bulb

ml:

medial lemniscus

ML:

medial mammillary nucleus, lateral part

mlf:

medial longitudinal fasciculus

MM:

medial mammillary nucleus, medial part

MnR:

median raphe nucleus

MO:

medial orbital cortex

MOB:

main olfactory bulb

MPA:

medial preoptic area

MPB:

medial parabrachial nucleus

MPT:

medial pretectal nucleus

mRt:

mesencephalic reticular formation

MS:

medial septal nucleus

MSO:

medial superior olive

mt:

mamillothalamic tract

MVe:

medial vestibular nucleus

MVeMC:

medial vestibular nucleus, magnocellular part

MVePC:

medial vestibular nucleus, parvicellular part

MVPO:

medioventral periolivary nucleus

ns:

nigrostriatal tract

OB:

olfactory bulb

och:

optic chiasm

on:

olfactory nerve fibers

ON:

olfactory nerve fibre layer of bulb

opt:

optic tract

p1Rt:

reticular formation of prosomere 1

Pa:

paraventricular nucleus of hypothalamus

PAG:

periaqueductal gray

PaS:

parasubiculum

PBP:

parabrachial pigmented nucleus

pc:

posterior commissure

PC:

paracentral nucleus of thalamus

PCRt:

parvicellular nucleus of reticular formation

PF:

parafascicular nucleus

PFlD:

paraflocculus dorsal

PFlV:

paraflocculus ventral

Pir:

piriform cortex

PLCo:

posterolateral cortical amygdala

PLH:

posterolateral hypothalamus

PMnR:

paramedian raphe nucleus

Pn:

pontine nuclei

PnC:

pontine reticular nucleus, caudal part

PnO:

pontine reticular nucleus, oral part

PnV:

pontine reticular nucleus, ventral part

Po:

posterior thalamic nucleus

PPit:

posterior pituitary

Pr5:

principal sensory trigeminal nucleus

PrCnF:

precuneiform nucleus

PrG:

pregeniculate nucleus of prethalamus

PRh:

perirhinal nucleus

PrL:

prelimbic cortex

PrS:

presubiculum

PT:

paratenial nucleus

Pu:

putamen

PV:

paraventricular thalamic nucleus

PVA:

paraventricular thalamic nucleus, anterior

PVP:

paraventricular thalamic nucleus, posterior

py:

pyramidal tract

Re:

reuniens nucleus of thalamus

rf:

rhinal fissure

RMC:

red nucleus, magnocellular part

RMg:

raphe magnus nucleus

ROb:

raphe obscurus nucleus

RPC:

red nucleus, parvicellular part

RSD:

retrosplenial dysgranular cortex

RSGa:

retrosplenial gyrus, part a

RSGb:

retrosplenial gyrus, part b

Rt:

reticular nucleus

RtSt:

reticulostriatal nucleus

RtTg:

reticulotegmental nucleus

S:

subiculum

S1:

primary somatosensory cortex

S2:

secondary somatosensory cortex

s5:

sensory trigeminal nerve root

SCh:

suprachiasmatic nucleus of hypothalamus

scp:

superior cerebellar peduncle

scpd:

superior cerebellar penduncle decussation

SFi:

septofimbrial nucleus

SHi:

septohippocampal nucleus

SIB:

substantia innominata, B cell groups

Sim:

simplex lobule of cerebellum

sm:

stria medullaris thalami

SNCD:

substantia nigra, compact part, dorsal tier

SNL:

substantia nigra, lateral part

SO:

supraoptic nucleus of hypothalamus

Sol:

nucleus of solitary tract

sp5:

spinal trigeminal tract

Sp5I:

spinal trigeminal nucleus, interpolar part

Sp5O:

spinal trigeminal nucleus, oral part

SpC:

spinal cord

SPO:

superior paraolivary nucleus

SpVe:

spinal vestibular nucleus

st:

stria terminalis

STh:

subthalamic nucleus

STLP:

bed nucleus of stria terminalis, lateral division, posterior part

STLV:

bed nucleus of stria terminalis, lateral division, ventral part

STMD:

bed nucleus of stria terminalis, medial division, dorsal part

SubCD:

subcoeruleus nucleus, dorsal part

SubG:

subgeniculate nucleus of prethalamus

SuG:

superficial gray of superior colliculus

TeA:

temporal association cortex

tfp:

transverse fibers of pons

TS:

triangular septal nucleus

Tu:

olfactory tubercle

tz:

trapezoid body

Tz:

trapezoid nucleus

V1:

primary visual cortex

V2L:

secondary visual area, lateral part

V2M:

secondary visual area, medial part

VA:

ventral anterior thalamic nucleus

VC:

ventral cochlear nucleus

VEn:

ventral endopiriform nucleus

vhc:

ventral hippocampal commissure

VL:

ventral lateral thalamic nucleus

VLH:

ventral lateral hypothalamic nucleus

VLL:

ventral nucleus of lateral lemniscus

VM:

ventromedial thalamic nucleus

VMH:

ventromedial hypothalamic nucleus

VMPO:

ventromedial preoptic nucleus

VO:

ventral orbital cortex

VP:

ventral pallidum

VPL:

ventral posterolateral thalamic nucleus

VPM:

ventral posteromedial thalamic nucleus

VPPC:

ventral posterior nucleus of thalamus, parvicellular part

VRe:

ventral reuniens nucleus

VS:

ventral subiculum

vsc:

venstral spinocerebellar tract

VTA:

ventral tegmental area

VTAR:

ventral tegmental area, rostral part

VTg:

ventral tegmental nucleus

ZI:

zona incerta

Zo:

stratum zonale of superior colliculus

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Acknowledgements

We are extremely grateful to Emeritus Professor John Nelson of Monash University and Dr. Leo Joseph of Commonwealth Scientific and Industrial Research Organization (CSIRO), who kindly gave permission to photograph and analyze the sectioned and stained marsupial brains from the Nelson Brain Collection at the Australian National Wildlife Collection in Canberra. The study would also not have been possible without the excellent online resources of neurosciencelibrary.org.

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  1. Department of Anatomy, School of Medical Sciences, The University of New South Wales, New South Wales, 2052, Australia

    Yamila Gurovich & Kenneth W. S. Ashwell

  2. CIEMEP, CONICET-UNPSJB, Roca 780, 9200, Esquel, Chubut, Argentina

    Yamila Gurovich

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  1. Yamila Gurovich
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Correspondence to Kenneth W. S. Ashwell.

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Gurovich, Y., Ashwell, K.W.S. Brain and Behavior of Dromiciops gliroides. J Mammal Evol 27, 177–197 (2020). https://doi.org/10.1007/s10914-018-09458-1

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