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Afferent projections to the different medial amygdala subdivisions: a retrograde tracing study in the mouse

Brain Structure and Function volume 221, pages 1033–1065 (2016)Cite this article

Abstract

The medial amygdaloid nucleus (Me) is a key node in the socio-sexual brain, composed of anterior (MeA), posteroventral (MePV) and posterodorsal (MePD) subdivisions. These subdivisions have been suggested to play a different role in reproductive and defensive behaviours. In the present work we analyse the afferents of the three Me subdivisions using restricted injections of fluorogold in female outbred CD1 mice. The results reveal that the MeA, MePV and MePD share a common pattern of afferents, with some differences in the density of retrograde labelling in several nuclei. Common afferents to Me subdivisions include: the accessory olfactory bulbs, piriform cortex and endopiriform nucleus, chemosensory amygdala (receiving direct inputs from the olfactory bulbs), posterior part of the medial bed nucleus of the stria terminalis (BSTM), CA1 in the ventral hippocampus and posterior intralaminar thalamus. Minor projections originate from the basolateral amygdala and amygdalo-hippocampal area, septum, ventral striatum, several allocortical and periallocortical areas, claustrum, several hypothalamic structures, raphe and parabrachial complex. MeA and MePV share minor inputs from the frontal cortex (medial orbital, prelimbic, infralimbic and dorsal peduncular cortices), but differ in the lack of main olfactory projections to the MePV. By contrast, the MePD receives preferential projections from the rostral accessory olfactory bulb, the posteromedial BSTM and the ventral premammillary nucleus. In summary, the common pattern of afferents to the Me subdivisions and their interconnections suggest that they play cooperative instead of differential roles in the various behaviours (e.g., sociosexual, defensive) in which the Me has been shown to be involved.

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Abbreviations

1:

Layer 1

2:

Layer 2

2Cb:

2nd cerebellar lobule

3:

Layer 3

3V:

3rd ventricle

4V:

4th ventricle

7n:

Facial nerve or its root

8n:

Vestibulocochlear nerve

8vn:

Vestibular root of the vestibulocochlear nerve

AA:

Anterior amygdaloid area

AAD:

Anterior amygdaloid area, dorsal part

AAV:

Anterior amygdaloid area, ventral part

aca:

Anterior commissure, anterior part

aci:

Anterior commissure, intrabulbar part

Acb:

Accumbens nucleus

AcbC:

Accumbens nucleus, core

AcbSh:

Accumbens nucleus, shell

ACo:

Anterior cortical amygdaloid nucleus

AH:

Anterior hypothalamic area

AHA:

Anterior hypothalamic area, anterior part

AHC:

Anterior hypothalamic area, central part

AHi:

Amygdalohippocampal area

AHP:

Anterior hypothalamic area, posterior part

AI:

Agranular insular cortex

AID:

Agranular insular cortex, dorsal part

AIP:

Agranular insular cortex, posterior part

AIV:

Agranular insular cortex, ventral part

AOB:

Accessory olfactory bulb

AOM:

Anterior olfactory nucleus, medial part

AON:

Anterior olfactory nucleus

AOP:

Anterior olfactory nucleus, posterior part

APir:

Amygdalopiriform transition area

Aq:

Aqueduct

Arc:

Arcuate hypothalamic nucleus

BAOT:

Bed nucleus of the accessory olfactory tract

BLA:

Basolateral amygdaloid nucleus, anterior part

BLP:

Basolateral amygdaloid nucleus, posterior part

BLV:

Basolateral amygdaloid nucleus, ventral part

BMA:

Basomedial amygdaloid nucleus, anterior part

BMP:

Basomedial amygdaloid nucleus, posterior part

BST:

Bed nucleus of the stria terminalis

BSTIA:

BST, intraamygdaloid division

BSTLP:

BST, lateral division, posterior part

BSTLV:

BST, lateral division, ventral part

BSTMA:

BST, medial division, anterior part

BSTMPI:

BST, medial division, posterointermediate part

BSTMPL:

BST, medial division, posterolateral part

BSTMPM:

BST, medial division, posteromedial part

BSTMV:

BST, medial division, ventral part

BSTS:

Bed nucleus of stria terminalis, supracapsular part

CA1:

Field CA1 of hippocampus

CA3:

Field CA3 of hippocampus

Ce:

Central amygdaloid nucleus

CeC:

Central amygdaloid nucleus, capsular part

CeL:

Central amygdaloid nucleus, lateral division

CeM:

Central amygdaloid nucleus, medial division

Cl:

Claustrum

CM:

Central medial thalamic nucleus

cp:

Cerebral peduncle

CPu:

Caudate putamen

csc:

Commissure of the superior colliculus

cst:

Commissural stria terminalis

CxA:

Cortex-amygdala transition zone

D3V:

Dorsal 3rd ventricle

DEn:

Dorsal endopiriform nucleus

DG:

Dentate gyrus

dlot:

Dorsal lateral olfactory tract

DM:

Dorsomedial hypothalamic nucleus

DP:

Dorsal peduncular cortex

DR:

Dorsal raphe nucleus

DTT:

Dorsal tenia tecta

E/OV:

Ependymal and subependymal layer/olfactory ventricle

ec:

External capsule

EPl:

External plexiform layer of the main olfactory bulb

EPlA:

External plexiform layer of the accessory olfactory bulb

f:

Fornix

fi:

Fimbria of the hippocampus

fmi:

Forceps minor of the corpus callosum

fr:

Fasciculus retroflexus

Gl:

Glomerular layer of the main olfactory bulb

GlA:

Glomerular layer of the AOB

GrA:

Granule cell layer of the AOB

GrO:

Granular cell layer of the main olfactory bulb

HDB:

Nucleus of the horizontal limb of the diagonal band

I:

Intercalated nuclei of the amygdala

ic:

Internal capsule

IL:

Infralimbic cortex

IM:

Intercalated amygdaloid nucleus, main part

IP:

Interpeduncular nucleus

IPAC:

Interstitial nucleus of the posterior limb of the anterior commissure

IPl:

Internal plexiform layer of the main olfactory bulb

LA:

Lateroanterior hypothalamic nucleus

La:

Lateral amygdaloid nucleus

LaDL:

Lateral amygdaloid nucleus, dorsolateral part

LaVL:

Lateral amygdaloid nucleus, ventrolateral part

LaVM:

Lateral amygdaloid nucleus, ventromedial part

LC:

Locus coeruleus

Ld:

Lambdoid septal zone

LDTg:

Laterodorsal tegmental nucleus

LEnt:

Lateral entorhinal cortex

LGP:

Lateral globus pallidus

LH:

Lateral hypothalamic area

LHb:

Lateral habenular nucleus

LPB:

Lateral parabrachial nucleus

LPO:

Lateral preoptic area

LO:

Lateral orbital cortex

lo:

Lateral olfactory tract

LOT:

Nucleus of the lateral olfactory tract

LPO:

Lateral preoptic area

LSD:

Lateral septal nucleus, dorsal part

LSI:

Lateral septal nucleus, intermediate part

LSV:

Lateral septal nucleus, ventral part

LV:

Lateral ventricle

mcp:

Middle cerebellar peduncle

MCPO:

Magnocellular preoptic nucleus

MD:

Mediodorsal thalamic nucleus

ME:

Median eminence

Me:

Medial amygdaloid nucleus

me5:

Mesencephalic trigeminal tract

MeA:

Medial amygdaloid nucleus, anterior subnucleus

MeAD:

Medial amygdaloid nucleus, anterodorsal part

MeAV:

Medial amygdaloid nucleus, anteroventral part

MePD:

Medial amygdaloid nucleus, posterodorsal subnucleus

MePV:

Medial amygdaloid nucleus, posteroventral subnucleus

MGD:

Medial geniculate nucleus, dorsal part

MGM:

Medial geniculate nucleus, medial part

MGV:

Medial geniculate nucleus, ventral part

MHb:

Medial habenular nucleus

Mi:

Mitral cell layer of the main olfactory bulb

MiA:

Mitral cell layer of the AOB

ml:

Medial lemniscus

mlf:

Medial longitudinal fasciculus

MM:

Medial mammillary nucleus, medial part

MnR:

Median raphe nucleus

MO:

Medial orbital cortex

Mo5:

Motor trigeminal nucleus

MOB:

Main olfactory bulb

MPA:

Medial preoptic area

MPB:

Medial parabrachial nucleus

MPO:

Medial preoptic nucleus

MS:

Medial septal nucleus

mt:

Mammillothalamic tract

mtg:

Mammillotegmental tract

ns:

Nigrostriatal bundle

opt:

Optic tract

ox:

Optic chiasm

Pa:

Paraventricular hypothalamic nucleus

PAG:

Periaqueductal gray

PB:

Parabrachial nucleus

pc:

Posterior commissure

Pe:

Periventricular hypothalamic nucleus

PH:

Posterior hypothalamic area

PIL:

Posterior intralaminar thalamic nucleus

Pir:

Piriform cortex

PLCo:

Posterolateral cortical amygdaloid nucleus

PMCo:

Posteromedial cortical amygdaloid nucleus

PMD:

Premammillary nucleus, dorsal part

PMV:

Premammillary nucleus, ventral part

PnC:

Pontine reticular nucleus, caudal part

Po:

Posterior thalamic nuclear group

PP:

Peripeduncular nucleus

Pr5VL:

Principal sensory trigeminal nucleus, ventrolateral part

PRh:

Perirhinal cortex

PrL:

Prelimbic cortex

pv:

Periventricular fibre system

PV:

Paraventricular thalamic nucleus

PVA:

Paraventricular thalamic nucleus, anterior part

PVP:

Paraventricular thalamic nucleus, posterior part

py:

Pyramidal tract

Re:

Reuniens thalamic nucleus

RLi:

Rostral linear nucleus of the raphe

S:

Subiculum

s5:

Sensory root of the trigeminal nerve

scp:

Superior cerebellar peduncle

SG:

Suprageniculate thalamic nucleus

SHi:

Septohippocampal nucleus

SI:

Substantia innominata

SL:

Semilunar nucleus

sm:

Stria medullaris

SNR:

Substantia nigra, reticular part

sox:

Supraoptic decussation

sp5:

Spinal trigeminal tract

SPF:

Subparafascicular thalamic nucleus

SPFPC:

Subparafascicular thalamic nucleus, parvicellular part

st:

Stria terminalis

str:

Superior thalamic radiation

Su5:

Supratrigeminal nucleus

SuM:

Supramammillary nucleus

TC:

Tuber cinereum area

Tu:

Olfactory tubercle

VDB:

Nucleus of the vertical limb of the diagonal band

VEn:

Ventral endopiriform nucleus

VL:

Ventrolateral thalamic nucleus

VMH:

Ventromedial hypothalamic nucleus

VO:

Ventral orbital cortex

VP:

Ventral pallidum

vsc:

Ventral spinocerebellar tract

VTA:

Ventral tegmental area

VTT:

Ventral tenia tecta

ZI:

Zona incerta

ZID:

Zona incerta, dorsal part

ZIV:

Zona incerta, ventral part

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Acknowledgments

Funded by the Spanish Ministry of Science-FEDER (BFU2010-16656 and BFU2013-47688-P). B.C.-M. is a predoctoral fellow of the “Becas Chile” program of the Government of Chile.

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  1. Fernando Martínez-García

    Present address: Unitat Predepartamental de Medicina, Fac. Ciències de la Salut, Universitat Jaume I, Av. Sos Baynat, s/n; Campus del Riu Sec, 12071, Castellón de la Plana, Spain

Authors and Affiliations

  1. Laboratori de Neuroanatomia Funcional Comparada, Departaments de Biologia Cel·lular and Biologia Funcional, Facultat de Ciències Biològiques, Universitat de València, C/Dr. Moliner, 50, Burjassot, 46100, Valencia, Spain

    Bernardita Cádiz-Moretti, Marcos Otero-García, Fernando Martínez-García & Enrique Lanuza

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  1. Bernardita Cádiz-Moretti
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Cádiz-Moretti, B., Otero-García, M., Martínez-García, F. et al. Afferent projections to the different medial amygdala subdivisions: a retrograde tracing study in the mouse. Brain Struct Funct 221, 1033–1065 (2016). https://doi.org/10.1007/s00429-014-0954-y

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Keywords

  • Vomeronasal
  • Olfactory system
  • Fluorogold
  • Retrograde tracing
  • Socio-sexual behaviour