Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

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

References

  • Arakawa H, Arakawa K, Deak T (2010) Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor. Neuroscience 171:1141–1151

    Article  CAS  PubMed  Google Scholar 

  • Bader A, Breer H, Strotmann J (2012) Untypical connectivity from olfactory sensory neurons expressing OR37 into higher brain centers visualized by genetic tracing. Histochem Cell Biol 137:615–628

    Article  CAS  Google Scholar 

  • Bautze V, Bar R, Fissler B, Trapp M, Schmidt D, Beifuss U, Bufe B, Zufall F, Breer H, Strotmann J (2012) Mammalian-specific OR37 receptors are differentially activated by distinct odorous fatty aldehydes. Chem Senses 37:479–493

    Article  CAS  PubMed  Google Scholar 

  • Bautze V, Schwack W, Breer H, Strotmann J (2014) Identification of a natural source for the OR37B ligand. Chem Senses 39:27–38

    Article  CAS  PubMed  Google Scholar 

  • Bergan JF, Ben-Shaul Y, Dulac C (2014) Sex-specific processing of social cues in the medial amygdala. Elife 3:e02743. doi:10.7554/eLife02743

    Article  PubMed  PubMed Central  Google Scholar 

  • Bordi F, LeDoux JE (1994) Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdala stimulation. Exp Brain Res 98:275–286

    Article  CAS  PubMed  Google Scholar 

  • Bourgeais L, Gauriau C, Bernard JF (2001) Projections from the nociceptive area of the central nucleus of the amygdala to the forebrain: a PHA-L study in the rat. Eur J Neurosci 14:229–255

    Article  CAS  PubMed  Google Scholar 

  • Bupesh M, Legaz I, Abellan A, Medina L (2011) Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol 519:1505–1525

    Article  PubMed  Google Scholar 

  • Cadiz-Moretti B, Martinez-Garcia F, Lanuza E (2013) Neural substrate to associate odorants and pheromones: convergence of projections from the main and accessory olfactory bulbs in mice. In: East ML, Dehnhard M (eds) Chemical signals in vertebrates 12. Springer Science, New York, pp 3–16

    Chapter  Google Scholar 

  • Cahill L, McGaugh JL (1990) Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav Neurosci 104:532–543

    Article  CAS  PubMed  Google Scholar 

  • Calu DJ, Roesch MR, Stalnaker TA, Schoenbaum G (2007) Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb Cortex 17:1342–1349

    Article  PubMed  PubMed Central  Google Scholar 

  • Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324:180–194

    Article  CAS  PubMed  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1992a) Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143–179

    Article  CAS  PubMed  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1992b) Projections of the ventral premammillary nucleus. J Comp Neurol 324:195–212

    Article  CAS  PubMed  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1994) Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348:41–79

    Article  CAS  PubMed  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213–245

    Article  CAS  PubMed  Google Scholar 

  • Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56:1–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450:899–902

    Article  CAS  PubMed  Google Scholar 

  • Choi GB, Dong HW, Murphy AJ, Valenzuela DM, Yancopoulos GD, Swanson LW, Anderson DJ (2005) Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46:647–660

    Article  CAS  PubMed  Google Scholar 

  • Christensen MK, Frederickson CJ (1998) Zinc-containing afferent projections to the rat corticomedial amygdaloid complex: a retrograde tracing study. J Comp Neurol 400:375–390

    Article  CAS  PubMed  Google Scholar 

  • Coolen LM, Wood RI (1998) Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: simultaneous anterograde and retrograde tract tracing. J Comp Neurol 399:189–209

    Article  CAS  PubMed  Google Scholar 

  • Cousens G, Otto T (1998) Both pre- and posttraining excitotoxic lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning. Behav Neurosci 112:1092–1103

    Article  CAS  PubMed  Google Scholar 

  • Cousens GA, Kearns A, Laterza F, Tundidor J (2012) Excitotoxic lesions of the medial amygdala attenuate olfactory fear-potentiated startle and conditioned freezing behavior. Behav Brain Res 229:427–432

    Article  PubMed  Google Scholar 

  • de la Rosa-Prieto C, Ubeda-Banon I, Mohedano-Moriano A, Pro-Sistiaga P, Saiz-Sanchez D, Insausti R, Martinez-Marcos A (2009) Subicular and CA1 hippocampal projections to the accessory olfactory bulb. Hippocampus 19:124–129

    Article  PubMed  Google Scholar 

  • de Olmos JS, Beltramino CA, Alheid GF (2004) Amygdala and extended Amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In: Paxinos G (ed) The rat nervous system. Elsevier Academic Press, San Diego, pp 509–603

    Google Scholar 

  • Dielenberg RA, Hunt GE, McGregor IS (2001) ”When a rat smells a cat”: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104:1085–1097

    Article  CAS  PubMed  Google Scholar 

  • Dong HW, Swanson LW (2004) Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J Comp Neurol 471:396–433

    Article  PubMed  Google Scholar 

  • Dong HW, Petrovich GD, Swanson LW (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Rev 38:192–246

    Article  CAS  PubMed  Google Scholar 

  • Doron NN, LeDoux JE (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J Comp Neurol 412:383–409

    Article  CAS  PubMed  Google Scholar 

  • Erskine MS (1993) Mating-induced increases in FOS protein in preoptic area and medial amygdala of cycling female rats. Brain Res Bull 32:447–451

    Article  CAS  PubMed  Google Scholar 

  • Falkner AL, Dollar P, Perona P, Anderson DJ, Lin D (2014) Decoding ventromedial hypothalamic neural activity during male mouse aggression. J Neurosci 34:5971–5984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fortes-Marco L, Lanuza E, Martinez-Garcia F (2013) Of pheromones and kairomones: what receptors mediate innate emotional responses? Anat Rec (Hoboken) 296:1346–1363

    Article  CAS  Google Scholar 

  • Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319:229–259

    Article  CAS  PubMed  Google Scholar 

  • Gomez DM, Newman SW (1992) Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster. J Comp Neurol 317:195–218

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48:11–22

    Article  PubMed  PubMed Central  Google Scholar 

  • Gu G, Cornea A, Simerly RB (2003) Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J Comp Neurol 460:542–562

    Article  PubMed  Google Scholar 

  • Guillamon A, Segovia S (1997) Sex differences in the vomeronasal system. Brain Res Bull 44:377–382

    Article  CAS  PubMed  Google Scholar 

  • Gulia KK, Jodo E, Kawauchi A, Miki T, Kayama Y, Mallick HN, Koyama Y (2008) The septal area, site for the central regulation of penile erection during waking and rapid eye movement sleep in rats: a stimulation study. Neuroscience 156:1064–1073

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Castellanos N, Martínez-Marcos A, Martínez-García F, Lanuza E (2010) Chemosensory function of the amygdala. Vitam Horm 83:165–196

    Article  PubMed  Google Scholar 

  • Gutiérrez-Castellanos N, Pardo-Bellver C, Martínez-García F, Lanuza E (2014) The vomeronasal cortex—afferent and efferent projections of the posteromedial cortical nucleus of the amygdala in mice. Eur J Neurosci 39:141–158

    Article  PubMed  Google Scholar 

  • Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551–576

    Article  CAS  PubMed  Google Scholar 

  • Halem HA, Cherry JA, Baum MJ (1999) Vomeronasal neuroepithelium and forebrain Fos responses to male pheromones in male and female mice. J Neurobiol 39:249–263

    Article  CAS  PubMed  Google Scholar 

  • Halpern M, Martinez-Marcos A (2003) Structure and function of the vomeronasal system: an update. Prog Neurobiol 70:245–318

    Article  CAS  PubMed  Google Scholar 

  • Hari Dass SA, Vyas A (2014) Copulation or sensory cues from the female augment fos expression in arginine vasopressin neurons of the posterodorsal medial amygdala of male rats. Front Zool 11:42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249–276

    Article  CAS  PubMed  Google Scholar 

  • Isogai Y, Si S, Pont-Lezica L, Tan T, Kapoor V, Murthy VN, Dulac C (2011) Molecular organization of vomeronasal chemoreception. Nature 478:241–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang N, Baum MJ, Cherry JA (2009) A direct main olfactory bulb projection to the ‘vomeronasal’ amygdala in female mice selectively responds to volatile pheromones from males. Eur J Neurosci 29:624–634

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang N, Baum MJ, Cherry JA (2011) Different profiles of main and accessory olfactory bulb mitral/tufted cell projections revealed in mice using an anterograde tracer and a whole-mount, flattened cortex preparation. Chem Senses 36:251–260

    Article  PubMed  PubMed Central  Google Scholar 

  • Kishi T, Tsumori T, Yokota S, Yasui Y (2006) Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J Comp Neurol 496:349–368

    Article  PubMed  Google Scholar 

  • Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99:10825–10830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kollack-Walker S, Newman SW (1995) Mating and agonistic behavior produce different patterns of fos immunolabeling in the male Syrian hamster brain. Neurosci 66:721–736

    Article  CAS  Google Scholar 

  • Koolhaas JM, van den Brink THC, Roozendaal B, Boorsma F (1990) Medial amygdala and aggressive behavior: interaction between testosterone and vasopressin. Aggr Behav 16:223–229

    CAS  Google Scholar 

  • Krieger MS, Conrad LC, Pfaff DW (1979) An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. J Comp Neurol 183:785–815

    Article  CAS  PubMed  Google Scholar 

  • Krieger J, Schmitt A, Lobel D, Gudermann T, Schultz G, Breer H, Boekhoff I (1999) Selective activation of G protein subtypes in the vomeronasal organ upon stimulation with urine-derived compounds. J Biol Chem 274:4655–4662

    Article  CAS  PubMed  Google Scholar 

  • Lanuza E, Nader K, LeDoux JE (2004) Unconditioned stimulus pathways to the amygdala: effects of posterior thalamic and cortical lesions on fear conditioning. Neuroscience 125:305–315

    Article  CAS  PubMed  Google Scholar 

  • Lanuza E, Moncho-Bogani J, LeDoux JE (2008) Unconditioned stimulus pathways to the amygdala: effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala. Neuroscience 155:959–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ (1987) Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123–146

    Article  CAS  PubMed  Google Scholar 

  • LeDoux JE, Farb C, Ruggiero DA (1990a) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10:1043–1054

    CAS  PubMed  Google Scholar 

  • LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990b) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069

    CAS  PubMed  Google Scholar 

  • Lehman MN, Winans SS, Powers JB (1980) Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science 210:557–560

    Article  CAS  PubMed  Google Scholar 

  • Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796

    Article  CAS  PubMed  Google Scholar 

  • Li S, Kirouac GJ (2008) Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 506:263–287

    Article  PubMed  Google Scholar 

  • Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linke R, De Lima AD, Schwegler H, Pape HC (1999) Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J Comp Neurol 403:158–170

    Article  CAS  PubMed  Google Scholar 

  • Majak K, Pitkanen A (2003) Projections from the periamygdaloid cortex to the amygdaloid complex, the hippocampal formation, and the parahippocampal region: a PHA-L study in the rat. Hippocampus 13:922–942

    Article  PubMed  Google Scholar 

  • Maras PM, Petrulis A (2010a) Anatomical connections between the anterior and posterodorsal sub-regions of the medial amygdala: integration of odor and hormone signals. Neuroscience 170:610–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maras PM, Petrulis A (2010b) The anterior medial amygdala transmits sexual odor information to the posterior medial amygdala and related forebrain nuclei. Eur J Neurosci 32:469–482

    Article  PubMed  Google Scholar 

  • Maras PM, Petrulis A (2010c) Lesions that functionally disconnect the anterior and posterodorsal sub-regions of the medial amygdala eliminate opposite-sex odor preference in male Syrian hamsters (Mesocricetus auratus). Neuroscience 165:1052–1062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maren S, Fanselow MS (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 15:7548–7564

    CAS  PubMed  Google Scholar 

  • Martínez-García F, Novejarque A, Gutiérrez-Castellanos N, Lanuza E (2012) Piriform cortex and amygdala. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic Press, San Diego, pp 140–172

    Chapter  Google Scholar 

  • McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71:55–75

    Article  CAS  PubMed  Google Scholar 

  • Meredith M (1986) Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol Behav 36:737–743

    Article  CAS  PubMed  Google Scholar 

  • Meredith M, Westberry JM (2004) Distinctive responses in the medial amygdala to same-species and different-species pheromones. J Neurosci 24:5719–5725

    Article  CAS  PubMed  Google Scholar 

  • Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055–2067

    Article  CAS  PubMed  Google Scholar 

  • Mohedano-Moriano A, Pro-Sistiaga P, Ubeda-Banon I, Crespo C, Insausti R, Martinez-Marcos A (2007) Segregated pathways to the vomeronasal amygdala: differential projections from the anterior and posterior divisions of the accessory olfactory bulb. Eur J Neurosci 25:2065–2080

    Article  PubMed  Google Scholar 

  • Moncho-Bogani J, Martinez-Garcia F, Novejarque A, Lanuza E (2005) Attraction to sexual pheromones and associated odorants in female mice involves activation of the reward system and basolateral amygdala. Eur J Neurosci 21:2186–2198

    Article  PubMed  Google Scholar 

  • Morgan HD, Watchus JA, Milgram NW, Fleming AS (1999) The long lasting effects of electrical simulation of the medial preoptic area and medial amygdala on maternal behavior in female rats. Behav Brain Res 99:61–73

    Article  CAS  PubMed  Google Scholar 

  • Morris JA, Jordan CL, King ZA, Northcutt KV, Breedlove SM (2008) Sexual dimorphism and steroid responsiveness of the posterodorsal medial amygdala in adult mice. Brain Res 1190:115–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Motta SC, Guimaraes CC, Furigo IC, Sukikara MH, Baldo MV, Lonstein JS, Canteras NS (2013) Ventral premammillary nucleus as a critical sensory relay to the maternal aggression network. Proc Natl Acad Sci USA 110:14438–14443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman SW (1999) The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 877:242–257

    Article  CAS  PubMed  Google Scholar 

  • Nitecka L (1981) Connections of the hypothalamus and preoptic area with nuclei of the amygdaloid body in the rat; HRP retrograde transport study. Acta Neurobiol Exp 41:53–67

    CAS  Google Scholar 

  • Nodari F, Hsu FF, Fu X, Holekamp TF, Kao LF, Turk J, Holy TE (2008) Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J Neurosci 28:6407–6418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olucha-Bordonau FE, Fortes-Marco L, Otero-García M, Lanuza E, Martínez-García F (2015) Amygdala, structure and function. In: Paxinos G (ed) The rat nervous system. Academic Press, New York, pp 441–490

    Google Scholar 

  • Otero-Garcia M, Martin-Sanchez A, Fortes-Marco L, Martínez-Ricós J, Agustin-Pavón C, Lanuza E, Martínez-García F (2014) Extending the socio-sexual brain: arginine-vasopressin immunoreactive circuits in the telencephalon of mice. Brain Struct Funct 219:1055–1081

    Article  CAS  PubMed  Google Scholar 

  • Ottersen OP (1980) Afferent connections of the amygdaloid complex of the rat and cat. II. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol 194:267–289

    Article  CAS  PubMed  Google Scholar 

  • Ottersen OP, Ben-Ari Y (1979) Afferent connections of the amygdaloid complex of the rat and cat. I. Projections from the thalamus. J Comp Neurol 187:401–424

    Article  CAS  PubMed  Google Scholar 

  • Oxley G, Fleming AS (2000) The effects of medial preoptic area and amygdala lesions on maternal behavior in the juvenile rat. Dev Psychobiol 37:253–265

    Article  CAS  PubMed  Google Scholar 

  • Palomero-Gallagher N, Zilles K (2015) Isocortex. In: Paxinos G (ed) The rat nervous system, 4th edn. Academic Press, London, pp 601–625

    Google Scholar 

  • Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pardo-Bellver C, Cadiz-Moretti B, Novejarque A, Martinez-Garcia F, Lanuza E (2012) Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice. Front Neuroanat 6:33

    Article  PubMed  PubMed Central  Google Scholar 

  • Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  • Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374:387–420

    Article  CAS  PubMed  Google Scholar 

  • Petrulis A (2013) Chemosignals, hormones and mammalian reproduction. Horm Behav 63:723–741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pezzone MA, Lee W-, Hoffman GE, Rabin BS (1992) Induction of c-Fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res 597:41–50

    Article  CAS  PubMed  Google Scholar 

  • Pfaus JG, Kleopoulos SP, Mobbs CV, Gibbs RB, Pfaff DW (1993) Sexual stimulation activates c-fos within estrogen-concentrating regions of the female rat forebrain. Brain Res 624:253–267

    Article  CAS  PubMed  Google Scholar 

  • Pfaus JG, Marcangione C, Smith WJ, Manitt C, Abillamaa H (1996) Differential induction of Fos in the female rat brain following different amounts of vaginocervical stimulation: modulation by steroid hormones. Brain Res 741:314–330

    Article  CAS  PubMed  Google Scholar 

  • Pitkanen A (2000) Connectivity of the rat amygdaloid complex. In: Aggleton J (ed) The amygdala. A functional analysis, 2nd edn. Oxford University Press, Oxford, pp 31–115

    Google Scholar 

  • Polston EK, Erskine MS (1995) Patterns of induction of the immediate-early genes c-fos and egr-1 in the female rat brain following differential amounts of mating stimulation. Neuroendocrinology 62:370–384

    Article  CAS  PubMed  Google Scholar 

  • Pro-Sistiaga P, Mohedano-Moriano A, Ubeda-Banon I, Del Mar Arroyo-Jimenez M, Marcos P, Artacho-Perula E, Crespo C, Insausti R, Martinez-Marcos A (2007) Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J Comp Neurol 504:346–362

    Article  PubMed  Google Scholar 

  • Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes dlx-2, emx-1, nkx- 2.1, pax-6, and tbr-1. J Comp Neurol 424:409–438

    Article  CAS  PubMed  Google Scholar 

  • Risold PY (2004) The septal region. In: Paxinos G (ed) The rat nervous system, 3rd edn. Academic Press, San Diego, pp 605–632

    Google Scholar 

  • Risold PY, Canteras NS, Swanson LW (1994) Organization of projections from the anterior hypothalamic nucleus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348:1–40

    Article  CAS  PubMed  Google Scholar 

  • Riviere S, Challet L, Fluegge D, Spehr M, Rodriguez I (2009) Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 459:574–577

    Article  CAS  PubMed  Google Scholar 

  • Rood BD, Stott RT, You S, Smith CJ, Woodbury ME, De Vries GJ (2013) Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J Comp Neurol 521:2321–2358

    Article  CAS  PubMed  Google Scholar 

  • Rosen JB, Fanselow MS, Young SL, Sitcoske M, Maren S (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res 796:132–142

    Article  CAS  PubMed  Google Scholar 

  • Salazar I, Brennan PA (2001) Retrograde labelling of mitral/tufted cells in the mouse accessory olfactory bulb following local injections of the lipophilic tracer DiI into the vomeronasal amygdala. Brain Res 896:198–203

    Article  CAS  PubMed  Google Scholar 

  • Samuelsen CL, Meredith M (2009a) Categorization of biologically relevant chemical signals in the medial amygdala. Brain Res 1263:33–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuelsen CL, Meredith M (2009b) The vomeronasal organ is required for the male mouse medial amygdala response to chemical-communication signals, as assessed by immediate early gene expression. Neuroscience 164:1468–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sano K, Tsuda MC, Musatov S, Sakamoto T, Ogawa S (2013) Differential effects of site-specific knockdown of estrogen receptor alpha in the medial amygdala, medial pre-optic area, and ventromedial nucleus of the hypothalamus on sexual and aggressive behavior of male mice. Eur J Neurosci 37:1308–1319

    Article  PubMed  Google Scholar 

  • Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161:31–55

    Article  CAS  PubMed  Google Scholar 

  • Shi CJ, Cassell MD (1998) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399:440–468

    Article  CAS  PubMed  Google Scholar 

  • Shi C, Davis M (1999) Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci 19:420–430

    CAS  PubMed  Google Scholar 

  • Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–538

    Article  PubMed  PubMed Central  Google Scholar 

  • Simerly RB (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25:507–536

    Article  CAS  PubMed  Google Scholar 

  • Simerly RB, Chang C, Muramatsu M, Swanson LW (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76–95

    Article  CAS  PubMed  Google Scholar 

  • Swann J, Fabre-Nys C, Barton R (2009) Hormonal and pheromonal modulation of the extended amygdala: implications for social behavior. In: Pfaff DW, Arnold AP, Fahrbach SE, Etgen AM, Rubin RT (eds) Hormones, brain and behavior, 2nd edn. Academic Press, San Diego, pp 441–474

    Chapter  Google Scholar 

  • Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886:113–164

    Article  CAS  PubMed  Google Scholar 

  • Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331

    Article  CAS  PubMed  Google Scholar 

  • Tachikawa KS, Yoshihara Y, Kuroda KO (2013) Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J Neurosci 33:5120–5126

    Article  CAS  PubMed  Google Scholar 

  • Takahashi LK (2014) Olfactory systems and neural circuits that modulate predator odor fear. Front Behav Neurosci 8:72

    Article  PubMed  PubMed Central  Google Scholar 

  • Takahashi LK, Hubbard DT, Lee I, Dar Y, Sipes SM (2007) Predator odor-induced conditioned fear involves the basolateral and medial amygdala. Behav Neurosci 121:100–110

    Article  PubMed  Google Scholar 

  • Tetel MJ, Getzinger MJ, Blaustein JD (1993) Fos expression in the rat brain following vaginal-cervical stimulation by mating and manual probing. J Neuroendocrinol 5:397–404

    Article  CAS  PubMed  Google Scholar 

  • Thompson RH, Canteras NS, Swanson LW (1996) Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J Comp Neurol 376:143–173

    Article  CAS  PubMed  Google Scholar 

  • Thompson JA, Salcedo E, Restrepo D, Finger TE (2012) Second-order input to the medial amygdala from olfactory sensory neurons expressing the transduction channel TRPM5. J Comp Neurol 520:1819–1830

    Article  PubMed  PubMed Central  Google Scholar 

  • Tirindelli R, Dibattista M, Pifferi S, Menini A (2009) From pheromones to behavior. Physiol Rev 89:921–956

    Article  CAS  PubMed  Google Scholar 

  • Tsukahara S, Tsuda MC, Kurihara R, Kato Y, Kuroda Y, Nakata M, Xiao K, Nagata K, Toda K, Ogawa S (2011) Effects of aromatase or estrogen receptor gene deletion on masculinization of the principal nucleus of the bed nucleus of the stria terminalis of mice. Neuroendocrinology 94(2):137–147

    Article  CAS  PubMed  Google Scholar 

  • Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing. J Comp Neurol 313:295–325

    Article  CAS  PubMed  Google Scholar 

  • Usunoff KG, Schmitt O, Itzev DE, Haas SJ, Lazarov NE, Rolfs A, Wree A (2009) Efferent projections of the anterior and posterodorsal regions of the medial nucleus of the amygdala in the mouse. Cells Tissues Organs 190:256–285

    Article  PubMed  Google Scholar 

  • Veening JG (1978) Subcortical afferents of the amygdaloid complex in the rat: an HRP study. Neurosci Lett 8:197–202

    Article  CAS  PubMed  Google Scholar 

  • Veening JG, Coolen LM (1998) Neural activation following sexual behavior in the male and female rat brain. Behav Brain Res 92:181–193

    Article  CAS  PubMed  Google Scholar 

  • Veening JG, Coolen LM, de Jong TR, Joosten HW, de Boer SF, Koolhaas JM, Olivier B (2005) Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur J Pharmacol 526:226–239

    Article  CAS  PubMed  Google Scholar 

  • Vertes RP, Hoover WB (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 508:212–237

    Article  PubMed  Google Scholar 

  • Vertes RP, Crane AM, Colom LV, Bland BH (1995) Ascending projections of the posterior nucleus of the hypothalamus: PHA-L analysis in the rat. J Comp Neurol 359:90–116

    Article  CAS  PubMed  Google Scholar 

  • von Campenhausen H, Mori K (2000) Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur J Neurosci 12:33–46

    Article  Google Scholar 

  • Wang Y, He Z, Zhao C, Li L (2013) Medial amygdala lesions modify aggressive behavior and immediate early gene expression in oxytocin and vasopressin neurons during intermale exposure. Behav Brain Res 245:42–49

    Article  PubMed  Google Scholar 

  • Yokosuka M, Matsuoka M, Ohtani-Kaneko R, Iigo M, Hara M, Hirata K, Ichikawa M (1999) Female-soiled bedding induced fos immunoreactivity in the ventral part of the premammillary nucleus (PMv) of the male mouse. Physiol Behav 68:257–261

    Article  CAS  PubMed  Google Scholar 

  • Zhang WN, Bast T, Feldon J (2001) The ventral hippocampus and fear conditioning in rats: different anterograde amnesias of fear after infusion of N-methyl-d-aspartate or its noncompetitive antagonist MK-801 into the ventral hippocampus. Behav Brain Res 126:159–174

    Article  CAS  PubMed  Google Scholar 

  • Zufall F, Leinders-Zufall T (2007) Mammalian pheromone sensing. Curr Opin Neurobiol 17:483–489

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Author notes

  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

Authors
  1. Bernardita Cádiz-Moretti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcos Otero-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Martínez-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Enrique Lanuza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Enrique Lanuza.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-014-0954-y

Keywords

Search

Navigation