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Orexinergic innervation of the extended amygdala and basal ganglia in the rat

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Abstract

The orexinergic system interacts with several functional states of emotions, stress, hunger, wakefulness and behavioral arousal through four pathways originating in the lateral hypothalamus (LH). Hundreds of orexinergic efferents have been described by tracing studies and direct immunohistochemistry of orexin in the forebrain, olfactory regions, hippocampus, amygdala, septum, basal ganglia, thalamus, hypothalamus, brain stem and spinal cord. Most of these tracing studies investigated the whole orexinergic projection to all regions of the intracranial part of the CNS. To identify the orexinergic efferents at the subnuclear level of resolution, we focussed on the orexinergic target in the amygdala, which is substantially involved in the LH output and contributes mostly to the functional outcome of the orexinergic system and the basal ganglia. Immunohistochemical identification of axonal orexin A and orexin B in male adult rats has been performed on serial sections. In the extended amygdala many new orexinergic targets were found in the anterior amygdaloid area (dense), anterior cortical nucleus (moderate), amygdalostriatal transition region (moderate), basolateral regions (moderate), basomedial nucleus (moderate), several bed nucleus of the stria terminals regions (few to dense), central amygdaloid subdivisions (dense), posteromedial cortical nucleus (moderate) and medial amygdaloid subnuclei (dense). Furthermore, the entopeduncular nucleus has been newly identified as another target for orexinergic fibers with a high density. These results suggest that subdivisions and subnuclei of the extended amygdala are specific targets of the orexinergic system.

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Abbreviations

3:

Oculomotor nc.

3V:

Third ventricle

4:

Trochlear nc.

6:

Abducens nc.

7:

Facial nc.

10:

Dors. motor nc. vagus

12S:

Hypoglossal nc.

AAA:

Ant. amygdaloid area

AAD:

Ant. amygdaloid area dors. p.

AASh:

Ant. amygdaloid area shell area

AAV:

Ant. amygdaloid area vent. p.

ABC:

Avidin–biotin–horseradish peroxidase

Ac:

Accumbens nc.

AcbC:

Accumbens nc. core

AcbSh:

Accumbens nc. shell

ACo:

Ant. cortical amygdaloid nc.

AD:

Anterodors. thalamic nc.

AHAA:

Ant. hypothalamic area ant. p.

AHA:

Ant. hypothalamic area

AHi:

Amygdalohippocampal area

AHiAL:

Amygdalohippocampal area anterolateral p.

AHn:

Ant. hypothalamic nc.

AI:

Agranular insular cortex

Am:

Amygdala

AM:

Anteromed. thalamic nc.

Amb:

Ambiguus nc.

AON:

Ant. olfactory nc.

AP:

Area postrema

APT:

Ant. pretectal nc.

Arc:

Arcuate nc.

AStr:

Amygdalostriatal transition area

ATg:

Ant. tegmental nc.

AV:

Anterovent. thalamic nc.

AVPe:

Anterovent. periventricular nc.

B:

Bregma

B9:

B9 serotonin cells

BAC:

Bed nc. ant. commissure

Bar:

Barringtons nc.

BIC:

Nc. brachium inferior colliculus

Ll:

Lat. lemniscus

BLA:

Ant. basolat. nc.

BLP:

Posterior basolat. nc.

BLV:

Ventral basolat. nc.

BL:

Basolat. nc.

BMA:

Ant. basomed. nc.

BMP:

Posterior basomed. nc.

BM:

Basomed. nc.

BST:

Bed nc. stria terminalis

BSTAL:

BST ant. lat. area

BSTAM:

BST ant. med. p.

BSTIA:

BST intraamygdaloid div.

BSTLD:

BST lat. div. dors. p.

BSTLI:

BST lat. div. intermediate p.

BSTLJ:

BST lat. div. juxtacapsular p.

BSTLP:

BST lat. div. posterior p.

BSTLV:

BST lat. div. vent. p.

BSTL:

BST lat. div.

BSTMA:

BST med. div. ant. p.

BSTMPI:

BST med. div. posterointermediate p.

BSTMPL:

BST med. div. posterolat. p.

BSTMPM:

BST med. div. posteromed. p.

BSTMV:

BST med. div. vent. p.

BSTM:

BST med. div.

BSTP:

BST posterior div.

BSTV:

BST posterior div. vent. nc.

BSTd:

BST dors. nc.

BSTrL:

BST lat. div. rostral p.

BSTrm:

BST med. div. rostral p.

CA1:

Field CA1 hippocampus

CA2:

Field CA2 hippocampus

CA3:

Field CA3 hippocampus

CAn:

Cortical amygdaloid nc.

CCL1:

Cerebral cortex layer 1

CCL2:

Cerebral cortex layer 2

CCL3:

Cerebral cortex layer 3

CCL4:

Cerebral cortex layer 4

CCL5:

Cerebral cortex layer 5

CCL6:

Cerebral cortex layer 6

Ce:

Central amygdaloid nc.

CeC:

Capsular p.

CeL:

Central amygdaloid nc. lat. div.

CeM:

Central amygdaloid nc. med. div.

CERC:

Cerebellar cortex

Cg:

Cingulate cortex

CG:

Central gray

CIC:

Central nc. inferior colliculus

Cl:

Claustrum

CL:

Centrolat. thalamic nc.

CM:

Central med. thalamic nc.

CnF:

Cuneiforme nc.

COS:

Cochlear system

cp:

Cerebral peduncle

CPu:

Caudate putamen

cpv3:

choroid plexus 3rd ventricle

cpv4:

choroid plexus 4th ventricle

CVLM:

Caudal ventrolat. medulla

D3V:

Dorsal 3rd ventricle

DA:

Dors. hypothalamic area

DCIC:

Dors. cortex inferior colliculus

DC:

Dors. cochlear nc.

DEn:

Dors. endopiriform nc.

DG:

Dentate gyrus

Dk:

Nc. Darkschewitsch

DLGl:

Dors. geniculate nc. lat. p.

DM:

Dorsomed. hypothalamic nc.

DMDM:

Dorsomed. hypothalamic nc. dorsomed. p.

DNC:

Deep cerebellar nuclei

DPGi:

Dors. paragigantocellular nc.

DpMe:

Deep mesencephalic nc.

DPPn:

Dors. peduncular pontine nc.

DR:

Dors. raphe nc.

DRC:

Dors. raphe nc. caudal p.

DRcep:

Dors. raphe nc. central p.

DRI:

Dors. raphe nc. interfascicular p.

DRlw:

Dors. raphe nc. lat. wing

DRr:

Dors. raphe nc. rostral p.

DTg:

Dors. tegmental nc.

DTgC:

Dors. tegmental nc. central p.

E:

Ependyma and subependymal layer

ECIC:

External cortex inferior colliculus

EnN:

Endopiriform system

EP:

Entopeduncular nucleus

Ent:

Entorhinal cortex

f:

Fornix

F:

Nc. fields Forel

Fl:

Flocculus

FrA:

Frontal association cortex

FS:

Fundus striatum

G:

Gelatinosus thalamic nc.

Ge5:

Gelatinous layer caudal spinal trigeminal nc.

Gi:

Gigantocellular reticular nc.

GI:

Granular insular cortex

GiA:

Gigantocellular reticular nc. alpha p.

GiV:

Gigantocellular reticular nc. vent. p.

GN:

Geniculate nucleus

GP:

Globus pallidus

Gra:

Gracile nc.

GraD:

Gracile nc. dors. p.

HDB:

Nc. horizontal limb diagonal band

HIPP:

Hippocampus

I:

Intercalated nc. amygdala

IAM:

Interoanteromed. thalamic nc.

Ilc:

Internal capsule

ICj:

Islands Calleja

ICOL:

Inferior colliculus

IF:

Interfascicular nc.

IGL:

Intergeniculate leaf

IG:

Indusium griseum

ILN:

Intralaminar nuclei

IMD:

Intermediodors. thalamic nc.

IM:

Intercalated amygdaloid nc. main p.

InC:

Interstitial nc. Cajal

i.p.:

intra peritoneal

IP:

Interpeduncular nc.

IPA:

Interpeduncular nc. apical subnc.

IPDM:

Interpeduncular nc. dorsomed. subnc.

IPI:

Interpeduncular nc. intermediate subnc.

IPL:

Interpeduncular nc. lat. subnc.

IPR:

Interpeduncular nc. rostral subnc.

IPRc:

Interpeduncular nc. central subnc.

IRt:

Intermediate reticular nc.

KF:

Koelliker Fuse nc.

LA:

Lat. amygdaloid nc.

LAH:

Lateroant. hypothalamic nc.

LC:

Locus coeruleus

LD:

Laterodors. thalamic nc.

LDTg:

Laterodors. tegmental nc.

LG:

Lat. geniculate complex

LGP:

Lat. globus pallidus

LH:

Lat. hypothalamic area

LHb:

Lat. habenular nc.

LIR:

Linear nc. raphe

LM:

Lat. mammillary nc.

LOT:

Nc. lat. olfactory tract

LP:

Lat. posterior thalamic nc.

LPB:

Lat. parabrachial nc.

LPGi:

Lat. paragigantocellular nc.

LPN:

Lat. preoptic nc.

LPO:

Lat. preoptic area

LRt:

Lat. reticular nc.

LS:

Lat. septal nc.

LSD:

Lat. septal nc. dors. p.

LSI:

Lat. septal nc. intermediate p.

LSV:

Lat. septal nc. vent. p.

LV:

Lateral ventricle

MCPO:

Magnocellular preoptic nc.

MDC:

Mediodors. thalamic nc. central p.

MDL:

Mediodors. thalamic nc. lat. p.

MDM:

Mediodors. thalamic nc. med. p.

MD:

Mediodors. thalamic nc.

MdD:

Medullary reticular nc.

MdDd:

Medullary reticular nc. dors. p.

MdV:

Medullary reticular nc. vent. p.

MED:

Med. group dors. thalamus

Me:

Med. amygdaloid nc.

ME:

Median eminence

Me5:

Mesencephalic trigeminal nc.

MeAD:

Med. amygdaloid nc. anterodors. p.

MePD:

Med. amygdaloid nc. posterodors. p.

MePV:

Med. amygdaloid nc. posterovent. p.

MGP:

Med. globus pallidus

MG:

Med. geniculate nc.

MHb:

Med. habenular nc.

MM:

Med. mammillary nc. med. p.

MMn:

Med. mammillary nc.

MMnm:

Med. mammillary nc. median p.

MnPO:

Median preoptic nc.

MnR:

Median raphe nc.

Mo5:

Motor trigeminal nc.

MOB:

Olfactory bulb A16

MPA:

Med. preoptic area

MPB:

Med. parabrachial nc.

MPO:

Med. preoptic nc.

MPT:

Med. pretectal nc.

MRF:

Mesencephalic reticular formation

MS:

Med. septal nc.

mt:

Mammillothalamic tract

NADPHd:

Nicotinamide adenine dinucleotide hydrogen phosphate diaphorase

NGS:

Normal goat serum

NLL:

Nuclei lat. lemniscus

ON:

Olivary nc.

ONn:

Olfactory nuclei

opt:

Optic tract

OrC:

Orbital cortex

OT:

Nc. optic tract

OX:

Orexin, hypocretin

OX-A:

Orexin A (Hypocretin 1)

OX-B:

Orexin B (Hypocretin 2)

OX1R:

Orexin 1 receptor

OX2R:

Orexin 2 receptor

Pa:

Paraventricular nc.

PaAM:

Paraventricular hypothalamic nc. magnocellular p.

PAG:

Periaqueductal gray

PaPc:

Paraventricular hypothalamic nc. parvicellular p.

PB:

Parabrachial nc.

PBG:

Parabigeminal nc.

PBP:

Parabrachial pigmented nc.

PBS:

Phosphate buffered saline

PC:

Paracentral thalamic nc.

PCom:

Nc. posterior commissure

PCRt:

Parvicellular reticular nc.

PDP:

Posterodors. preoptic nc.

Pe:

Periventricular hypothalamic nc.

PeF:

Perifornical area

PeP:

Posterior periventricular nc.

PePO:

Preoptic periventricular nc.

Pir:

Piriform cortex

PF:

Parafascicular thalamic nc.

PFx:

Lat. hypothalamic area perifornical p.

PG:

Pontine gray

PHA:

Posterior hypothalamic area

PLCo:

Posterolat. cortical nc.

PLH:

Posterolat. hypothalamus

PMCo:

Posteromed. cortical nc.

PMn:

Paramedian reticular nc.

PN:

Paranigral nc.

PnO:

Pontine reticular nc. oral p.

PnR:

Pontine raphe nc.

Po:

Posterior thalamic nuclear group

PP:

Peripeduncular nc.

PPit:

Posterior lobe pituitary

PPN:

Peduncularpontine nc.

PPT:

Posterior pretectal nc.

PPTg:

Pedunculopontine tegmental nc.

Pr:

Prepositus nc.

Pr5:

Principal sensory trigeminal nc.

PRN:

Pontine reticular nc.

PS:

Parastriatal nc.

PSTh:

Parasubthalamic nucleus

PT:

Paratenial thalamic nc.

PtA:

Parietal association cortex

PV:

Paraventricular thalamic nc.

PVHd:

Paraventricular hypothalamic nc. descending div.

R:

Red nc.

RAN:

Raphe nuclei

RCh:

Retrochiasmatic area

Re:

Reuniens thalamic nc.

RETn:

Reticulotegmental nc.

Rh:

Rhomboid thalamic nc.

RhN:

Rhomboid nc.

RLi:

Rostral linear nc. raphe

RMg:

Raphe magnus nc.

Ro:

Nc. Roller

ROb:

Raphe obscurus nc.

RPa:

Raphe pallidus nc.

Rt:

Reticular thalamic nc.

RVLM:

Rostral ventrolat. medulla

S:

Subiculum

SC:

Superior colliculus

SCh:

Suprachiasmatic nc.

SCO:

Subcommissural organ

SFO:

Subfornical organ

SFi:

Septofimbrial nc.

SHi:

Septohippocampal nc.

SHy:

Septohypothalamic nc.

SI:

Substantia innominata

sm:

Stria medullaris thalamus

SMT:

Submammillothalamic nc.

SN:

Substantia nigra A9

SNC:

Substantia nigra compact p.

SNL:

Substantia nigra lat. p.

SNR:

Substantia nigra reticular p.

SO:

Supraoptic nc.

Sol:

Nc. solitary tract

sox:

Supraoptic decussation

Sp5C:

Spinal trigeminal nc. caudal p.

Sp5O:

Spinal trigeminal nc. oral p.

Sp5nc:

Spinal trigeminal nc.

SPF:

Subparafascicular thalamic nc.

STh:

Subthalamic nc.

STLD:

Equivalent to BSTLD

STLJ:

Equivalent to BSTLJ

STLP:

Equivalent to BSTLP

STLV:

Equivalent to BSTLV

STMA:

Equivalent to BSTMA

STMV:

Equivalent to BSTMV

SubI:

Subincertal nc.

SuM:

Supramammillar nc.

SuOLi:

Superior olive

TC:

Tuber cinereum area

TGAC:

Central tegmental field

TM:

Tuberomammillary nc.

TS:

Triangular septal nc.

TT:

Tenia tecta

TuLH:

Tuberal region lat. hypothalamus

TuO:

Olfactory tubercle

Tz:

Nc. trapezoid body

VC:

Ventral cochlear nc.

VDB:

Nc. vertical limb diagonal band

VES:

Vestibular system

VLG:

Ventral lat. geniculate nc.

VLPAG:

Ventrolat. periaqueductal gray

VL:

Ventrolat. thalamic nc.

VMHA:

Ventromed. hypothalamic nc. ant. p.

VMHP:

Ventromed. hypothalamic nc. posterior p

VMH:

Ventromed. hypothalamic nc.

VPPn:

Ventral peduncular pontine nc.

VP:

Ventral pallidum

VR:

Visual regions

VTA:

Ventral tegmental area A10

VTg:

Ventral tegmental nc.

Vnc:

Vestibular nuclei

ZI:

Zona incerta

ZID:

Zona incerta dors. p.

ZIV:

Zona incerta vent. p.

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Acknowledgments

This article is dedicated to the memory of our friend and colleague, Prof. Dr. Kamen Usunoff, who sadly passed away on February 28, 2009. He was an outstanding personality with an enormous experience in neuroanatomy and the whole field of neuroscience. Kamen has provided substantial work to this study. We thank Frauke Winzer for expert technical assistance and Alexander Hawlitschka for sharing his knowledge on immunohistochemical methods.

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Authors and Affiliations

  1. Institute of Anatomy, University of Rostock, P. O. Box 100888, 18055, Rostock, Germany

    Oliver Schmitt, Peter Eipert & Andreas Wree

  2. Department of Anatomy and Histology, Faculty of Medicine, Medical University, 1431, Sofia, Bulgaria

    Kamen G. Usunoff & Nikolai E. Lazarov

  3. Institute of Neurobiology, Bulgarian Academy of Sciences, 1113, Sofia, Bulgaria

    Kamen G. Usunoff & Dimitar E. Itzev

  4. Albrecht Kossel Institute for Neuroregeneration, University of Rostock, 18147, Rostock, Germany

    Arndt Rolfs

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  1. Oliver Schmitt
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  2. Kamen G. Usunoff
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  7. Andreas Wree
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Correspondence to Oliver Schmitt.

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Abbreviations used within the abbreviation list: ant.: anterior, div.: division, dors: dorsal lat.: lateral, med.: medial, p.: part, post.: posterior, nc.: nucleus.

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Schmitt, O., Usunoff, K.G., Lazarov, N.E. et al. Orexinergic innervation of the extended amygdala and basal ganglia in the rat. Brain Struct Funct 217, 233–256 (2012). https://doi.org/10.1007/s00429-011-0343-8

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