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Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24aʹ and 24bʹ in the mouse

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Abstract

The anterior cingulate cortex (ACC), constituted by areas 25, 32, 24a and 24b in rodents, plays a major role in cognition, emotion and pain. In a previous study, we described the afferents of areas 24a and 24b and those of areas 24aʹ and 24bʹ of midcingulate cortex (MCC) in mice and highlighted some density differences among cingulate inputs (Fillinger et al., Brain Struct Funct 222:1509–1532, 2017). To complete this connectome, we analyzed here the efferents of ACC and MCC by injecting anterograde tracers in areas 24a/24b of ACC and 24aʹ/24bʹ of MCC. Our results reveal a common projections pattern from both ACC and MCC, targeting the cortical mantle (intracingulate, retrosplenial and parietal associative cortex), the non-cortical basal forebrain, (dorsal striatum, septum, claustrum, basolateral amygdala), the hypothalamus (anterior, lateral, posterior), the thalamus (anterior, laterodorsal, ventral, mediodorsal, midline and intralaminar nuclei), the brainstem (periaqueductal gray, superior colliculus, pontomesencephalic reticular formation, pontine nuclei, tegmental nuclei) and the spinal cord. In addition to an overall denser ACC projection pattern compared to MCC, our analysis revealed clear differences in the density and topography of efferents between ACC and MCC, as well as between dorsal (24b/24bʹ) and ventral (24a/24aʹ) areas, suggesting a common functionality of these two cingulate regions supplemented by specific roles of each area. These results provide a detailed analysis of the efferents of the mouse areas 24a/24b and 24aʹ/24bʹ and achieve the description of the cingulate connectome, which bring the anatomical basis necessary to address the roles of ACC and MCC in mice.

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Abbreviations

3:

3rd ventricle

4:

4th ventricle

7n:

Facial nerve

aca:

Anterior commissure, anterior part

AcbC:

Accumbens N, core region

AcbSh:

Accumbens N, shell region

ACC:

Anterior cingulate cortex

AD:

Anterodorsal thalamic N

AHC:

Anterior hypothalamic area, central part

AHP:

Anterior hypothalamic area, posterior part

AI:

Agranular insular cortex

AM:

Anteromedial thalamic N

AOM:

Anterior olfactory N, medial part

AOP:

Anterior olfactory N, posterior part

APT:

Anterior pretectal N

aq:

Aqueduct

Au:

Primary auditory cortex

AV:

Anteroventral thalamic N

Bar:

Barrington’s N

BLA:

Basolateral amygdaloid N, anterior part

CA1:

Field CA1 of the hippocampus

cc:

Corpus callosum

cg:

Cingulum

CG:

Central gray

Cl:

Claustrum

CL:

Centrolateral thalamic N

CM:

Central medial thalamic N

cp:

Cerebral peduncle

CPu:

Caudate putamen

dhc:

Dorsal hippocampal commissure

DLG:

Dorsal lateral geniculate N

DpG:

Deep gray layer of the superior colliculus

DpWh:

Deep white layer of the superior colliculus

DR:

Dorsal raphe nucleus

DS:

Dorsal subiculum

DTT:

Dorsal tenia tecta

ec:

External capsule

Ect:

Ectorhinal cortex

eml:

External medullary lamina

Ent:

Enthorinal cortex

f:

Fornix

fmi:

Forceps minor of the corpus callosum

fmj:

Forceps major of the corpus callosum

fr:

Fasciculus retroflexus

GiA:

Gigantocellular reticular N, alpha part

GiV:

Gigantocellular reticular N, ventral part

GP:

Globus pallidus

HDB:

Diagonal band of Broca, horizontal limb

IAD:

Interanterodorsal thalamic N

IAM:

Interanteromedial thalamic N

ic:

Internal capsule

IMD:

Intermediodorsal thalamic N

InG:

Intermediate gray layer of the superior colliculus

InWh:

Intermediate white layer of the superior colliculus

IP:

Interpedoncular N

LAcbSh:

Lateral accumbens, shell region

LC:

Locus coeruleus

LD:

Laterodorsal thalamic N

LDDM:

LD, dorsomedial part

LDTg:

Laterodorsal tegmental N

LDVL:

LD, ventrolateral part

LH:

Lateral hypothalamic area

LHb:

Lateral habenula

LO:

Lateral orbital cortex

LP:

Lateral posterior thalamic N

LPLR:

Lateral posterior thalamic N, laterorostral part

LPMR:

Lateral posterior thalamic N, mediorostral part

LPO:

Lateral preoptic area

LSI:

Lateral septal N, intermediate part

LV:

Lateral ventricle

M2:

Secondary motor cortex

MB:

Mammillary bodies

MCC:

Midcingulate cortex

MD:

Mediodorsal thalamic N

MDC:

Mediodorsal thalamic N, central part

MDL:

Mediodorsal thalamic N, lateral part

MDM:

Mediodorsal thalamic N, medial part

me5:

Mesencephalic trigeminal tract

MHb:

Medial habenular N

MnR:

Median raphe N

MO:

Medial orbital cortex

MPT:

Medial pretectal N

mRt:

Mesencephalic reticular formation

MS:

Medial septal N

mt:

Mamillotegmental tract

N:

Nucleus

Op:

Optic nerve layer of the superior colliculus

opt:

Optic tract

PaF:

Parafascicular thalamic N

PAG:

Periaqueductal gray

PAGdl:

Periaqueductal gray, dorsolateral part

PAGdm:

Periaqueductal gray, dorsomedial part

PAGl:

Periaqueductal gray, lateral part

PAGvl:

Periaqueductal gray, ventrolateral part

PAGr:

Periaqueductal gray, rostral part

PC:

Paracentral thalamic N

PH:

Posterior hypothalamic N

pm:

Principal mammillary tract

PMnR:

Paramedian raphe N

Pn:

Pontine N

PnC:

Pontine reticular N, caudal part

PnO:

Pontine reticular N, oral part

Po:

Posterior thalamic N group

Post:

Postsubiculum

PrCnF:

Precuneiform area

PrG:

Pregeniculate N of the prethalamus

PR:

Prerubral field

PRh:

Perirhinal cortex

PT:

Paratenial thalamic N

PtA:

Parietal associative cortex

PTg:

Pedunculotegmental N

PV:

Paraventricular thalamic N

PVH:

Hypothalamic paraventricular N

py:

Pyramidal tract

Re:

Reuniens thalamic N

Rh:

Rhomboid thalamic N

RIP:

Raphe interpositus N

RM:

Retromamillary N

RMg:

Raphe magnus N

RPa:

Raphe pallidus N

RSC:

Retrosplenial cortex

Rt:

Reticular N

RVM:

Ventromedial medulla region

S1:

Primary somatosensory cortex

SC:

Superior colliculus

scp:

Superior cerebellar peduncle

sm:

Stria medullaris

SNc:

Substantia nigra, pars compacta

SNr:

Substantia nigra, pars reticulata

st:

Stria terminalis

STh:

Subthalamic N

Sub:

Submedius N

SuG:

Superficial gray layer of the superior colliculus

TeA:

Temporal association cortex

ts:

Tectospinal tract

Tu:

Olfactory tubercle

V1:

Primary visual cortex

V2L:

Secondary visual cortex, lateral area

V2M:

Secondary visual cortex, medial area

V2ML:

Secondary visual cortex, mediolateral area

V2MM:

Secondary visual cortex, mediomedial area

VA:

Ventral anterior thalamic N

VDB:

Diagonal band of Broca, vertical limb

VL:

Ventrolateral thalamic N

VM:

Ventromedial thalamic N

VO:

Ventral orbital cortex

VP:

Ventral pallidum

VPL:

Ventral posterolateral thalamic N

VPM:

Ventral posteromedial thalamic N

VTA:

Ventral tegmental area

VTg:

Ventral tegmental N

ZI:

Zona incerta

ZID:

ZI, dorsal part

ZIR:

ZI, rostral part

ZIV:

ZI, ventral part

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Acknowledgements

We thank the Chronobiotron (UMS3415) for animal housing and animal care. This work was supported by the Centre National de la Recherche Scientifique (contract UPR3212), the University of Strasbourg and by a NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation.

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Fillinger, C., Yalcin, I., Barrot, M. et al. Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24aʹ and 24bʹ in the mouse. Brain Struct Funct 223, 1747–1778 (2018). https://doi.org/10.1007/s00429-017-1585-x

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