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Connections of the mouse subfornical region of the lateral hypothalamus (LHsf)

Abstract

The lateral hypothalamus is a major integrative hub with a complex architecture characterized by intricate and overlapping cellular populations expressing a large variety of neuro-mediators. In rats, the subfornical lateral hypothalamus (LHsf) was identified as a discrete area with very specific outputs, receiving a strong input from the nucleus incertus, and involved in defensive and foraging behaviors. We identified in the mouse lateral hypothalamus a discrete subfornical region where a conspicuous cluster of neurons express the mu opioid receptor. We thus examined the inputs and outputs of this LHsf region in mice using retrograde tracing with the cholera toxin B subunit and anterograde tracing with biotin dextran amine, respectively. We identified a connectivity profile largely similar, although not identical, to what has been described in rats. Indeed, the mouse LHsf has strong reciprocal connections with the lateral septum, the ventromedial hypothalamic nucleus and the dorsal pre-mammillary nucleus, in addition to a dense output to the lateral habenula. However, the light input from the nucleus incertus and the moderate bidirectional connectivity with nucleus accumbens are specific to the mouse LHsf. A preliminary neurochemical study showed that LHsf neurons expressing mu opioid receptors also co-express calcitonin gene-related peptide or somatostatin and that the reciprocal connection between the LHsf and the lateral septum may be functionally modulated by enkephalins acting on mu opioid receptors. These results suggest that the mouse LHsf may be hodologically and functionally comparable to its rat counterpart, but more atypical connections also suggest a role in consummatory behaviors.

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Availability of data and materials

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Not applicable.

Abbreviations

3N:

Oculomotor N

3V:

3Rd ventricle

A24a:

Anterior cingulate area 24a

A24b:

Anterior cingulate area 24b

A25:

Anterior cingulate area 25

A32:

Anterior cingulate area 32

AAA:

Anterior amygdaloid area

an:

Anterior commissure

aca:

Anterior commissure, anterior limb

Acb:

N accumbens

AcbC:

N accumbens, core

AcbSh:

N accumbens, shell

ACo:

Anterior cortical amygdaloid N

AD:

Anterodorsal thalamic N

AH:

Anterior hypothalamic area

AHiA:

Amygdalohippocampal area, anterior part

AI:

Agranular insular cortex

AOM:

Anterior olfactory N, medial part

Aq:

Cerebral aqueduct

Arc:

Arcuate hypothalamic N

ATg:

Anterior tegmental N

Bar:

Barrington’s N

BDA:

Biotin dextran amine

BLA:

Basolateral amygdaloid N, anterior

BLP:

Basolateral amygdaloid N, posterior

BMA:

Basomedial amygdaloid N, anterior

BMP:

Basomedial amygdaloid N, posterior

BST:

Bed N of the stria terminalis

BSTIA:

BST, intra-amygdaloid

BSTLD:

Lateral BST, dorsal

BSTLP:

Lateral BST, posterior

BSTLV:

Lateral BST, ventral

BSTMA:

Medial BST, anterior part

BSTMP:

Medial BST, posterior

BSTMPI:

Medial BST, postero-intermediate

BSTMPL:

Medial BST, posterolateral

BSTMPM:

Medial BST, posteromedial part

BSTMV:

Medial BST, ventral

cb:

Cerebellum

cc:

Corpus callosum

CeC:

Central amygdaloid N, capsular

CeL:

Central amygdaloid N, lateral

CeM:

Central amygdaloid N, medial

CGA:

Central gray, alpha part

CGB:

Central gray, beta part

CGRP:

Calcitonin gene-related peptide

CM:

Central medial thalamic N

CnF:

Cuneiform N

cp:

Cerebral peduncle

CPu:

Caudate putamen

CTB:

Cholera toxin B subunit

DEn:

Dorsal endopiriform N

DG:

Dentate gyrus

Dk:

N of Darkschewitsch

DLL:

Dorsal N of the lateral lemniscus

dlPAG:

Dorsolateral periaqueductal gray

DM:

Dorsomedial hypothalamic N

dmPAG:

Dorsomedial periaqueductal gray

DR:

Dorsal raphe N

DRC:

Dorsal raphe N, caudal

DRD:

Dorsal raphe N, dorsal

DRL:

Dorsal raphe N, lateral

DRV:

Dorsal raphe N, ventral

DTg:

Dorsal tegmental N

DTT:

Dorsal tenia tecta

EA:

Extended amygdala

f:

Fornix

fmi:

Forceps minor of the corpus callosum

fr:

Fasciculus retroflexus

hbc:

Habenular commissure

HDB:

N of the horizontal limb of the diagonal band

I:

Intercalated nuclei of the amygdala

Im:

Intercalated nucleus of the amygdala, main part

ic:

Internal capsule

IC:

Inferior colliculus

ICjM:

Island of Calleja, major island

IF:

Interfascicular N

IPN:

Interpeduncular N

IsRt:

Isthmic reticular formation

JPLH:

Juxtaparaventricular lateral hypothalamus

La:

Lateral amygdaloid N

LaDL:

Lateral amygdaloid N, dorsolateral part

LaV:

Lateral amygdaloid N, ventral part

LA:

Lateroanterior hypothalamic N

LC:

Locus coeruleus

LDTg:

Laterodorsal tegmental N

LH:

Lateral hypothalamic area

LHAa:

Lateral hypothalamic area, anterior region (Rat)

LHAd:

Lateral hypothalamic area, dorsal region (Rat)

LHAjv:

Lateral hypothalamic area, juxtaventromedial region (Rat)

LHAsfa:

Lateral hypothalamic area, subfornical region, anterior zone (Rat)

LHAsfp:

Lateral hypothalamic area, subfornical region, posterior zone (Rat)

LHb:

Lateral habenular N

LHbL:

Lateral habenular N, lateral part

LHbM:

Lateral habenular N, medial part

LHsf:

Lateral hypothalamus, subfornical region (mouse)

ll:

Lateral lemniscus

lPAG:

Lateral periaqueductal gray

LPBC:

Lateral parabrachial N, central

LPBD:

Lateral parabrachial N, dorsal

LPBE:

Lateral parabrachial N, external

LPBI:

Lateral parabrachial N, internal

LPBS:

Lateral parabrachial N, superior

LPBV:

Lateral parabrachial N, ventral

LPO:

Lateral preoptic area

LS:

Lateral septum

LSD:

Lateral septal N, dorsal

LSI:

Lateral septal N, intermediate

LSV:

Lateral septal N, ventral

LV:

Lateral ventricle

MA3:

Medial accessory oculomotor N

MD:

Mediodorsal thalamic N

MeA:

Medial amygdaloid N

Me5:

Mesencephalic trigeminal N and tract

MeAD:

Medial amygdaloid N, anterodorsal

MeAV:

Medial amygdaloid N, anteroventral

MePD:

Medial amygdaloid N, posterodorsal

MePV:

Medial amygdaloid N, posteroventral

MHb:

Medial habenular N

MiTg:

Microcellular tegmental N

ml:

Medial lemniscus

mlf:

Medial longitudinal fasciculus

ML:

Medial mammillary N, lateral

MM:

Medial mammillary N, medial

MnPO:

Median preoptic N

MnR:

Median raphe N

MO:

Medial orbital cortex

MPA:

Medial preoptic area

MPB:

Medial parabrachial N

MPL:

Medial paralemniscal N

MPO:

Medial preoptic N

mRt:

Mesencephalic reticular formation

MS:

Medial septal N

mt:

Mammillothalamic tract

MT:

Medial terminal N

MTu:

Medial tuberal hypothalamic N

N:

Nucleus

NI:

N Incertus

ot:

Optic tract

Pa:

Paraventricular hypothalamic N

PAG:

Periaqueductal gray

PBP:

Parabrachial pigmented N of the VTA

pc:

Posterior commissure

PDR:

Posterodorsal raphe N

PH:

Posterior hypothalamic N

PIF:

Parainterfascicular N of the VTA

PIL:

Posterior intralaminar thalamic N

Pir:

Piriform cortex

PLCo:

Posterolateral cortical amygdaloid area

pm:

Principal mammillary tract

PMCo:

Posteromedial cortical amygdaloid area PMD: premammillary N, dorsal part

PMnR:

Paramedian raphe N

PMV:

Premammillary N, ventral part

PN:

Paranigral N of the VTA

PoT:

Posterior thalamic nuclear group, triangular

PR:

Prerubral field

PrC:

Precommissural N

PT:

Paratenial thalamic N

PTg:

Pedunculotegmental N

PV:

Paraventricular thalamic N

PVA:

Paraventricular thalamic N, anterior

RCh:

Retrochiasmatic area

RChL:

Retrochiasmatic area, lateral

Re:

Reuniens thalamic N

RLi:

Rostral linear N

RM:

Retromammillary N

RMC:

Red N, magnocellular part

RMM:

Retromammillary N, medial

rPAG:

Rostral periaqueductal gray

RPC:

Red N, parvicellular part

Rt:

Reticular thalamic N

SCh:

Suprachiasmatic N

scp:

Superior cerebellar peduncle

Shi:

Septohippocampal N

Shy:

Septohypothalamic N

sm:

Stria medullaris

SNC:

Substantia nigra, compact part

SNR:

Substantia nigra, reticular part

SO:

Supraoptic N

sox:

Supraoptic decussation

SST:

Somatostatin

st:

Stria terminalis

StHy:

Striohypothalamic N

Su3:

Supraoculomotor periaqueductal gray

Su3C:

Supraoculomotor cap

Sub:

Submedius thalamic N

VDB:

N of the vertical limb of the diagonal band

vlPAG:

Ventrolateral periaqueductal gray

VMH:

Ventromedial hypothalamic N

VMHC:

Ventromedial hypothalamic N, central part

VMHDM:

Ventromedial hypothalamic N, dorsomedial part

VMHVL:

Ventromedial hypothalamic N, ventrolateral part

VMPO:

Ventromedial preoptic N

VO:

Ventral orbital cortex

VP:

Ventral pallidum

vsc:

Ventral spinocerebellar tract

VTA:

Ventral tegmental area

VTAR:

Ventral tegmental area, rostral part

VTg:

Ventral tegmental N

xscp:

Decussation of the superior cerebellar peduncle

ZI:

Zona incerta

References

  1. Ardianto C, Yonemochi N, Yamamoto S, Yang L, Takenoya F, Shioda S, Nagase H, Ikeda H, Kamei J (2016) Opioid systems in the lateral hypothalamus regulate feeding behavior through orexin and GABA neurons. Neuroscience 320:183–193. https://doi.org/10.1016/j.neuroscience.2016.02.002

    CAS  Article  PubMed  Google Scholar 

  2. Baldo BA, Gual-Bonilla L, Sijapati K, Daniel RA, Landry CF, Kelley AE (2004) Activation of a subpopulation of orexin/hypocretin-containing hypothalamic neurons by GABAA receptor-mediated inhibition of the nucleus accumbens shell, but not by exposure to a novel environment. Eur J Neurosci 19(2):376–386

    Article  Google Scholar 

  3. Berthoud HR, Munzberg H (2011) The lateral hypothalamus as integrator of metabolic and environmental needs: from electrical self-stimulation to opto-genetics. Physiol Behav 104(1):29–39. https://doi.org/10.1016/j.physbeh.2011.04.051

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Bester H, Besson JM, Bernard JF (1997) Organization of efferent projections from the parabrachial area to the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 383(3):245–281

    CAS  Article  Google Scholar 

  5. Bodnar RJ (2019) Endogenous opioid modulation of food intake and body weight: implications for opioid influences upon motivation and addiction. Peptides 116:42–62. https://doi.org/10.1016/j.peptides.2019.04.008

    CAS  Article  PubMed  Google Scholar 

  6. Bonnavion P, Mickelsen LE, Fujita A, de Lecea L, Jackson AC (2016) Hubs and spokes of the lateral hypothalamus: cell types, circuits and behaviour. J Physiol 594(22):6443–6462. https://doi.org/10.1113/JP271946

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Canteras NS (2002) The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol Biochem Behav 71(3):481–491. https://doi.org/10.1016/s0091-3057(01)00685-2

    CAS  Article  PubMed  Google Scholar 

  8. 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(2):213–245. https://doi.org/10.1002/cne.903600203

    CAS  Article  PubMed  Google Scholar 

  9. Comoli E, Ribeiro-Barbosa ER, Canteras NS (2000) Afferent connections of the dorsal premammillary nucleus. J Comp Neurol 423(1):83–98. https://doi.org/10.1002/1096-9861(20000717)423:1%3c83::aid-cne7%3e3.0.co;2-3

    CAS  Article  PubMed  Google Scholar 

  10. Dobolyi A, Irwin S, Makara G, Usdin TB, Palkovits M (2005) Calcitonin gene-related peptide-containing pathways in the rat forebrain. J Comp Neurol 489(1):92–119. https://doi.org/10.1002/cne.20618

    CAS  Article  PubMed  Google Scholar 

  11. Dobolyi A, Palkovits M, Usdin TB (2010) The TIP39-PTH2 receptor system: unique peptidergic cell groups in the brainstem and their interactions with central regulatory mechanisms. Prog Neurobiol 90(1):29–59. https://doi.org/10.1016/j.pneurobio.2009.10.017

    CAS  Article  PubMed  Google Scholar 

  12. 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(4):396–433. https://doi.org/10.1002/cne.20002

    Article  PubMed  Google Scholar 

  13. Erbs E, Faget L, Scherrer G, Matifas A, Filliol D, Vonesch JL, Koch M, Kessler P, Hentsch D, Birling MC, Koutsourakis M, Vasseur L, Veinante P, Kieffer BL, Massotte D (2015) A mu-delta opioid receptor brain atlas reveals neuronal co-occurrence in subcortical networks. Brain Struct Funct 220(2):677–702. https://doi.org/10.1007/s00429-014-0717-9

    CAS  Article  PubMed  Google Scholar 

  14. Fillinger C, Yalcin I, Barrot M, Veinante P (2018) Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24a’ and 24b’ in the mouse. Brain Struct Funct 223(4):1747–1778. https://doi.org/10.1007/s00429-017-1585-x

    Article  PubMed  Google Scholar 

  15. Georgescu D, Zachariou V, Barrot M, Mieda M, Willie JT, Eisch AJ, Yanagisawa M, Nestler EJ, DiLeone RJ (2003) Involvement of the lateral hypothalamic peptide orexin in morphine dependence and withdrawal. J Neurosci 23(8):3106–3111

    CAS  Article  Google Scholar 

  16. Goto M, Swanson LW, Canteras NS (2001) Connections of the nucleus incertus. J Comp Neurol 438(1):86–122

    CAS  Article  Google Scholar 

  17. Goto M, Canteras NS, Burns G, Swanson LW (2005) Projections from the subfornical region of the lateral hypothalamic area. J Comp Neurol 493(3):412–438. https://doi.org/10.1002/cne.20764

    Article  PubMed  PubMed Central  Google Scholar 

  18. Groenewegen HJ, Ahlenius S, Haber SN, Kowall NW, Nauta WJ (1986) Cytoarchitecture, fiber connections, and some histochemical aspects of the interpeduncular nucleus in the rat. J Comp Neurol 249(1):65–102. https://doi.org/10.1002/cne.902490107

    CAS  Article  PubMed  Google Scholar 

  19. Hahn JD, Swanson LW (2010) Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res Rev 64(1):14–103. https://doi.org/10.1016/j.brainresrev.2010.02.002

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hahn JD, Swanson LW (2015) Connections of the juxtaventromedial region of the lateral hypothalamic area in the male rat. Front Syst Neurosci 9:66. https://doi.org/10.3389/fnsys.2015.00066

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Jennings JH, Ung RL, Resendez SL, Stamatakis AM, Taylor JG, Huang J, Veleta K, Kantak PA, Aita M, Shilling-Scrivo K, Ramakrishnan C, Deisseroth K, Otte S, Stuber GD (2015) Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 160(3):516–527. https://doi.org/10.1016/j.cell.2014.12.026

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Kincheski GC, Mota-Ortiz SR, Pavesi E, Canteras NS, Carobrez AP (2012) The dorsolateral periaqueductal gray and its role in mediating fear learning to life threatening events. PLoS ONE 7(11):e50361. https://doi.org/10.1371/journal.pone.0050361

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Lantos TA, Gorcs TJ, Palkovits M (1995) Immunohistochemical mapping of neuropeptides in the premamillary region of the hypothalamus in rats. Brain Res Brain Res Rev 20(2):209–249. https://doi.org/10.1016/0165-0173(94)00013-f

    CAS  Article  PubMed  Google Scholar 

  24. Martinez RC, Carvalho-Netto EF, Amaral VC, Nunes-de-Souza RL, Canteras NS (2008) Investigation of the hypothalamic defensive system in the mouse. Behav Brain Res 192(2):185–190. https://doi.org/10.1016/j.bbr.2008.03.042

    Article  PubMed  Google Scholar 

  25. Mendez IA, Ostlund SB, Maidment NT, Murphy NP (2015) Involvement of endogenous enkephalins and beta-endorphin in feeding and diet-induced obesity. Neuropsychopharmacology 40(9):2103–2112. https://doi.org/10.1038/npp.2015.67

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Millhouse OE (1973) The organization of the ventromedial hypothalamic nucleus. Brain Res 55(1):71–87

    CAS  Article  Google Scholar 

  27. Paxinos G, Franklin KBJ (2012) Paxinos and Franklin’s the mouse brain in stereotaxic coordinates, 4th edn. Academic Press

    Google Scholar 

  28. Pecina S, Berridge KC (2005) Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci 25(50):11777–11786. https://doi.org/10.1523/JNEUROSCI.2329-05.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 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(3):387–420. https://doi.org/10.1002/(SICI)1096-9861(19961021)374:3%3c387::AID-CNE6%3e3.0.CO;2-Y

    CAS  Article  PubMed  Google Scholar 

  30. Reppucci CJ, Petrovich GD (2016) Organization of connections between the amygdala, medial prefrontal cortex, and lateral hypothalamus: a single and double retrograde tracing study in rats. Brain Struct Funct 221(6):2937–2962. https://doi.org/10.1007/s00429-015-1081-0

    Article  PubMed  Google Scholar 

  31. Reppucci CJ, Petrovich GD (2018) Neural substrates of fear-induced hypophagia in male and female rats. Brain Struct Funct 223(6):2925–2947. https://doi.org/10.1007/s00429-018-1668-3

    CAS  Article  PubMed  Google Scholar 

  32. Risold PY, Swanson LW (1997) Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24(2–3):115–195

    CAS  Article  Google Scholar 

  33. Sakanaka M, Magari S (1989) Reassessment of enkephalin (ENK)-containing afferents to the rat lateral septum with reference to the fine structures of septal ENK fibers. Brain Res 479(2):205–216

    CAS  Article  Google Scholar 

  34. Sakanaka M, Magari S, Shibasaki T, Inoue N (1989) Co-localization of corticotropin-releasing factor- and enkephalin-like immunoreactivities in nerve cells of the rat hypothalamus and adjacent areas. Brain Res 487(2):357–362

    CAS  Article  Google Scholar 

  35. Sukhov RR, Walker LC, Rance NE, Price DL, Young WS 3rd (1995) Opioid precursor gene expression in the human hypothalamus. J Comp Neurol 353(4):604–622. https://doi.org/10.1002/cne.903530410

    CAS  Article  PubMed  Google Scholar 

  36. Swanson LW (2004) Brain maps: structure of the rat brain. A laboratory guide with printed and electronic templates for data, models and schematics, 3rd edn. Elsevier, Amsterdam

    Google Scholar 

  37. Swanson LW, Cowan WM (1979) The connections of the septal region in the rat. J Comp Neurol 186(4):621–655. https://doi.org/10.1002/cne.901860408

    CAS  Article  PubMed  Google Scholar 

  38. Swanson LW, Sanchez-Watts G, Watts AG (2005) Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci Lett 387(2):80–84. https://doi.org/10.1016/j.neulet.2005.06.066

    CAS  Article  PubMed  Google Scholar 

  39. Thompson RH, Swanson LW (2010) Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc Natl Acad Sci U S A 107(34):15235–15239. https://doi.org/10.1073/pnas.1009112107

    Article  PubMed  PubMed Central  Google Scholar 

  40. Urstadt KR, Stanley BG (2015) Direct hypothalamic and indirect trans-pallidal, trans-thalamic, or trans-septal control of accumbens signaling and their roles in food intake. Front Syst Neurosci 9:8. https://doi.org/10.3389/fnsys.2015.00008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51(1):32–58. https://doi.org/10.1002/syn.10279

    CAS  Article  PubMed  Google Scholar 

  42. Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407(4):555–582

    CAS  Article  Google Scholar 

  43. Vertes RP, Linley SB, Hoover WB (2015) Limbic circuitry of the midline thalamus. Neurosci Biobehav Rev 54:89–107. https://doi.org/10.1016/j.neubiorev.2015.01.014

    Article  PubMed  PubMed Central  Google Scholar 

  44. Williams RG, Dockray GJ (1983) Distribution of enkephalin-related peptides in rat brain: immunohistochemical studies using antisera to met-enkephalin and met-enkephalin Arg6Phe7. Neuroscience 9(3):563–586. https://doi.org/10.1016/0306-4522(83)90175-6

    CAS  Article  PubMed  Google Scholar 

  45. Zahm DS, Parsley KP, Schwartz ZM, Cheng AY (2013) On lateral septum-like characteristics of outputs from the accumbal hedonic “hotspot” of Pecina and Berridge with commentary on the transitional nature of basal forebrain “boundaries.” J Comp Neurol 521(1):50–68. https://doi.org/10.1002/cne.23157

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Chronobiotron (UMS3415) for animal housing and animal care, and the imaging platform of INCI (UPS3156) for their assistance.

Funding

This work was supported by the Centre National de la Recherche Scientifique (contract UPR3212), the University of Strasbourg and the NeuroTime Erasmus Mundus Joint Doctorate Program.

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Correspondence to Pierre Veinante or Dominique Massotte.

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All experiments were approved by the Comité d’éthique en Matière d’expérimentation animale (authorization number 2015304113547b (APAFIS #300.02)) and conducted in agreement with the European Communities Council Directive 2010/63/EU for animal experiments.

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Ugur, M., Doridot, S., la Fleur, S.E. et al. Connections of the mouse subfornical region of the lateral hypothalamus (LHsf). Brain Struct Funct 226, 2431–2458 (2021). https://doi.org/10.1007/s00429-021-02349-x

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Keywords

  • Mu opioid receptor
  • Anterograde tracing
  • Retrograde tracing
  • Defensive behavior
  • Feeding