Skip to main content
SpringerLink
Log in

Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse

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

Abstract

Areas 24a and 24b of the anterior cingulate cortex (ACC) play a major role in cognition, emotion and pain. While their connectivity has been studied in primate and in rat, a complete mapping was still missing in the mouse. Here, we analyzed the afferents to the mouse ACC by injecting retrograde tracers in the ventral and dorsal areas of the ACC (areas 24a/b) and of the midcingulate cortex (MCC; areas 24a′/b′). Our results reveal inputs from five principal groups of structures: (1) cortical areas, mainly the orbital, medial prefrontal, retrosplenial, parietal associative, primary and secondary sensory areas and the hippocampus, (2) basal forebrain, mainly the basolateral amygdaloid nucleus, the claustrum and the horizontal limb of the diagonal band of Broca, (3) the thalamus, mainly the anteromedial, lateral mediodorsal, ventromedial, centrolateral, central medial and reuniens/rhomboid nuclei, (4) the hypothalamus, mainly the lateral and retromammillary areas, and (5) the brainstem, mainly the monoaminergic centers. The neurochemical nature of inputs from the diagonal band of Broca and brainstem centers was also investigated by double-labeling, showing that only a part of these afferents were cholinergic or monoaminergic. Comparisons between the areas indicate that areas 24a and 24b receive qualitatively similar inputs, but with different densities. These differences are more pronounced when comparing the inputs to ACC’s areas 24a/24b to the inputs to MCC’s areas 24a′/24b′. These results provide a complete analysis of the afferents to the mouse areas 24a/24b and 24a′/24b′, which shows important similarity with the connectivity of homologous areas in rats, and brings the anatomical basis necessary to address the roles of cingulate areas in mice.

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

Similar content being viewed by others

Abbreviations

3n:

Oculomotor nerve

5-HT:

5-Hydroxytryptamine

ACC:

Anterior cingulate cortex

AD:

Anterodorsal thalamic N

AH:

Anterior hypothalamic area

AI:

Agranular insular cortex

AM:

Anteromedial thalamic N

Au:

Primary auditory cortex

AV:

Anteroventral thalamic N

BDA:

Biotinylated dextran amine

BL:

Basolateral amygdaloid N

BLA:

Basolateral amygdaloid N, anterior part

BLP:

Basolateral amygdaloid N, posterior part

C:

Caudal

CA1:

Amon’s horn 1

CG:

Central gray

Cg1:

Anterior cingulate cortex, dorsal

Cg2:

Anterior cingulate cortex, ventral

ChAT:

Choline acetyltransferase

Cl:

Claustrum

CL:

Centrolateral thalamic N

CM:

Central medial thalamic N

cp:

Cerebral peduncle

CPu:

Caudate putamen

CTb:

β Subunit of choleric toxin

DI:

Dysgranular insular cortex

DR:

Dorsal raphe nucleus

ec:

External capsula

Ect:

Ectorhinal cortex

Ent:

Entorhinal cortex

FG:

FluoroGold®

fmi:

Forceps minor of the corpus callosum

fmj:

Forceps major of the corpus callosum

GI:

Granular insular cortex

GP:

Globus pallidus

HDB:

Diagonal band of Broca, horizontal limb

IAD:

Interanterodorsal thalamic N

IAM:

Interanteromedial thalamic N

ic:

Internal capsule

IG:

Infragranular

La:

Lateral amygdaloid N

LC:

Locus coeruleus

LD:

Laterodorsal thalamic N

LH:

Lateral hypothalamic area

Li:

Linear raphe

LO:

Lateral orbital cortex

LP:

Lateral posterior thalamic N

LPMR:

Lateral posterior thalamic N, mediorostral part

M1:

Primary motor cortex

M2:

Secondary motor cortex

MCC:

Midcingulate cortex

MD:

Mediodorsal thalamic N

me5:

Mesencephalic trigeminal tract

MD:

Mediodorsal thalamic N

MDL:

Mediodorsal thalamic N, lateral part

ml:

Medial lemniscus

MnR:

Median raphe N

MO:

Medial orbital cortex

mPFC:

Medial prefrontal cortex

MS:

Medial septal N

N:

Nucleus

PaF:

Parafascicular thalamic N

PBP:

Parabrachial pigmented N of the VTA

PC:

Paracentral thalamic N

PH:

Posterior hypothalamic N

PLH:

Peduncular lateral hypothalamus

pMnR:

Paramedian raphe N

Po:

Posterior thalamic N group

PRh:

Perirhinal cortex

PT:

Paratenial thalamic N

PtA:

Parietal associative cortex

PV:

Paraventricular thalamic N

R:

Rostral

Re:

Reuniens thalamic N

Rh:

Rhomboid thalamic N

RM:

Retromamillary N

RS:

Retrosplenial cortex

S1:

Primary somatosensory cortex

S2:

Secondary somatosensory cortex

SG:

Supragranular

sm:

Stria medullaris

SNc:

Substantia nigra, pars compacta

SNr:

Substantia nigra, pars reticulata

TeA:

Temporal association cortex

TH:

Tyrosine hydroxylase

V1:

Primary visual cortex

V2L:

Secondary visual cortex, lateral area

V2M:

Secondary visual cortex, medial area

VA:

Ventral anterior thalamic N

VDB:

Diagonal band of Broca, vertical limb

VM:

Ventromedial thalamic N

VO:

Ventral orbital cortex

VP:

Ventral pallidum

VTA:

Ventral tegmental area

References

  • Abiri D, Douglas CE, Calakos KC, Barbayannis G, Roberts A, Bauer EP (2014) Fear extinction learning can be impaired or enhanced by modulation of the CRF system in the basolateral nucleus of the amygdala. Behav Brain Res 271:234–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aggleton JP, Nelson AJ (2015) Why do lesions in the rodent anterior thalamic nuclei cause such severe spatial deficits? Neurosci Biobehav Rev 54:131–144

    Article  PubMed  PubMed Central  Google Scholar 

  • Alba-Delgado C, Llorca-Torralba M, Horrillo I, Ortega JE, Mico JA, Sanchez-Blazquez P, Meana JJ, Berrocoso E (2013) Chronic pain leads to concomitant noradrenergic impairment and mood disorders. Biol Psychiatry 73:54–62

    Article  CAS  PubMed  Google Scholar 

  • Apkarian AV, Bushnell MC, Treede RD, Zubieta JK (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9:463–484

    Article  PubMed  Google Scholar 

  • Bachevalier J, Meunier M, Lu MX, Ungerleider LG (1997) Thalamic and temporal cortex input to medial prefrontal cortex in rhesus monkeys. Exp Brain Res 115:430–444

    Article  CAS  PubMed  Google Scholar 

  • Bair MJ, Robinson RL, Katon W, Kroenke K (2003) Depression and pain comorbidity: a literature review. Arch Intern Med 163:2433–2445

    Article  PubMed  Google Scholar 

  • Baldauf KJ, Royal JM, Hamorsky KT, Matoba N (2015) Cholera toxin B: one subunit with many pharmaceutical applications. Toxins (Basel) 7:974–996

    Article  CAS  Google Scholar 

  • Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375

    Article  CAS  PubMed  Google Scholar 

  • Barthas F, Sellmeijer J, Hugel S, Waltisperger E, Barrot M, Yalcin I (2015) The anterior cingulate cortex is a critical hub for pain-induced depression. Biol Psychiatry 77:236–245

    Article  PubMed  Google Scholar 

  • Benarroch EE (2015) Pulvinar: associative role in cortical function and clinical correlations. Neurology 84:738–747

    Article  PubMed  Google Scholar 

  • Berger B, Trottier S, Verney C, Gaspar P, Alvarez C (1988) Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: a radioautographic study. J Comp Neurol 273:99–119

    Article  CAS  PubMed  Google Scholar 

  • Bissonette GB, Martins GJ, Franz TM, Harper ES, Schoenbaum G, Powell EM (2008) Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 28:11124–11130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bissonette GB, Powell EM, Roesch MR (2013) Neural structures underlying set-shifting: roles of medial prefrontal cortex and anterior cingulate cortex. Behav Brain Res 250:91–101

    Article  PubMed  PubMed Central  Google Scholar 

  • Brecht M, Krauss A, Muhammad S, Sinai-Esfahani L, Bellanca S, Margrie TW (2004) Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells. J Comp Neurol 479:360–373

    Article  PubMed  Google Scholar 

  • Burk JA, Sarter M (2001) Dissociation between the attentional functions mediated via basal forebrain cholinergic and GABAergic neurons. Neuroscience 105:899–909

    Article  CAS  PubMed  Google Scholar 

  • Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222

    Article  CAS  PubMed  Google Scholar 

  • Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, Rosen BR (2002) Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci USA 99:523–528

    Article  CAS  PubMed  Google Scholar 

  • Bussey TJ, Muir JL, Everitt BJ, Robbins TW (1997) Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behav Neurosci 111:920–936

    Article  CAS  PubMed  Google Scholar 

  • Carlson JM, Beacher F, Reinke KS, Habib R, Harmon-Jones E, Mujica-Parodi LR, Hajcak G (2012) Nonconscious attention bias to threat is correlated with anterior cingulate cortex gray matter volume: a voxel-based morphometry result and replication. Neuroimage 59:1713–1718

    Article  PubMed  Google Scholar 

  • Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641

    Article  CAS  PubMed  Google Scholar 

  • Cassel JC, Pereira de Vasconcelos A, Loureiro M, Cholvin T, Dalrymple-Alford JC, Vertes RP (2013) The reuniens and rhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog Neurobiol 111:34–52

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaillan FA, Marchetti E, Delfosse F, Roman FS, Soumireu-Mourat B (1997) Opposite effects depending on learning and memory demands in dorsomedial prefrontal cortex lesioned rats performing an olfactory task. Behav Brain Res 82:203–212

    Article  CAS  PubMed  Google Scholar 

  • Chandler HC, King V, Corwin JV, Reep RL (1992) Thalamocortical connections of rat posterior parietal cortex. Neurosci Lett 143:237–242

    Article  CAS  PubMed  Google Scholar 

  • Chandler DJ, Lamperski CS, Waterhouse BD (2013) Identification and distribution of projections from monoaminergic and cholinergic nuclei to functionally differentiated subregions of prefrontal cortex. Brain Res 1522:38–58

    Article  CAS  PubMed  Google Scholar 

  • Cholvin T, Loureiro M, Cassel R, Cosquer B, Geiger K, De Sa Nogueira D, Raingard H, Robelin L, Kelche C, Pereira de Vasconcelos A, Cassel JC (2013) The ventral midline thalamus contributes to strategy shifting in a memory task requiring both prefrontal cortical and hippocampal functions. J Neurosci 33:8772–8783

    Article  CAS  PubMed  Google Scholar 

  • Cipolloni PB, Pandya DN (1999) Cortical connections of the frontoparietal opercular areas in the rhesus monkey. J Comp Neurol 403:431–458

    Article  CAS  PubMed  Google Scholar 

  • Clements JR, Madl JE, Johnson RL, Larson AA, Beitz AJ (1987) Localization of glutamate, glutaminase, aspartate and aspartate aminotransferase in the rat midbrain periaqueductal gray. Exp Brain Res 67:594–602

    Article  CAS  PubMed  Google Scholar 

  • Coghill RC, McHaffie JG, Yen YF (2003) Neural correlates of interindividual differences in the subjective experience of pain. Proc Natl Acad Sci USA 100:8538–8542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conde F, Audinat E, Maire-Lepoivre E, Crepel F (1990) Afferent connections of the medial frontal cortex of the rat. A study using retrograde transport of fluorescent dyes I. Thalamic afferents. Brain Res Bull 24:341–354

    Article  CAS  PubMed  Google Scholar 

  • Courtin J, Bienvenu TC, Einarsson EO, Herry C (2013) Medial prefrontal cortex neuronal circuits in fear behavior. Neuroscience 240:219–242

    Article  CAS  PubMed  Google Scholar 

  • Crick FC, Koch C (2005) What is the function of the claustrum? Philos Trans R Soc Lond B Biol Sci 360:1271–1279

    Article  PubMed  PubMed Central  Google Scholar 

  • Czajkowski R, Jayaprakash B, Wiltgen B, Rogerson T, Guzman-Karlsson MC, Barth AL, Trachtenberg JT, Silva AJ (2014) Encoding and storage of spatial information in the retrosplenial cortex. Proc Natl Acad Sci USA 111:8661–8666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771–784

    Article  CAS  PubMed  Google Scholar 

  • Delatour B, Gisquet-Verrier P (2001) Involvement of the dorsal anterior cingulate cortex in temporal behavioral sequencing: subregional analysis of the medial prefrontal cortex in rat. Behav Brain Res 126:105–114

    Article  CAS  PubMed  Google Scholar 

  • Delatour B, Witter MP (2002) Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur J Neurosci 15:1400–1407

    Article  CAS  PubMed  Google Scholar 

  • Delevich K, Tucciarone J, Huang ZJ, Li B (2015) The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J Neurosci 35:5743–5753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deniau JM, Menetrey A, Thierry AM (1994) Indirect nucleus accumbens input to the prefrontal cortex via the substantia nigra pars reticulata: a combined anatomical and electrophysiological study in the rat. Neuroscience 61:533–545

    Article  CAS  PubMed  Google Scholar 

  • Dilgen J, Tejeda HA, O’Donnell P (2013) Amygdala inputs drive feedforward inhibition in the medial prefrontal cortex. J Neurophysiol 110:221–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong WK, Ryu H, Wagman IH (1978) Nociceptive responses of neurons in medial thalamus and their relationship to spinothalamic pathways. J Neurophysiol 41:1592–1613

    CAS  PubMed  Google Scholar 

  • Dumont JR, Aggleton JP (2013) Dissociation of recognition and recency memory judgments after anterior thalamic nuclei lesions in rats. Behav Neurosci 127:415–431

    Article  PubMed  PubMed Central  Google Scholar 

  • Einarsson EO, Nader K (2012) Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory. Learn Mem 19:449–452

    Article  PubMed  Google Scholar 

  • Einarsson EO, Pors J, Nader K (2015) Systems reconsolidation reveals a selective role for the anterior cingulate cortex in generalized contextual fear memory expression. Neuropsychopharmacology 40:480–487

    Article  CAS  PubMed  Google Scholar 

  • Erlich JC, Bush DE, Ledoux JE (2012) The role of the lateral amygdala in the retrieval and maintenance of fear-memories formed by repeated probabilistic reinforcement. Front Behav Neurosci 6:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Everitt BJ, Robbins TW, Evenden JL, Marston HM, Jones GH, Sirkia TE (1987) The effects of excitotoxic lesions of the substantia innominata, ventral and dorsal globus pallidus on the acquisition and retention of a conditional visual discrimination: implications for cholinergic hypotheses of learning and memory. Neuroscience 22:441–469

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Pastor B, Meana JJ (2002) In vivo tonic modulation of the noradrenaline release in the rat cortex by locus coeruleus somatodendritic alpha(2)-adrenoceptors. Eur J Pharmacol 442:225–229

    Article  CAS  PubMed  Google Scholar 

  • Fortin GD, Desrosiers CC, Yamaguchi N, Trudeau LE (2006) Basal somatodendritic dopamine release requires snare proteins. J Neurochem 96:1740–1749

    Article  CAS  PubMed  Google Scholar 

  • Fosse VM, Fonnum F (1987) Biochemical evidence for glutamate and/or aspartate as neurotransmitters in fibers from the visual cortex to the lateral posterior thalamic nucleus (pulvinar) in rats. Brain Res 400:219–224

    Article  CAS  PubMed  Google Scholar 

  • Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304:881–883

    Article  CAS  PubMed  Google Scholar 

  • Frankle WG, Laruelle M, Haber SN (2006) Prefrontal cortical projections to the midbrain in primates: evidence for a sparse connection. Neuropsychopharmacology 31:1627–1636

    Article  CAS  PubMed  Google Scholar 

  • Fuchs PN, Peng YB, Boyette-Davis JA, Uhelski ML (2014) The anterior cingulate cortex and pain processing. Front Integr Neurosci 8:35

    Article  PubMed  PubMed Central  Google Scholar 

  • Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145–177

    Article  PubMed  Google Scholar 

  • Gabbott PL, Warner TA, Busby SJ (2006) Amygdala input monosynaptically innervates parvalbumin immunoreactive local circuit neurons in rat medial prefrontal cortex. Neuroscience 139:1039–1048

    Article  CAS  PubMed  Google Scholar 

  • Gabbott P, Warner TA, Brown J, Salway P, Gabbott T, Busby S (2012) Amygdala afferents monosynaptically innervate corticospinal neurons in rat medial prefrontal cortex. J Comp Neurol 520:2440–2458

    Article  PubMed  Google Scholar 

  • Goll Y, Atlan G, Citri A (2015) Attention: the claustrum. Trends Neurosci 38:486–495

    Article  CAS  PubMed  Google Scholar 

  • Gorelova N, Mulholland PJ, Chandler LJ, Seamans JK (2012) The glutamatergic component of the mesocortical pathway emanating from different subregions of the ventral midbrain. Cereb Cortex 22:327–336

    Article  PubMed  Google Scholar 

  • Gracia-Llanes FJ, Crespo C, Blasco-Ibanez JM, Nacher J, Varea E, Rovira-Esteban L, Martinez-Guijarro FJ (2010) GABAergic basal forebrain afferents innervate selectively GABAergic targets in the main olfactory bulb. Neuroscience 170:913–922

    Article  CAS  PubMed  Google Scholar 

  • Gustorff B, Dorner T, Likar R, Grisold W, Lawrence K, Schwarz F, Rieder A (2008) Prevalence of self-reported neuropathic pain and impact on quality of life: a prospective representative survey. Acta Anaesthesiol Scand 52:132–136

    Article  CAS  PubMed  Google Scholar 

  • Hallock HL, Wang A, Shaw CL, Griffin AL (2013) Transient inactivation of the thalamic nucleus reuniens and rhomboid nucleus produces deficits of a working-memory dependent tactile-visual conditional discrimination task. Behav Neurosci 127:860–866

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasanein P, Parviz M, Keshavarz M, Javanmardi K (2007) CB1 receptor activation in the basolateral amygdala produces antinociception in animal models of acute and tonic nociception. Clin Exp Pharmacol Physiol 34:439–449

    Article  CAS  PubMed  Google Scholar 

  • Haxby JV, Petit L, Ungerleider LG, Courtney SM (2000) Distinguishing the functional roles of multiple regions in distributed neural systems for visual working memory. Neuroimage 11:380–391

    Article  CAS  PubMed  Google Scholar 

  • Heidbreder CA, Groenewegen HJ (2003) The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci Biobehav Rev 27:555–579

    Article  PubMed  Google Scholar 

  • Hnasko TS, Hjelmstad GO, Fields HL, Edwards RH (2012) Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J Neurosci 32:15076–15085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149–179

    Article  PubMed  Google Scholar 

  • Hoover WB, Vertes RP (2011) Projections of the medial orbital and ventral orbital cortex in the rat. J Comp Neurol 519:3766–3801

    Article  PubMed  Google Scholar 

  • Horikawa K, Kinjo N, Stanley LC, Powell EW (1988) Topographic organization and collateralization of the projections of the anterior and laterodorsal thalamic nuclei to cingulate areas 24 and 29 in the rat. Neurosci Res 6:31–44

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Nagano M, Suzuki H, Murakoshi T (2010) Chronic stress enhances synaptic plasticity due to disinhibition in the anterior cingulate cortex and induces hyper-locomotion in mice. Neuropharmacology 58:746–757

    Article  CAS  PubMed  Google Scholar 

  • Jankowski MM, Ronnqvist KC, Tsanov M, Vann SD, Wright NF, Erichsen JT, Aggleton JP, O’Mara SM (2013) The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front Syst Neurosci 7:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Ji G, Sun H, Fu Y, Li Z, Pais-Vieira M, Galhardo V, Neugebauer V (2010) Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation. J Neurosci 30:5451–5464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansen JP, Fields HL, Manning BH (2001) The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci USA 98:8077–8082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson DA, Pilar G (1980) The release of acetylcholine from post-ganglionic cell bodies in response to depolarization. J Physiol 299:605–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones BF, Groenewegen HJ, Witter MP (2005) Intrinsic connections of the cingulate cortex in the rat suggest the existence of multiple functionally segregated networks. Neuroscience 133:193–207

    Article  CAS  PubMed  Google Scholar 

  • Jurgens U (1983) Afferent fibers to the cingular vocalization region in the squirrel monkey. Exp Neurol 80:395–409

    Article  CAS  PubMed  Google Scholar 

  • Kesner RP, Churchwell JC (2011) An analysis of rat prefrontal cortex in mediating executive function. Neurobiol Learn Mem 96:417–431

    Article  PubMed  Google Scholar 

  • Kobbert C, Apps R, Bechmann I, Lanciego JL, Mey J, Thanos S (2000) Current concepts in neuroanatomical tracing. Prog Neurobiol 62:327–351

    Article  CAS  PubMed  Google Scholar 

  • Koga K, Descalzi G, Chen T, Ko HG, Lu J, Li S, Son J, Kim T, Kwak C, Huganir RL, Zhao MG, Kaang BK, Collingridge GL, Zhuo M (2015) Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain. Neuron 85:377–389

    Article  CAS  PubMed  Google Scholar 

  • Koike H, Demars MP, Short JA, Nabel EM, Akbarian S, Baxter MG, Morishita H (2016) Chemogenetic inactivation of dorsal anterior cingulate cortex neurons disrupts attentional behavior in mouse. Neuropsychopharmacology 41:1014–1023

    Article  CAS  PubMed  Google Scholar 

  • Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157–191

    Article  CAS  PubMed  Google Scholar 

  • Lewis DA (1992) The catecholaminergic innervation of primate prefrontal cortex. J Neural Transm Suppl 36:179–200

    CAS  PubMed  Google Scholar 

  • Li ZK, Takada M, Hattori T (1986) Topographic organization and collateralization of claustrocortical projections in the rat. Brain Res Bull 17:529–532

    Article  CAS  PubMed  Google Scholar 

  • Lindner K, Neubert J, Pfannmoller J, Lotze M, Hamm AO, Wendt J (2015) Fear-potentiated startle processing in humans: parallel fMRI and orbicularis EMG assessment during cue conditioning and extinction. Int J Psychophysiol 98:535–545

    Article  PubMed  Google Scholar 

  • Lopez J, Herbeaux K, Cosquer B, Engeln M, Muller C, Lazarus C, Kelche C, Bontempi B, Cassel JC, de Vasconcelos AP (2012) Context-dependent modulation of hippocampal and cortical recruitment during remote spatial memory retrieval. Hippocampus 22:827–841

    Article  PubMed  Google Scholar 

  • Loureiro M, Cholvin T, Lopez J, Merienne N, Latreche A, Cosquer B, Geiger K, Kelche C, Cassel JC, Pereira de Vasconcelos A (2012) The ventral midline thalamus (reuniens and rhomboid nuclei) contributes to the persistence of spatial memory in rats. J Neurosci 32:9947–9959

    Article  CAS  PubMed  Google Scholar 

  • Marchand A, Faugere A, Coutureau E, Wolff M (2014) A role for anterior thalamic nuclei in contextual fear memory. Brain Struct Funct 219:1575–1586

    Article  CAS  PubMed  Google Scholar 

  • Mathur BN, Caprioli RM, Deutch AY (2009) Proteomic analysis illuminates a novel structural definition of the claustrum and insula. Cereb Cortex 19:2372–2379

    Article  PubMed  PubMed Central  Google Scholar 

  • Matyas F, Lee J, Shin HS, Acsady L (2014) The fear circuit of the mouse forebrain: connections between the mediodorsal thalamus, frontal cortices and basolateral amygdala. Eur J Neurosci 39:1810–1823

    Article  PubMed  Google Scholar 

  • McDonald AJ (1987) Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: a fluorescence retrograde transport study in the rat. J Comp Neurol 262:46–58

    Article  CAS  PubMed  Google Scholar 

  • McGaughy J, Kaiser T, Sarter M (1996) Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci 110:247–265

    Article  CAS  PubMed  Google Scholar 

  • McKenna JT, Yang C, Franciosi S, Winston S, Abarr KK, Rigby MS, Yanagawa Y, McCarley RW, Brown RE (2013) Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. J Comp Neurol 521:1225–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Metz AE, Yau HJ, Centeno MV, Apkarian AV, Martina M (2009) Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. Proc Natl Acad Sci USA 106:2423–2428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller AM, Vedder LC, Law LM, Smith DM (2014) Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition. Front Hum Neurosci 8:586

    PubMed  PubMed Central  Google Scholar 

  • Mitchell AS (2015) The mediodorsal thalamus as a higher order thalamic relay nucleus important for learning and decision-making. Neurosci Biobehav Rev 54:76–88

    Article  PubMed  Google Scholar 

  • Monconduit L, Villanueva L (2005) The lateral ventromedial thalamic nucleus spreads nociceptive signals from the whole body surface to layer I of the frontal cortex. Eur J Neurosci 21:3395–3402

    Article  PubMed  Google Scholar 

  • Monconduit L, Bourgeais L, Bernard JF, Villanueva L (2003) Convergence of cutaneous, muscular and visceral noxious inputs onto ventromedial thalamic neurons in the rat. Pain 103:83–91

    Article  PubMed  Google Scholar 

  • Morecraft RJ, Stilwell-Morecraft KS, Cipolloni PB, Ge J, McNeal DW, Pandya DN (2012) Cytoarchitecture and cortical connections of the anterior cingulate and adjacent somatomotor fields in the rhesus monkey. Brain Res Bull 87:457–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura H, Hioki H, Furuta T, Kaneko T (2015) Different cortical projections from three subdivisions of the rat lateral posterior thalamic nucleus: a single-neuron tracing study with viral vectors. Eur J Neurosci 41:1294–1310

    Article  PubMed  Google Scholar 

  • Nanopoulos D, Belin MF, Maitre M, Vincendon G, Pujol JF (1982) Immunocytochemical evidence for the existence of GABAergic neurons in the nucleus raphe dorsalis. Possible existence of neurons containing serotonin and GABA. Brain Res 232:375–389

    Article  CAS  PubMed  Google Scholar 

  • Newman LA, Creer DJ, McGaughy JA (2015) Cognitive control and the anterior cingulate cortex: how conflicting stimuli affect attentional control in the rat. J Physiol Paris 109:95–103

    Article  PubMed  Google Scholar 

  • Ochi J, Shimizu K (1978) Occurrence of dopamine-containing neurons in the midbrain raphe nuclei of the rat. Neurosci Lett 8:317–320

    Article  CAS  PubMed  Google Scholar 

  • Oertel WH, Tappaz ML, Berod A, Mugnaini E (1982) Two-color immunohistochemistry for dopamine and GABA neurons in rat substantia nigra and zona incerta. Brain Res Bull 9:463–474

    Article  CAS  PubMed  Google Scholar 

  • Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508:207–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219

    Article  CAS  PubMed  Google Scholar 

  • Orsini CA, Trotta RT, Bizon JL, Setlow B (2015) Dissociable roles for the basolateral amygdala and orbitofrontal cortex in decision-making under risk of punishment. J Neurosci 35:1368–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan WX, McNaughton N (2004) The supramammillary area: its organization, functions and relationship to the hippocampus. Prog Neurobiol 74:127–166

    Article  PubMed  Google Scholar 

  • Passetti F, Chudasama Y, Robbins TW (2002) The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. Cereb Cortex 12:1254–1268

    Article  PubMed  Google Scholar 

  • Pastoriza LN, Morrow TJ, Casey KL (1996) Medial frontal cortex lesions selectively attenuate the hot plate response: possible nocifensive apraxia in the rat. Pain 64:11–17

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Paxinos G, Watson C (2014) Paxinos and Watson’s the rat brain in stereotaxic coordinates, 7th edn. Academic Press, Waltham

    Google Scholar 

  • Peschanski M, Guilbaud G, Gautron M (1981) Posterior intralaminar region in rat: neuronal responses to noxious and nonnoxious cutaneous stimuli. Exp Neurol 72:226–238

    Article  CAS  PubMed  Google Scholar 

  • Qu C, King T, Okun A, Lai J, Fields HL, Porreca F (2011) Lesion of the rostral anterior cingulate cortex eliminates the aversiveness of spontaneous neuropathic pain following partial or complete axotomy. Pain 152:1641–1648

    Article  PubMed  PubMed Central  Google Scholar 

  • Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH (2004) Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125:1–6

    Article  CAS  PubMed  Google Scholar 

  • Rana SA, Parker LA (2008) Differential effects of neurotoxin-induced lesions of the basolateral amygdala and central nucleus of the amygdala on lithium-induced conditioned disgust reactions and conditioned taste avoidance. Behav Brain Res 189:284–297

    Article  CAS  PubMed  Google Scholar 

  • Reep RL, Chandler HC, King V, Corwin JV (1994) Rat posterior parietal cortex: topography of corticocortical and thalamic connections. Exp Brain Res 100:67–84

    Article  CAS  PubMed  Google Scholar 

  • 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 221:2937–2962

    Article  PubMed  Google Scholar 

  • Restivo L, Vetere G, Bontempi B, Ammassari-Teule M (2009) The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J Neurosci 29:8206–8214

    Article  CAS  PubMed  Google Scholar 

  • Roland JJ, Savage LM (2009) The role of cholinergic and GABAergic medial septal/diagonal band cell populations in the emergence of diencephalic amnesia. Neuroscience 160:32–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Root DH, Mejias-Aponte CA, Qi J, Morales M (2014) Role of glutamatergic projections from ventral tegmental area to lateral habenula in aversive conditioning. J Neurosci 34:13906–13910

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanchez-Catalan MJ, Kaufling J, Georges F, Veinante P, Barrot M (2014) The antero-posterior heterogeneity of the ventral tegmental area. Neuroscience 282C:198–216

    Article  CAS  Google Scholar 

  • Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35:146–160

    Article  CAS  PubMed  Google Scholar 

  • Schoenbaum G, Esber GR (2010) How do you (estimate you will) like them apples? Integration as a defining trait of orbitofrontal function. Curr Opin Neurobiol 20:205–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12:154–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shenhav A, Botvinick MM, Cohen JD (2013) The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 79:217–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shenhav A, Straccia MA, Cohen JD, Botvinick MM (2014) Anterior cingulate engagement in a foraging context reflects choice difficulty, not foraging value. Nat Neurosci 17:1249–1254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibata H (1993) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330:533–542

    Article  CAS  PubMed  Google Scholar 

  • Shyu BC, Vogt BA (2009) Short-term synaptic plasticity in the nociceptive thalamic-anterior cingulate pathway. Mol Pain 5:51

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith JB, Alloway KD (2014) Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Front Syst Neurosci 8:93

    PubMed  PubMed Central  Google Scholar 

  • Sutin EL, Jacobowitz DM (1991) Neurochemicals in the dorsal pontine tegmentum. Prog Brain Res 88:3–14

    Article  CAS  PubMed  Google Scholar 

  • Takada M, Hattori T (1986) Collateral projections from the substantia nigra to the cingulate cortex and striatum in the rat. Brain Res 380:331–335

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M (2005) Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 1:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Teixeira CM, Pomedli SR, Maei HR, Kee N, Frankland PW (2006) Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci 26:7555–7564

    Article  PubMed  Google Scholar 

  • Torrealba F, Valdes JL (2008) The parietal association cortex of the rat. Biol Res 41:369–377

    Article  PubMed  Google Scholar 

  • Totah NK, Jackson ME, Moghaddam B (2013) Preparatory attention relies on dynamic interactions between prelimbic cortex and anterior cingulate cortex. Cereb Cortex 23:729–738

    Article  PubMed  Google Scholar 

  • Tripp A, Oh H, Guilloux JP, Martinowich K, Lewis DA, Sibille E (2012) Brain-derived neurotrophic factor signaling and subgenual anterior cingulate cortex dysfunction in major depressive disorder. Am J Psychiatry 169:1194–1202

    Article  PubMed  PubMed Central  Google Scholar 

  • Trueta C, De-Miguel FF (2012) Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system. Front Physiol 3:319

    PubMed  PubMed Central  Google Scholar 

  • Trueta C, Mendez B, De-Miguel FF (2003) Somatic exocytosis of serotonin mediated by L-type calcium channels in cultured leech neurones. J Physiol 547:405–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trulson ME, Cannon MS, Raese JD (1985) Identification of dopamine-containing cell bodies in the dorsal and median raphe nuclei of the rat brain using tyrosine hydroxylase immunochemistry. Brain Res Bull 15:229–234

    Article  CAS  PubMed  Google Scholar 

  • Uhl GR, Goodman RR, Kuhar MJ, Childers SR, Snyder SH (1979a) Immunohistochemical mapping of enkephalin containing cell bodies, fibers and nerve terminals in the brain stem of the rat. Brain Res 166:75–94

    Article  CAS  PubMed  Google Scholar 

  • Uhl GR, Goodman RR, Snyder SH (1979b) Neurotensin-containing cell bodies, fibers and nerve terminals in the brain stem of the rat: immunohistochemical mapping. Brain Res 167:77–91

    Article  CAS  PubMed  Google Scholar 

  • Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39:107–140

    Article  PubMed  Google Scholar 

  • Van Eden CG, Uylings HB (1985) Cytoarchitectonic development of the prefrontal cortex in the rat. J Comp Neurol 241:253–267

    Article  PubMed  Google Scholar 

  • Veinante P, Yalcin I, Barrot M (2013) The amygdala between sensation and affect: a role in pain. J Mol Psychiatry 1:9

    Article  PubMed  PubMed Central  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, Hoover WB, Do Valle AC, Sherman A, Rodriguez JJ (2006) Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J Comp Neurol 499:768–796

    Article  PubMed  Google Scholar 

  • Vogt BA (1993) Structural organization of cingulate cortex: areas, neurons, and somatodendritic transmitter receptors. In: Vogt BA, Gabriel M (eds) Neurobiology of cingulate cortex and limbic thalamus. Birkhaüser Boston Inc, Boston, pp 19–70

    Chapter  Google Scholar 

  • Vogt BA (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6:533–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt BA (2015) Cingulate cortex and pain architecture. In: Paxinos G (ed) The rat nervous system, 4th edn. Elsevier Academic Press, San Diego, pp 575–599

    Chapter  Google Scholar 

  • Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:192–210

    Article  CAS  PubMed  Google Scholar 

  • Vogt BA, Pandya DN (1987) Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 262:271–289

    Article  CAS  PubMed  Google Scholar 

  • Vogt BA, Paxinos G (2014) Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct Funct 219:185–192

    Article  PubMed  Google Scholar 

  • Vogt BA, Sikes RW (2009) Cingulate nociceptive circuitry and roles in pain processing: the cingulate premotor pain model. In: Vogt BA (ed) Cingulate neurobiology and disease. Oxford University Press, New York, pp 312–339

    Google Scholar 

  • Vogt BA, Pandya DN, Rosene DL (1987) Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents. J Comp Neurol 262:256–270

    Article  CAS  PubMed  Google Scholar 

  • Vogt BA, Derbyshire S, Jones AK (1996) Pain processing in four regions of human cingulate cortex localized with co-registered PET and MR imaging. Eur J Neurosci 8:1461–1473

    Article  CAS  PubMed  Google Scholar 

  • Weible AP (2013) Remembering to attend: the anterior cingulate cortex and remote memory. Behav Brain Res 245:63–75

    Article  PubMed  Google Scholar 

  • Whalen PJ, Bush G, McNally RJ, Wilhelm S, McInerney SC, Jenike MA, Rauch SL (1998) The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biol Psychiatry 44:1219–1228

    Article  CAS  PubMed  Google Scholar 

  • White MG, Cody PA, Bubser M, Wang HD, Deutch AY, Mathur BN (2016) Cortical hierarchy governs rat claustrocortical circuit organization. J Comp Neurol. doi:10.1002/cne.23970

    PubMed  Google Scholar 

  • Wolff M, Faugere A, Desfosses E, Coutureau E, Marchand AR (2015) Mediodorsal but not anterior thalamic nuclei lesions impair acquisition of a conditional discrimination task. Neurobiol Learn Mem 125:80–84

    Article  PubMed  Google Scholar 

  • Wright NF, Vann SD, Aggleton JP, Nelson AJ (2015) A critical role for the anterior thalamus in directing attention to task-relevant stimuli. J Neurosci 35:5480–5488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu W, Sudhof TC (2013) A neural circuit for memory specificity and generalization. Science 339:1290–1295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yalcin I, Barrot M (2014) The anxiodepressive comorbidity in chronic pain. Curr Opin Anaesthesiol 27:520–527

    Article  CAS  PubMed  Google Scholar 

  • Yalcin I, Bohren Y, Waltisperger E, Sage-Ciocca D, Yin JC, Freund-Mercier MJ, Barrot M (2011) A time-dependent history of mood disorders in a murine model of neuropathic pain. Biol Psychiatry 70:946–953

    Article  PubMed  Google Scholar 

  • Yamaguchi T, Wang HL, Li X, Ng TH, Morales M (2011) Mesocorticolimbic glutamatergic pathway. J Neurosci 31:8476–8490

    Article  CAS  PubMed  Google Scholar 

  • Yang JW, Shih HC, Shyu BC (2006) Intracortical circuits in rat anterior cingulate cortex are activated by nociceptive inputs mediated by medial thalamus. J Neurophysiol 96:3409–3422

    Article  PubMed  Google Scholar 

  • Yetnikoff L, Lavezzi HN, Reichard RA, Zahm DS (2014) An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience 282:23–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu T, Guo M, Garza J, Rendon S, Sun XL, Zhang W, Lu XY (2011) Cognitive and neural correlates of depression-like behaviour in socially defeated mice: an animal model of depression with cognitive dysfunction. Int J Neuropsychopharmacol 14:303–317

    Article  PubMed  Google Scholar 

  • Yung WH, Hausser MA, Jack JJ (1991) Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J Physiol 436:643–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Q, Wang S, Lim G, Yang L, Mao J, Sung B, Chang Y, Lim JA, Guo G (2008) Exacerbated mechanical allodynia in rats with depression-like behavior. Brain Res 1200:27–38

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Xu M, Kamigaki T, Hoang Do JP, Chang WC, Jenvay S, Miyamichi K, Luo L, Dan Y (2014) Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345:660–665

    Article  CAS  PubMed  Google Scholar 

  • Zhuo M (2014) Long-term potentiation in the anterior cingulate cortex and chronic pain. Philos Trans R Soc Lond B Biol Sci 369:20130146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong HW (2014) Neural networks of the mouse neocortex. Cell 156:1096–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

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 & Behavior Research Foundation. The authors thank Dr. R. A. Ceredig for reading the paper.

Author information

Authors and Affiliations

  1. Centre National de la Recherche Scientifique, Institut des Neurosciences Cellulaires et Intégratives, 5 rue Blaise Pascal, 67084, Strasbourg, France

    Clémentine Fillinger, Ipek Yalcin, Michel Barrot & Pierre Veinante

  2. Université de Strasbourg, Strasbourg, France

    Clémentine Fillinger & Pierre Veinante

Authors
  1. Clémentine Fillinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ipek Yalcin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Barrot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Veinante
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre Veinante.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 10039 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fillinger, C., Yalcin, I., Barrot, M. et al. Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse. Brain Struct Funct 222, 1509–1532 (2017). https://doi.org/10.1007/s00429-016-1290-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1290-1

Keywords

Search

Navigation