Skip to main content
Log in

Arborization patterns of amygdalopetal axons from the rat ventral pallidum

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

Abstract

We previously analyzed the arborization patterns of rat ventral pallidal (VP) axons that coursed caudally to innervate the thalamus and brainstem (Tripathi et al. in Brain Struct Funct 218:1133–1157, 2013). Here, we have reconstructed 16 previously undetected axons from the same tracer deposits that follow a more lateral trajectory. Virtually all 16 axons emanating from the different VP compartments collateralized in the extended amygdala system (EAS) and amygdaloid complex. The most frequent targets of axons from the lateral and medial (VPm) VP compartments were the rostral sublenticular extended amygdala, the extended amygdala (EA), the central nucleus of the amygdala and the posterior part of the basolateral amygdaloid nucleus. In contrast, axons from the rostral extension of the VP preferentially innervated the anterior amygdaloid area, the magnocellular preoptic nucleus, and the anterior part of the basomedial amygdaloid nucleus. We additionally found and reconstructed a single corticopetal axon arising from the VPm. The new results show that both direct and indirect projections from the basolateral complex and EAS to the ventral striatopallidal system are reciprocated by VP projections, and suggest that the systems can be activated simultaneously. The results additionally suggest that the amygdaloid complex and cortex are innervated separately from the VP. Finally, the combination of new and previous data indicate that approximately 84 % of VP axons (88/105) participate in basal ganglia circuits, 15 % (16/105) target the amygdaloid complex, and less than 1 % innervate the cortex.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AA:

Anterior amygdaloid area

acp:

Anterior commissure posterior part

Acb:

Nucleus accumbens

AcbC:

Nucleus accumbens, core

AcbSh:

Nucleus accumbens, shell

AHi:

Amygdalohippocampal area

AHiAL:

Amygdalohippocampal area, anterolateral part

AHiPM:

Amygdalohippocampal area, posteromedial part

APir:

Amygdalopiriform transition area

B:

Basal nucleus of Meynert

BDA:

Biotinylated dextran amine

BL:

Basolateral amygdaloid nucleus

BLA:

Basolateral amygdaloid nucleus, anterior part

BLP:

Basolateral amygdaloid nucleus, posterior part

BLV:

Basolateral amygdaloid nucleus, ventral part

BM:

Basomedial amygdaloid nucleus

BMA:

Basomedial amygdaloid nucleus, anterior part

BMP:

Basomedial amygdaloid nucleus, posterior part

BST:

Bed nucleus of the stria terminalis

BSTL:

Bed nucleus of the stria terminalis, lateral division

BSTM:

Bed nucleus of the stria terminalis, medial division

C:

Caudal

CalB:

Calbindin D28k

Ce:

Central amygdaloid nucleus

CeC:

Central amygdala nucleus, capsular

CeL:

Central amygdala nucleus, lateral

CeM:

Central amygdala nucleus, medial

CPu:

Caudate putamen

cst:

Commissural stria terminalis

CxA:

Cortex–amygdala transition zone

D:

Dorsal

DP:

Dorsal peduncular cortex

DTT:

Dorsal tenia tecta

EA:

Extended amygdala

EAS:

Extended amygdala system

Enk:

Leu-enkephalin

EP:

Entopeduncular nucleus

f:

Fornix

FrA:

Frontal association cortex

GP:

Globus pallidus

I:

Intercalated nuclei of amygdala

ic:

Internal capsule

IL:

Infralimbic cortex

IPAC:

Interstitial nucleus of posterior limb of anterior commissure

L:

Lateral

LaDL:

Lateral amygdaloid nucleus, dorsolateral

LaVM:

Lateral amygdaloid nucleus, ventromedial

LHb:

Lateral habenula

LSS:

Lateral stripe of striatum

LV:

Lateral ventricle

MCPO:

Magnocellular preoptic nucleus

Me:

Medial amygdaloid nucleus

MeAD:

Medial amygdaloid nucleus, anterodorsal

MeAV:

Medial amygdaloid nucleus, anteroventral

MePD:

Medial amygdaloid nucleus, posterodorsal

MePV:

Medial amygdaloid nucleus, posteroventral

opt:

Optic tract

Pir:

Piriform cortex

PLCo:

Posterolateral cortical amygdaloid nucleus

PMCo:

Posteromedial cortical amygdaloid nucleus

PrL:

Prelimbic cortex

Sib :

Substantia innominata, basal part

SLEA:

Sublenticular extended amygdala

SLEAr:

Rostral sublenticular extended amygdala

STIA:

Bed nucleus of stria terminalis intraamygdaloid division

Tu:

Olfactory tubercle

VEn:

Ventral endopiriform nucleus

VP:

Ventral pallidum

VPl:

Ventral pallidum, dorsolateral compartment

VPm:

Ventral pallidum, ventromedial compartment

VPr:

Ventral pallidum, rostral portion

References

  • Abdi A, Mallet N, Mohamed FY, Sharott A, Dodson PD, Nakamura KC, Suri S, Avery SV, Larvin JT, Garas FN, Garas SN, Vinciati F, Morin S, Bezard E, Baufreton J, Magill PJ (2015) Prototypic and arkypallidal neurons in the dopamine-intact external globus pallidus. J Neurosci 35:6667–6688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1–39

    Article  CAS  PubMed  Google Scholar 

  • Anglada-Figueroa D, Quirk GJ (2005) Lesions of the basal amygdala block expression of conditioned fear but not extinction. J Neurosci 25:9680–9685

    Article  CAS  PubMed  Google Scholar 

  • Balleine BW, Killcross S (2006) Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 29:272–279

    Article  CAS  PubMed  Google Scholar 

  • Baufreton J, Kirkham E, Atherton JF, Menard A, Magill PJ, Bolam JP, Bevan MD (2009) Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus. J Neurophysiol 102:532–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berendse HW, Galis-de Graaf Y, Groenewegen HJ (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316:314–347

    Article  CAS  PubMed  Google Scholar 

  • Bernard JF, Alden M, Besson JM (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329:201–229

    Article  CAS  PubMed  Google Scholar 

  • Bienkowski MS, Rinaman L (2012) Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats. Brain Struct Funct 218:187–208

    Article  PubMed  PubMed Central  Google Scholar 

  • Bigl V, Woolf NJ, Butcher LL (1982) Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 8:727–749

    Article  CAS  PubMed  Google Scholar 

  • Bolam JP, Ingham CA, Izzo PN, Levey AI, Rye DB, Smith AD, Wainer BH (1986) Substance P-containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat. Brain Res 397:279–289

    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 

  • Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352

    Article  PubMed  Google Scholar 

  • Carlsen J, Zaborszky L, Heimer L (1985) Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 234:155–167

    Article  CAS  PubMed  Google Scholar 

  • Cebrián C, Parent A, Prensa L (2005) Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat. J Comp Neurol 492:349–369

    Article  PubMed  Google Scholar 

  • Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Muller C, Luthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277–282

    Article  CAS  PubMed  Google Scholar 

  • Commons KG, Beck SG, Bey VW (2005) Two populations of glutamatergic axons in the rat dorsal raphe nucleus defined by the vesicular glutamate transporters 1 and 2. Eur J Neurosci 21:1577–1586

    Article  PubMed  PubMed Central  Google Scholar 

  • Comoli E, Ribeiro-Barbosa ER, Negrao N, Goto M, Canteras NS (2005) Functional mapping of the prosencephalic systems involved in organizing predatory behavior in rats. Neuroscience 130:1055–1067

    Article  CAS  PubMed  Google Scholar 

  • de Olmos JS, Heimer L (1999) The concepts of the ventral striatopallidal system and extended amygdala. Ann N Y Acad Sci 877:1–32

    Article  PubMed  Google Scholar 

  • de Olmos JS, Beltramino CA, Alheid G (2004) Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier, Oxford, pp 509–603

    Chapter  Google Scholar 

  • Divac I (1975) Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res 93:385–398

    Article  CAS  PubMed  Google Scholar 

  • Duque A, Tepper JM, Detari L, Ascoli GA, Zaborszky L (2007) Morphological characterization of electrophysiologically and immunohistochemically identified basal forebrain cholinergic and neuropeptide Y-containing neurons. Brain Struct Funct 212:55–73

    Article  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (1992) Amygdala-ventral striatal interactions and reward-related processes. In: Aggleton JP (ed) The amygdala. Wiley, New York, pp 401–430

    Google Scholar 

  • Fox AS, Oler JA, Tromp do PM, Fudge JL, Kalin NH (2015) Extending the amygdala in theories of threat processing. Trends Neurosci 38:319–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furuta T, Kaneko T (2006) Third pathway in the cortico-basal ganglia loop: Neurokinin B-producing striatal neurons modulate cortical activity via striato-innominato-cortical projection. Neurosci Res 54:1–10

    Article  CAS  PubMed  Google Scholar 

  • Furuta T, Mori T, Lee T, Kaneko T (2000) Third group of neostriatofugal neurons: neurokinin B-producing neurons that send axons predominantly to the substantia innominata. J Comp Neurol 426:279–296

    Article  CAS  PubMed  Google Scholar 

  • Furuta T, Zhou L, Kaneko T (2002) Preprodynorphin-, preproenkephalin-, preprotachykinin A- and preprotachykinin B-immunoreactive neurons in the accumbens nucleus and olfactory tubercle: double-immunofluorescence analysis. Neuroscience 114:611–627

    Article  CAS  PubMed  Google Scholar 

  • Furuta T, Koyano K, Tomioka R, Yanagawa Y, Kaneko T (2004) GABAergic basal forebrain neurons that express receptor for neurokinin B and send axons to the cerebral cortex. J Comp Neurol 473:43–58

    Article  CAS  PubMed  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 

  • Gittis AH, Berke JD, Bevan MD, Chan CS, Mallet N, Morrow MM, Schmidt R (2014) New roles for the external globus pallidus in Basal Ganglia circuits and behavior. J Neurosci 34:15178–15183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gritti I, Mainville L, Mancia M, Jones BE (1997) GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 383:163–177

    Article  CAS  PubMed  Google Scholar 

  • Groenewegen HJ, Becker NE, Lohman AH (1980) Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid. Neuroscience 5:1903–1916

    Article  CAS  PubMed  Google Scholar 

  • Grove EA (1988a) Efferent connections of the substantia innominata in the rat. J Comp Neurol 277:347–364

    Article  CAS  PubMed  Google Scholar 

  • Grove EA (1988b) Neural associations of the substantia innominata in the rat: afferent connections. J Comp Neurol 277:315–346

    Article  CAS  PubMed  Google Scholar 

  • Grove EA, Domesick VB, Nauta WJ (1986) Light microscopic evidence of striatal input to intrapallidal neurons of cholinergic cell group Ch4 in the rat: a study employing the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 367:379–384

    Article  CAS  PubMed  Google Scholar 

  • Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4–26

    Article  PubMed  Google Scholar 

  • Haber S, McFarland NR (2001) The place of the thalamus in frontal cortical-basal ganglia circuits. Neuroscientist 7:315–324

    Article  CAS  PubMed  Google Scholar 

  • Haber SN, Nauta WJ (1983) Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry. Neuroscience 9:245–260

    Article  CAS  PubMed  Google Scholar 

  • Haber SN, Groenewegen HJ, Grove EA, Nauta WJ (1985) Efferent connections of the ventral pallidum: evidence of a dual striato pallidofugal pathway. J Comp Neurol 235:322–335

    Article  CAS  PubMed  Google Scholar 

  • Heimer L, Van Hoesen GW (2006) The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30:126–147

    Article  PubMed  Google Scholar 

  • Heimer L, Wilson RD (1975) The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: Santini M (ed) Golgi centennial symposium. Proceedings. Raven Press, New York, pp 177–193

    Google Scholar 

  • Heimer L, Zaborszky L, Zahm DS, Alheid GF (1987) The ventral striatopallidothalamic projection: I. The striatopallidal link originating in the striatal parts of the olfactory tubercle. J Comp Neurol 255:571–591

    Article  CAS  PubMed  Google Scholar 

  • Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89–125

    Article  CAS  PubMed  Google Scholar 

  • Heimer L, Harlan RE, Alheid GF, Garcia MM, de Olmos J (1997) Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders. Neuroscience 76:957–1006

    Article  CAS  PubMed  Google Scholar 

  • Henderson Z (1997) The projection from the striatum to the nucleus basalis in the rat: an electron microscopic study. Neuroscience 78:943–955

    Article  CAS  PubMed  Google Scholar 

  • Hikosaka O, Bromberg-Martin E, Hong S, Matsumoto M (2008) New insights on the subcortical representation of reward. Curr Opin Neurobiol 18:203–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobsohn L (1909) Über die Kerne des menschlichen hirnstamms. Verlag der Königl Akademie des Wisenschaftern, Berlin

    Google Scholar 

  • Kelley AE, Domesick VB, Nauta WJ (1982) The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7:615–630

    Article  CAS  PubMed  Google Scholar 

  • Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225–254

    Article  CAS  PubMed  Google Scholar 

  • Liu AK, Chang RC, Pearce RK, Gentleman SM (2015) Nucleus basalis of Meynert revisited: anatomy, history and differential involvement in Alzheimer’s and Parkinson’s disease. Acta Neuropathol 129:527–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, Nakamura KC, Magill PJ (2012) Dichotomous organization of the external globus pallidus. Neuron 74:1075–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Garcia F, Novejarque A, Lanuza E (2008) Two interconnected functional systems in the amygdala of amniote vertebrates. Brain Res Bull 75:206–213

    Article  PubMed  Google Scholar 

  • Mascagni F, McDonald AJ (2009) Parvalbumin-immunoreactive neurons and GABAergic neurons of the basal forebrain project to the rat basolateral amygdala. Neuroscience 160:805–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald AJ, Shammah-Lagnado SJ, Shi C, Davis M (1999) Cortical afferents to the extended amygdala. Ann N Y Acad Sci 877:309–338

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ, Muller JF, Mascagni F (2011) Postsynaptic targets of GABAergic basal forebrain projections to the basolateral amygdala. Neuroscience 183:144–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McFarland NR, Haber SN (2002) Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 22:8117–8132

    CAS  PubMed  Google Scholar 

  • McGinty VB, Hayden BY, Heilbronner SR, Dumont EC, Graves SM, Mirrione MM, du Hoffmann J, Sartor GC, Espana RA, Millan EZ, Difeliceantonio AG, Marchant NJ, Napier TC, Root DH, Borgland SL, Treadway MT, Floresco SB, McGinty JF, Haber S (2011) Emerging, reemerging, and forgotten brain areas of the reward circuit: notes from the 2010 motivational neural networks conference. Behav Brain Res 225:348–357

    Article  PubMed  PubMed Central  Google Scholar 

  • Mello LE, Tan AM, Finch DM (1992) GABAergic synaptic transmission in projections from the basal forebrain and hippocampal formation to the amygdala: an in vivo iontophoretic study. Brain Res 587:41–48

    Article  CAS  PubMed  Google Scholar 

  • Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1–Ch6). Neuroscience 10:1185–1201

    Article  CAS  PubMed  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 

  • Nobrega-Pereira S, Gelman D, Bartolini G, Pla R, Pierani A, Marin O (2010) Origin and molecular specification of globus pallidus neurons. J Neurosci 30:2824–2834

    Article  CAS  PubMed  Google Scholar 

  • Novejarque A, Gutierrez-Castellanos N, Lanuza E, Martinez-Garcia F (2011) Amygdaloid projections to the ventral striatum in mice: direct and indirect chemosensory inputs to the brain reward system. Front Neuroanat 5:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Ottersen OP (1980) Afferent connections to 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 (1982) Connections of the amygdala of the rat. IV: corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol 205:30–48

    Article  CAS  PubMed  Google Scholar 

  • Palomero-Gallagher N, Zilles K (2004) Isocortex. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier, Oxford, pp 729–747

    Chapter  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, CA

    Google Scholar 

  • Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press, San Diego

    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 

  • Rao ZR, Shiosaka S, Tohyama M (1987) Origin of cholinergic fibers in the basolateral nucleus of the amygdaloid complex by using sensitive double-labeling technique of retrograde biotinized tracer and immunocytochemistry. J Hirnforsch 28:553–560

    CAS  PubMed  Google Scholar 

  • Rasband, W.S. (1997-2012) ImageJ. US National Institutes of Health, Bethesda. http://imagej.nih.gov/ij/

  • Root DH, Melendez RI, Zaborszky L, Napier TC (2015) The ventral pallidum: subregion-specific functional anatomy and roles in motivated behaviors. Prog Neurobiol 130:29–70

    Article  PubMed  PubMed Central  Google Scholar 

  • Russchen FT (1982) Amygdalopetal projections in the cat. II. Subcortical afferent connections. A study with retrograde tracing techniques. J Comp Neurol 207:157–176

    Article  CAS  PubMed  Google Scholar 

  • Russchen FT, Price JL (1984) Amygdalostriatal projections in the rat. Topographical organization and fiber morphology shown using the lectin PHA-L as an anterograde tracer. Neurosci Lett 47:15–22

    Article  CAS  PubMed  Google Scholar 

  • Rye DB, Wainer BH, Mesulam MM, Mufson EJ, Saper CB (1984) Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13:627–643

    Article  CAS  PubMed  Google Scholar 

  • Saper CB (1984) Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J Comp Neurol 222:313–342

    Article  CAS  PubMed  Google Scholar 

  • Sarter M, Bruno JP (2002) The neglected constituent of the basal forebrain corticopetal projection system: GABAergic projections. Eur J Neurosci 15:1867–1873

    Article  PubMed  Google Scholar 

  • Sarter M, Bruno JP, Givens B (2003) Attentional functions of cortical cholinergic inputs: What does it mean for learning and memory? Neurobiol Learn Mem 80:245–256

    Article  CAS  PubMed  Google Scholar 

  • Saunders A, Granger AJ, Sabatini BL (2015a) Corelease of acetylcholine and GABA from cholinergic forebrain neurons. Elife 4. doi:10.7554/eLife.06412

  • Saunders A, Oldenburg IA, Berezovskii VK, Johnson CA, Kingery ND, Elliott HL, Xie T, Gerfen CR, Sabatini BL (2015b) A direct GABAergic output from the basal ganglia to frontal cortex. Nature 521:85–89

    Article  CAS  PubMed  PubMed Central  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 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    Article  CAS  PubMed  Google Scholar 

  • Sesack SR, Grace AA (2010) Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27–47

    Article  PubMed  Google Scholar 

  • Shammah-Lagnado SJ, Alheid GF, Heimer L (1999) Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat. Neuroscience 94:1097–1123

    Article  CAS  PubMed  Google Scholar 

  • Shammah-Lagnado SJ, Alheid GF, Heimer L (2001) Striatal and central extended amygdala parts of the interstitial nucleus of the posterior limb of the anterior commissure: evidence from tract-tracing techniques in the rat. J Comp Neurol 439:104–126

    Article  CAS  PubMed  Google Scholar 

  • Shipley MT, Ennis M, Puche AC (2004) Olfactory System. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier, Oxford, pp 923–964

    Chapter  Google Scholar 

  • Stefanik MT, Kupchik YM, Brown RM, Kalivas PW (2013) Optogenetic evidence that pallidal projections, not nigral projections, from the nucleus accumbens core are necessary for reinstating cocaine seeking. J Neurosci 33:13654–13662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, Kempadoo KA, Zhang F, Deisseroth K, Bonci A (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:377–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathi A, Mengual E (2012) Axonal collateralization patterns of the rostral sublenticular extended amygdala in the rat. FENS Forum 2012, Barcelona

  • Tripathi A, Prensa L, Cebrian C, Mengual E (2010) Axonal branching patterns of nucleus accumbens neurons in the rat. J Comp Neurol 518:4649–4673

    Article  PubMed  Google Scholar 

  • Tripathi A, Prensa L, Mengual E (2013) Axonal branching patterns of ventral pallidal neurons in the rat. Brain Struct Funct 218:1133–1157

    Article  PubMed  Google Scholar 

  • Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58

    Article  CAS  PubMed  Google Scholar 

  • Wilensky AE, Schafe GE, Kristensen MP, LeDoux JE (2006) Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 26:12387–12396

    Article  CAS  PubMed  Google Scholar 

  • Woolf NJ, Butcher LL (1982) Cholinergic projections to the basolateral amygdala: a combined Evans blue and acetylcholinesterase analysis. Brain Res Bull 8:751–763

    Article  CAS  PubMed  Google Scholar 

  • Woolf NJ, Eckenstein F, Butcher LL (1983) Cholinergic projections from the basal forebrain to the frontal cortex: a combined fluorescent tracer and immunohistochemical analysis in the rat. Neurosci Lett 40:93–98

    Article  CAS  PubMed  Google Scholar 

  • Woolf NJ, Eckenstein F, Butcher LL (1984) Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon. Brain Res Bull 13:751–784

    Article  CAS  PubMed  Google Scholar 

  • Yasui Y, Breder CD, Saper CB, Cechetto DF (1991) Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol 303:355–374

    Article  CAS  PubMed  Google Scholar 

  • Zaborszky L, Cullinan WE (1992) Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat. Brain Res 570:92–101

    Article  CAS  PubMed  Google Scholar 

  • Zaborszky L, Heimer L, Eckenstein F, Leranth C (1986) GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabeling. J Comp Neurol 250:282–295

    Article  CAS  PubMed  Google Scholar 

  • Zaborszky L, Hoemke L, Mohlberg H, Schleicher A, Amunts K, Zilles K (2008) Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain. Neuroimage 42:1127–1141

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaborszky L, Csordas A, Mosca K, Kim J, Gielow MR, Vadasz C, Nadasdy Z (2015) Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb Cortex 25:118–137

    Article  PubMed  Google Scholar 

  • Zahm DS (1989) The ventral striatopallidal parts of the basal ganglia in the rat–II. Compartmentation of ventral pallidal efferents. Neuroscience 30:33–50

    Article  CAS  PubMed  Google Scholar 

  • Zahm DS (2006) The evolving theory of basal forebrain functional-anatomical ‘macrosystems’. Neurosci Biobehav Rev 30:148–172

    Article  PubMed  Google Scholar 

  • Zahm DS, Heimer L (1990) Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol 302:437–446

    Article  CAS  PubMed  Google Scholar 

  • Zahm DS, Heimer L (1993) Specificity in the efferent projections of the nucleus-accumbens in the rat—comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220–232

    Article  CAS  PubMed  Google Scholar 

  • Zahm DS, Williams E, Wohltmann C (1996) Ventral striatopallidothalamic projection: IV. Relative involvements of neurochemically distinct subterritories in the ventral pallidum and adjacent parts of the rostroventral forebrain. J Comp Neurol 364:340–362

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Furuta T, Kaneko T (2004) Neurokinin B-producing projection neurons in the lateral stripe of the striatum and cell clusters of the accumbens nucleus in the rat. J Comp Neurol 480:143–161

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We want to thank John F. Wesseling for critical readings of the manuscript. S. Mongia is recipient of a predoctoral Grant from Asociación de Amigos de la Universidad de Navarra, while A. Tripathi was recipient of a predoctoral Grant from FIMA (Foundation for Applied Medical Research). This work was supported by the Spanish Ministry of Education and Science (MEC, BFU2004-06825), Gobierno de Navarra 2004, and the ‘UTE project CIMA’.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Mengual.

Additional information

S. Mongia and A. Tripathi have contributed equally to this paper.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mongia, S., Tripathi, A. & Mengual, E. Arborization patterns of amygdalopetal axons from the rat ventral pallidum. Brain Struct Funct 221, 4549–4573 (2016). https://doi.org/10.1007/s00429-016-1184-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1184-2

Keywords

Navigation