Skip to main content

Advertisement

SpringerLink
Log in

Axonal branching patterns of ventral pallidal neurons in the rat

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

Abstract

The ventral pallidum (VP) is a key component of the cortico-basal ganglia circuits that process motivational and emotional information, and also a crucial site for reward. Although the main targets of the two VP compartments, medial (VPm) and lateral (VPl) have already been established, the collateralization patterns of individual axons have not previously been investigated. Here we have fully traced eighty-four axons from VPm, VPl and the rostral extension of VP into the olfactory tubercle (VPr), using the anterograde tracer biotinylated dextran amine in the rat. Thirty to fifty percent of axons originating from VPm and VPr collateralized in the mediodorsal thalamic nucleus and lateral habenula, indicating a close association between the ventral basal ganglia-thalamo-cortical loop and the reward network at the single axon level. Additional collateralization of these axons in diverse components of the extended amygdala and corticopetal system supports a multisystem integration that may take place at the basal forebrain. Remarkably, we did not find evidence for a sharp segregation in the targets of axons arising from the two VP compartments, as VPl axons frequently collateralized in the caudal lateral hypothalamus and ventral tegmental area, the well-known targets of VPm, while VPm axons, in turn, also collateralized in typical VPl targets such as the subthalamic nucleus, substantia nigra pars compacta and reticulata, and retrorubral field. Nevertheless, VPl and VPm displayed collateralization patterns that paralleled those of dorsal pallidal components, confirming at the single axon level the parallel organization of functionally different basal ganglia loops.

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
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

AA:

Anterior amygdaloid area

ac:

Anterior commissure

aca:

Anterior commissure anterior part

acp:

Anterior commissure posterior part

Acb:

Nucleus accumbens

AcbC:

Nucleus accumbens, core

AcbSh:

Nucleus accumbens, shell

AD:

Anterodorsal thalamic nucleus

AM:

Anteromedial thalamic nucleus

AON:

Anterior olfactory nucleus

Atg:

Anterior tegmental nucleus

B:

Basal nucleus of Meynert

BDA:

Biotinylated dextran amine

BSTL:

Bed nucleus of the stria terminalis, lateral division

BSTM:

Bed nucleus of the stria terminalis, medial division

C:

Caudal

CalB:

Calbindin D28k

CG:

Central gray

Cl:

Claustrum

CLi:

Caudal linear nucleus of raphe

CPu:

Caudate putamen

D:

Dorsal

DMTg:

Dorsomedial tegmental area

DR:

Dorsal raphe

DpMe:

Deep mesencephalic nucleus

EA:

Extended amygdala

Enk:

Leucine-Enkephalin

EP:

Entopeduncular nucleus

f:

Fornix

fr:

Fasciculus retroflexus

GP:

Globus pallidus

GPe:

External globus pallidus

GPi:

Internal globus pallidus

HDB:

Horizontal limb of the diagonal band of Broca

ic:

Internal capsule

ICj:

Islets of Calleja

IP:

Interpeduncular nucleus

IPAC:

Interstitial nucleus of posterior limb of anterior commissure

L:

Lateral

LacbSh:

Lateral acumbens shell

LDDM:

Laterodorsal thalamic nucleus, dorsomedial part

LDTg:

Laterodorsal tegmental nucleus

LH:

Lateral hypothalamic area

LHb:

Lateral habenula

LM:

Lateral mammillary nucleus

LOT:

Nucleus of the lateral olfactory tract

LPO:

Lateral preoptic area

LSI:

Lateral septal nucleus intermediate part

LSS:

Lateral stripe of striatum

LSV:

Lateral septal nucleus, ventral part

LV:

Lateral ventricle

MCPO:

Magnocellular preoptic area

MD:

Mediodorsal thalamic nucleus

MeA:

Medial amygdaloid area

MHb:

Medial habenula

mp:

Mammillary peduncle

MPA:

Medial preoptic area

MT:

Medial terminal nucleus of the accessory optic tract

MTu:

Medial tuberal nucleus

opt:

Optic tract

PaR:

Pararubral area

PF:

Parafascicular thalamic nucleus

PMnR:

Paramedian raphe nucleus

PnO:

Pontine reticular nucleus, oral part

PnC:

Pontine reticular nucleus, caudal part

PPTg:

Pedunculopontine tegmental nucleus

PS:

Parastrial nucleus

PVA:

Paraventricular thalamic nucleus, anterior part

R:

Red nucleus

Rbd:

Rhabdoid nucleus

Re:

Reuniens thalamic nucleus

Rh:

Rhomboid thalamic nucleus

RPF:

Retroparafascicular nucleus

RRF:

Retrorubral field

Rt:

Reticular thalamic nucleus

RtTg:

Reticulotegmental nucleus of the pons

Sib :

Substantia innominata, basal part

SHy:

Septohypothalamic nucleus

SLEAr:

Rostral sublenticular extended amygdala

sm:

Stria medullaris

SMT:

Submammillothalamic nucleus

SN:

Substantia nigra

SNc:

Substantia nigra pars compacta

SNl:

Substantia nigra pars lateralis

SNr:

Substantia nigra pars reticulata

STh:

Subthalamic nucleus

StHy:

Striohypothalamic nucleus

Sub:

Submedius thalamic nucleus

SubCV:

Subcoeruleus nucleus, ventral part

SubI:

Subincertal nucleus

SuM:

Supramammillary nucleus

Tu:

Olfactory tubercle

VA:

Ventral anterior thalamic nucleus

VLPAG:

Ventrolateral periaqueductal gray

VLTg:

Ventrolateral tegmental nucleus

VM:

Ventromedial thalamic nucleus

VP:

Ventral pallidum

VPl:

Ventral pallidum, dorsolateral compartment

VPm:

Ventral pallidum, ventromedial compartment

VPr:

Ventral pallidum, rostral portion

VTA:

Ventral tegmental area

VTg:

Ventral tegmental nucleus

ZI:

Zona incerta

References

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    Article  PubMed  CAS  Google Scholar 

  • Bartho P, Freund TF, Acsady L (2002) Selective GABAergic innervation of thalamic nuclei from zona incerta. Eur J Neurosci 16:999–1014

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Bevan MD, Clarke NP, Bolam JP (1997) Synaptic integration of functionally diverse pallidal information in the entopeduncular nucleus and subthalamic nucleus in the rat. J Neurosci 17:308–324

    PubMed  CAS  Google Scholar 

  • Bevan MD, Booth PA, Eaton SA, Bolam JP (1998) Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci 18:9438–9452

    PubMed  CAS  Google Scholar 

  • Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993) The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338:255–278

    Article  PubMed  CAS  Google Scholar 

  • Cebrian C, Prensa L (2010) Basal ganglia and thalamic input from neurons located within the ventral tier cell cluster region of the substantia nigra pars compacta in the rat. J Comp Neurol 518:1283–1300

    PubMed  CAS  Google Scholar 

  • Cebrian 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 

  • Churchill L, Kalivas PW (1994) A topographically organized gamma-aminobutyric acid projection from the ventral pallidum to the nucleus accumbens in the rat. J Comp Neurol 345:579–595

    Article  PubMed  CAS  Google Scholar 

  • Cornwall J, Cooper JD, Phillipson OT (1990) Projections to the rostral reticular thalamic nucleus in the rat. Exp Brain Res 80:157–171

    Article  PubMed  CAS  Google Scholar 

  • Fujiyama F, Sohn J, Nakano T, Furuta T, Nakamura KC, Matsuda W, Kaneko T (2011) Exclusive and common targets of neostriatofugal projections of rat striosome neurons: a single neuron-tracing study using a viral vector. Eur J Neurosci 33:668–677

    Article  PubMed  Google Scholar 

  • Geisler S, Trimble M (2008) The lateral habenula: no longer neglected. CNS Spectr 13:484–489

    PubMed  Google Scholar 

  • Geisler S, Zahm DS (2005) Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490:270–294

    Article  PubMed  Google Scholar 

  • Groenewegen HJ (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24:379–431

    Article  PubMed  CAS  Google Scholar 

  • Groenewegen HJ, Berendse HW (1990) Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol 294:607–622

    Article  PubMed  CAS  Google Scholar 

  • Groenewegen HJ, Berendse HW, Haber SN (1993) Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience 57:113–142

    Article  PubMed  CAS  Google Scholar 

  • Haber SN (2010) Integrative networks across basal ganglia circuits. In: Steiner J, Tseng KY (eds) Handbook of basal ganglia structure and function. Elsevier, Amsterdam, pp 409–427

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

    Article  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  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE, Zahm DS (1997) The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci 9:354–381

    PubMed  CAS  Google Scholar 

  • Heise CE, Mitrofanis J (2004) Evidence for a glutamatergic projection from the zona incerta to the basal ganglia of rats. J Comp Neurol 468:482–495

    Article  PubMed  CAS  Google Scholar 

  • Herkenham M, Nauta WJ (1977) Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173:123–146

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka O, Sesack SR, Lecourtier L, Shepard PD (2008) Habenula: crossroad between the basal ganglia and the limbic system. J Neurosci 28:11825–11829

    Article  PubMed  CAS  Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) Use of avidin–biotin–peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580

    Article  PubMed  CAS  Google Scholar 

  • Kita H, Kitai ST (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260:435–452

    Article  PubMed  CAS  Google Scholar 

  • Kita H, Kitai ST (1994) The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res 636:308–319

    Article  PubMed  CAS  Google Scholar 

  • Klitenick MA, Deutch AY, Churchill L, Kalivas PW (1992) Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum. Neuroscience 50:371–386

    Article  PubMed  CAS  Google Scholar 

  • Kolmac C, Mitrofanis J (1999) Distribution of various neurochemicals within the zona incerta: an immunocytochemical and histochemical study. Anat Embryol (Berl) 199:265–280

    Article  CAS  Google Scholar 

  • Kowski AB, Geisler S, Krauss M, Veh RW (2008) Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol 507:1465–1478

    Article  PubMed  Google Scholar 

  • Kretschmer BD (2000) Functional aspects of the ventral pallidum. Amino Acids 19:201–210

    Article  PubMed  CAS  Google Scholar 

  • Kuo H, Chang HT (1992) Ventral pallido-striatal pathway in the rat brain: a light and electron microscopic study. J Comp Neurol 321:626–636

    Article  PubMed  CAS  Google Scholar 

  • Laverghetta AV, Toledo CA, Veenman CL, Yamamoto K, Wang H, Reiner A (2006) Cellular localization of AMPA type glutamate receptor subunits in the basal ganglia of pigeons (Columba livia). Brain Behav Evol 67:10–38

    Article  PubMed  Google Scholar 

  • Lavin A, Grace AA (1994) Modulation of dorsal thalamic cell activity by the ventral pallidum: its role in the regulation of thalamocortical activity by the basal ganglia. Synapse 18:104–127

    Article  PubMed  CAS  Google Scholar 

  • Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T (2009) Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J Neurosci 29:444–453

    Article  PubMed  CAS  Google Scholar 

  • Maurice N, Deniau JM, Menetrey A, Glowinski J, Thierry AM (1997) Position of the ventral pallidum in the rat prefrontal cortex-basal ganglia circuit. Neuroscience 80:523–534

    Article  PubMed  CAS  Google Scholar 

  • McBride RL (1981) Organization of afferent connections of the feline lateral habenular nucleus. J Comp Neurol 198:89–99

    Article  PubMed  CAS  Google Scholar 

  • Mengual E, Pickel VM (2004) Regional and subcellular compartmentation of the dopamine transporter and tyrosine hydroxylase in the rat ventral pallidum. J Comp Neurol 468:395–409

    Article  PubMed  CAS  Google Scholar 

  • Mengual E, Casanovas-Aguilar C, Perez-Clausell J, Gimenez-Amaya JM (2001) Thalamic distribution of zinc-rich terminal fields and neurons of origin in the rat. Neuroscience 102:863–884

    Article  PubMed  CAS  Google Scholar 

  • Mitrofanis J (2005) Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta. Neuroscience 130:1–15

    Article  PubMed  CAS  Google Scholar 

  • Napier TC, Simson PE, Givens BS (1991) Dopamine electrophysiology of ventral pallidal/substantia innominata neurons: comparison with the dorsal globus pallidus. J Pharmacol Exp Ther 258:249–262

    PubMed  CAS  Google Scholar 

  • O’Donnell P, Lavin A, Enquist LW, Grace AA, Card JP (1997) Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J Neurosci 17:2143–2167

    PubMed  Google Scholar 

  • Pang K, Tepper JM, Zaborszky L (1998) Morphological and electrophysiological characteristics of noncholinergic basal forebrain neurons. J Comp Neurol 394:186–204

    Article  PubMed  CAS  Google Scholar 

  • Parent M, Parent A (2004) The pallidofugal motor fiber system in primates. Parkinsonism Relat Disord 10:203–211

    Article  PubMed  Google Scholar 

  • Parent M, Levesque M, Parent A (1999) The pallidofugal projection system in primates: evidence for neurons branching ipsilaterally and contralaterally to the thalamus and brainstem. J Chem Neuroanat 16:153–165

    Article  PubMed  CAS  Google Scholar 

  • Parent A, Sato F, Wu Y, Gauthier J, Levesque M, Parent M (2000) Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci 23:S20–S27

    Article  PubMed  CAS  Google Scholar 

  • Parent M, Levesque M, Parent A (2001) Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J Comp Neurol 439:162–175

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Paxinos G, Kus L, Ashwell KWS, Watson C (1999) Chemoarchitectonic atlas of the rat forebrain. Academic Press, California

    Google Scholar 

  • Phillipson OT, Griffiths AC (1985) The topographic order of inputs to nucleus accumbens in the rat. Neuroscience 16:275–296

    Article  PubMed  CAS  Google Scholar 

  • Pombero A, Bueno C, Saglietti L, Rodenas M, Guimera J, Bulfone A, Martinez S (2011) Pallial origin of basal forebrain cholinergic neurons in the nucleus basalis of Meynert and horizontal limb of the diagonal band nucleus. Development 138:4315–4326

    Article  PubMed  CAS  Google Scholar 

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

  • Sato F, Lavallee P, Levesque M, Parent A (2000) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J Comp Neurol 417:17–31

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Smith KS, Tindell AJ, Aldridge JW, Berridge KC (2009) Ventral pallidum roles in reward and motivation. Behav Brain Res 196:155–167

    Article  PubMed  Google Scholar 

  • Staines WA, Fibiger HC (1984) Collateral projections of neurons of the rat globus pallidus to the striatum and substantia nigra. Exp Brain Res 56:217–220

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW (1976) An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol 167:227–256

    Article  PubMed  CAS  Google Scholar 

  • Takada M, Hattori T (1987) The rat striatum: a target nucleus for ascending axon collaterals of the entopedunculo-habenular pathway. Brain Res 418:129–137

    Article  PubMed  CAS  Google Scholar 

  • Tham WW, Stevenson RJ, Miller LA (2009) The functional role of the mediodorsal thalamic nucleus in olfaction. Brain Res Rev 62:109–126

    Article  PubMed  Google Scholar 

  • Thompson LH, Grealish S, Kirik D, Bjorklund A (2009) Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur J Neurosci 30:625–638

    Article  PubMed  Google Scholar 

  • 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 

  • Turner MS, Lavin A, Grace AA, Napier TC (2001) Regulation of limbic information outflow by the subthalamic nucleus: excitatory amino acid projections to the ventral pallidum. J Neurosci 21:2820–2832

    PubMed  CAS  Google Scholar 

  • van der Kooy D, Carter DA (1981) The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res 211:15–36

    Article  PubMed  Google Scholar 

  • Velayos JL, Reinoso-Suárez F (1985) Prosencephalic afferents to the mediodorsal thalamic nucleus. J Comp Neurol 242:161–181

    Article  PubMed  CAS  Google Scholar 

  • Wright CI, Groenewegen HJ (1996) Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat. Neuroscience 73:359–373

    Article  PubMed  CAS  Google Scholar 

  • Wright CI, Beijer AV, Groenewegen HJ (1996) Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci 16:1877–1893

    PubMed  CAS  Google Scholar 

  • Wu Y, Richard S, Parent A (2000) The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Neurosci Res 38:49–62

    Article  PubMed  CAS  Google Scholar 

  • Young WS 3rd, Alheid GF, Heimer L (1984) The ventral pallidal projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence. J Neurosci 4:1626–1638

    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  PubMed  CAS  Google Scholar 

  • Zahm DS (1999) Functional-anatomical implications of the nucleus accumbens core and shell subterritories. Ann N Y Acad Sci 877:113–128

    Article  PubMed  CAS  Google Scholar 

  • Zahm DS, Brog JS (1992) On the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience 50:751–767

    Article  PubMed  CAS  Google Scholar 

  • Zahm DS, Heimer L (1988) Ventral striatopallidal parts of the basal ganglia in the rat: I. Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreactivity. J Comp Neurol 272:516–535

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Zahm DS, Trimble M (2008) The dopaminergic projection system, basal forebrain macrosystems, and conditioned stimuli. CNS Spectr 13:32–40

    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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank John F. Wesseling and Julio Artieda for critical readings of the manuscript and John F. Wesseling and Manuel Alegre for assistance with the electrophysiology. We also thank Francisco Clascá for donating the Sindbis virus vector for the Supplementary material. Anushree Tripathi is 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

  1. Division of Neurosciences, Center for Applied Medical Research (CIMA), Universidad de Navarra, Avda. Pío XII, 55, 31008, Pamplona, Navarra, Spain

    Anushree Tripathi & Elisa Mengual

  2. Departamento de Anatomía, Facultad de Medicina, Universidad de Navarra, Pamplona, Spain

    Elisa Mengual

  3. Departamento de Anatomía, Histología y Neurociencia, Facultad de Medicina, Universidad Autónoma de Madrid, Madrid, Spain

    Lucía Prensa

Authors
  1. Anushree Tripathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lucía Prensa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elisa Mengual
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisa Mengual.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tripathi, A., Prensa, L. & Mengual, E. Axonal branching patterns of ventral pallidal neurons in the rat. Brain Struct Funct 218, 1133–1157 (2013). https://doi.org/10.1007/s00429-012-0451-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-012-0451-0

Keywords

Search

Navigation