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A quantitative study of the brainstem cholinergic projections to the ventral part of the oral pontine reticular nucleus (REM sleep induction site) in the cat

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Abstract

The ventral part of the cat oral pontine reticular nucleus (vRPO) is the site in which microinjections of small dose and volume of cholinergic agonists produce long-lasting rapid eye movement sleep with short latency. The present study determined the precise location and proportions of the cholinergic brainstem neuronal population that projects to the vRPO using a double-labeling method that combines the neuronal tracer horseradish peroxidase–wheat germ agglutinin with choline acetyltransferase immunocytochemistry in cats. Our results show that 88.9% of the double-labeled neurons in the brainstem were located, noticeably bilaterally, in the cholinergic structures of the pontine tegmentum. These neurons occupied not only the pedunculopontine and laterodorsal tegmental nuclei, which have been described to project to other pontine tegmentum structures, but also the locus ceruleus complex principally the locus ceruleus α and peri-α, and the parabrachial nuclei. Most double-labeled neurons were found in the pedunculopontine tegmental nucleus and locus ceruleus complex and, much less abundantly, in the laterodorsal tegmental nucleus and the parabrachial nuclei. The proportions of these neurons among all choline acetyltransferase positive neurons within each structure were highest in the locus ceruleus complex, followed in descending order by the pedunculopontine and laterodorsal tegmental nuclei and then, the parabrachial nuclei. The remaining 11.1% of double-labeled neurons were found bilaterally in other cholinergic brainstem structures: around the oculomotor, facial and masticatory nuclei, the caudal pontine tegmentum and the praepositus hypoglossi nucleus. The disperse origins of the cholinergic neurons projecting to the vRPO, in addition to the abundant noncholinergic afferents to this nucleus may indicate that cholinergic stimulation is not the only or even the most decisive event in the generation of REM sleep.

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Abbreviations

10M :

Motor nucleus of the vagus nerve

3 :

Nucleus of the oculomotor nerve

3N :

Oculomotor nerve

4 :

Nucleus of the trochlear nerve

4N :

Trochlear nerve

5M :

Motor nucleus of the trigeminal nerve

5N :

Trigeminal nerve

5P :

Principal trigeminal nucleus

5SN :

Spinal nucleus of the trigeminal nerve

5ST :

Spinal trigeminal tract

6 :

Nucleus of the abducens nerve

6N :

Abducens nerve

7 :

Nucleus of the facial nerve

7N :

Facial nerve

A :

Nucleus ambiguous

BC :

Brachium conjunctivum

BP :

Brachium pontis

Cnf :

Cuneiform nucleus

CS :

Central superior raphe nucleus

CtF :

Centrotegmental fascicle

DR :

Dorsal raphe nucleus

GR :

Gigantocellular reticular formation

IC :

Inferior colliculus

IO :

Inferior olive

Ip :

Interpeduncular nucleus

LC :

Locus coeruleus principal

LCC :

Locus coeruleus complex

LCα :

Locus coeruleus alpha

LdT :

Laterodorsal tegmental nucleus

Li :

Linearis centralis raphe nucleus

LL :

Lateral lemniscus

M5 :

Mesencephalic trigeminal tract

ML :

Medial lemniscus

MLF :

Medial longitudinal fascicle

MR :

Raphe magnus nucleus

MRF :

Mesencephalic reticular formation

P :

Pyramidal tract

PaG :

Central grey matter

PbD :

Dorsal parabrachial nucleus

Pbg :

Parabigeminal nucleus

PbV :

Ventral parabrachial nucleus

PH :

Praepositus hypoglossi nucleus

PoR :

Raphe pontis nucleus

PpT :

Pedunculopontine tegmental nucleus

Pα :

Perilocus coeruleus alpha

RB :

Restiform body

RM :

Raphe magnus nucleus

RN :

Red nucleus

RP :

Raphe pontis nucleus

RPC :

Caudal pontine reticular nucleus

RPO :

Oral pontine reticular nucleus

SC :

Superior colliculus

SCoe :

Nucleus subcoeruleus

SF :

Solitary fascicle

SN :

Substancia nigra

SO :

Superior olive

TD :

Dorsal tegmental nucleus of Gudden

Tp :

Tegmental pontine nucleus

Tr :

Trapezoid body

TV :

Ventral tegmental nucleus of Gudden

vRPO :

Ventral part of the RPO

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Acknowledgements

We thank Dr. I. De Andrés for critical reading and valuable suggestions of the manuscript and C. Warren for revising the English. The technical assistance of G. de la Fuente, P. Romero and R.M. Sánchez-Lozano is gratefully acknowledged. Supported by Grants DGESIC PB98-0097 and BFI2002–01314

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Authors and Affiliations

  1. Departamento de Morfología, Facultad de Medicina, Universidad Autónoma de Madrid, Arzobispo Morcillo 4, 28029, Madrid, Spain

    Margarita Lucía Rodrigo-Angulo & Fernando Reinoso-Suárez

  2. Departamento de Anatomía, Facultad de Veterinaria, Universidad Complutense de Madrid, Avda. Puerta de Hierro s/n, 28040, Madrid, Spain

    Elisia Rodríguez-Veiga

Authors
  1. Margarita Lucía Rodrigo-Angulo
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  2. Elisia Rodríguez-Veiga
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  3. Fernando Reinoso-Suárez
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Correspondence to Fernando Reinoso-Suárez.

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Rodrigo-Angulo, M.L., Rodríguez-Veiga, E. & Reinoso-Suárez, F. A quantitative study of the brainstem cholinergic projections to the ventral part of the oral pontine reticular nucleus (REM sleep induction site) in the cat. Exp Brain Res 160, 334–343 (2005). https://doi.org/10.1007/s00221-004-2015-x

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