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Sleep Research Online 1(3): 102-108, 1998http://www.sro.org/1998/Fort/102/Printed in the USA. All rights reserved.

1096-214X 1998 WebSciences

The state of paradoxical sleep (PS) is characterized by thesimultaneous appearance of desynchronized EEG activity andthe atonia of the anti-gravitic muscles including those of theoro-facial sphere (Jouvet, 1962). By means of intracellularrecordings in unanesthetized head-restrained cats, combinedwith the local iontophoretic application of strychnine (aglycinergic antagonist), pharmacological evidence has been

provided that the loss of muscular tone is mainly due to a PS-specific tonic hyperpolarization of cranial (including facial,trigeminal and hypoglossal) and spinal motoneurons byglycine (Glenn et al., 1978; Morales and Chase, 1978;Chandler et al., 1980; Nakamura et al., 1978; Chase et al.,1980, 1989; Morales et al., 1987; Soja et al., 1987a, 1987b,1991; review in Chase and Morales, 1990; Yamuy et al., 1998).Recently, it has been further shown in the cat that the PS-specific glycinergic inhibition of motoneurons is potentiatedby opioids (Xi et al., 1996). Indeed, microiontophoreticapplication during PS of morphine, an opiate receptor agonist,increased the amplitude of the inhibitory post-synaptic

potentials (IPSP) evoked in lumbar motoneurons by electricalstimulation of the medullary reticular formation. Moreover,Naloxone, a non-selective opiate receptor antagonist, reducedthe IPSP's amplitude.

Of great interest regarding these data, we reported thatMethionin-Enkephalin (M-Enk) afferent projections to the catfacial nucleus (FN) originate from the caudal raphe nuclei andthe nucleus paragigantocellularis lateralis. We also showed thatthe M-Enk inputs to the cat trigeminal motor nucleus (TMN)

arise from the rostral ventromedial medullary reticularformation (nuclei reticularis magnocellularis andgigantocellularis and nucleus paragigantocellularis lateralis)and the caudal raphe nuclei (Fort et al., 1989, 1990). Amongthese structures, it seems unlikely that the enkephalinergicprojections from the caudal raphe nuclei to the FN and TMNplay a role in the oro-facial atonia of PS. Indeed, enkephalin i

colocalized with serotonin in these neurons (Hunt and Lovick1982; Lger et al., 1986; Fort et al., 1989, 1990) and a numbeof studies indicate that serotonin has a facilitary rather than aninhibitory action on motoneurons (McCall and Aghajanian1979; Jacobs and Fornal, 1993). In contrast, enkephalinergicprojections from the rostral ventromedial medullary reticularformation to the FN and TMN could play a role in the atonia othe oro-facial musculature during PS in as much as this regionmore precisely the nucleus reticularis magnocellularis (Mc)has been proposed to contain neurons responsible for thehyperpolarization of motoneurons during PS (Magoun andRhines, 1946; Pompeiano, 1967; Sakai et al., 1979, 1981

Nakamura, 1986; Lai and Siegel, 1988; Yamuy et al., 1993).To test this hypothesis, it was necessary to preciselyreexamine the localization of the M-Enk neurons in the rostraventromedial medullary reticular formation projecting to theTMN and FN. Indeed, in our previous studies, we localizedthese neurons projecting to the FN and the TMN in differennuclei respectively the paragigantocellularis lateralis nucleusand the nucleus reticularis magnocellularis. Further, we did noprovide detailed localization and counting of the double-

Anatomical Demonstration of a Medullary EnkephalinergicPathway Potentially Implicated in the Oro-Facial Muscle

Atonia of Paradoxical Sleep in the Cat

Patrice Fort, Claire Rampon, Damien Gervasoni, Christelle Peyronand Pierre-Herv Luppi

Neurobiologie des tats de Sommeil et d'veil, INSERM U480, Universit Claude Bernard, Lyon 69373, France

The present study was aimed to compare in detail the distribution within the rostral ventromedial medulla of Methionin-Enkephalin-immunoreactive neurons with efferent projections to the facial or trigeminal motor nuclei, using a doubleimmunostaining technique in colchicine-treated cats.

Following cholera toxin B subunit injections in the facial or trigeminal motor nuclei, we found that respectively 55% and65% of the medium to large-sized retrogradely labeled cells in the lateral part of the nucleus reticularis magnocellularis wereMethionin-Enkephalin-positive. For both motor nuclei, the double-labeled neurons had similar morphology and size and were

located exactly in the same area. They could therefore belong to the same population of reticular enkephalinergic neurons.Based on these and previous anatomical and electrophysiological data, we propose that these enkephalin-containing neuronscould participate in the hyperpolarization of brainstem and spinal somatic motoneurons during paradoxical sleep.

CURRENT CLAIM: This study describes a new enkephalinergic pathway potentially involved in the atonia of oro-facialmuscles during paradoxical sleep.

Correspondence: Dr. Patrice Fort, Neurobiologie des tats de Sommeil et d'veil, INSERM U480, Facult de Mdecine, Universit ClaudeBernard, 8 avenue Rockefeller, 69373, cedex 08, Lyon, France, Tel: 33-4-78-77-71-23, Fax: 33-4-78-77-71-72 , E-mail: [email protected]


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103 FORT ET AL.

labeled cells. Therefore, to localize and compare the

distribution of M-Enk-immunoreactive neurons within therostral ventromedial medulla projecting to the FN or TMN, wecombined retrograde tracing with cholera toxin B (CTb)subunit and M-Enk immunohistochemistry in colchicine-treated cats.

METHODS

Tracer injection and perfusion-fixation procedure

For the retrograde-tracing experiments, 17 adult cats of bothsexes weighing 2.5-4.0 kg were used (n = 9 for the FN and n =8 for the TMN). Under profound anesthesia with pentobarbital(25 mg/kg, i.v.), 0.1 l of 1% CTb (List Biological

Laboratories) was injected stereotaxically into the right TMNor FN with a 5-l Hamilton syringe. Twenty-four hours afterthe tracer injection, two guide cannulae were implanted abovethe lateral and fourth ventricles for the colchicine treatment(200 g in 20 l of 0.9% NaCl for each ventricle). Forty-eighthours later, the cats were deeply anesthetized and perfusedthrough the ascending aorta with 1 liter of Ringer's lactatesolution, followed by 2.5 liters of an ice-cold fixative in 0.1MPB (pH 7.4) containing 4% paraformaldehyde (PF), 0.1%glutaraldehyde and 0.2% picric acid (PA). After overnightpost-fixation, the brains were put in a 30% sucrose solution at4C for 48 hours.

Double-immunostaining procedure

Immunohistochemical detection of CTb was carried out bysequential incubations of free-floating coronal sections (20mthick). They were first submitted to a long incubation over 3-4days at 4C with a goat CTb antiserum (1:40,000, LisBiological Laboratories, in PB saline with 0.3% Triton X-100and 0.1% azide, PBST-A). They were then incubated for 90min at room temperature in biotinylated donkey anti-goat IgG(1:2,000) followed by streptavidin-HRP (1:40,000, JacksonImmunores. Laboratories). Finally, the sections were immersedin 0.02% 3,3'-diaminobenzidine-4HCl (DAB, Sigma)containing 0.003% H2O2 and 0.6% nickel ammonium sulfatein 0.05 M Tris-HCl buffer (pH 7.6) for 10-15 min at roomtemperature.

The same sections were then incubated for 4-6 days at 4Cin rabbit antiserum to Methionin-Enkephalin (M-Enk, 1:5,000UCB), 90 min at room temperature in swine anti-rabbit IgG(1:400) and then in rabbit peroxidase-antiperoxidase (1:400PAP, DAKO). After rinses, the sections were reacted for 15-30min at room temperature with 0.025% DAB solutioncontaining 0.006% H2O2.

The CTb reaction products obtained by the DAB-nickehistochemical procedure consisted of black punctate granulesin the cell soma and dendrites, whereas the M-Enkimmunohistochemical reaction product revealed using DABappeared as a homogeneous light brown staining of the cel

Figure 1. Photomicrograph of a frontal section that was processed for immunohistochemical staining of CTb (DAB-Nickel, black punctatestaining) and M-Enk (DAB, brown coloration), showing singly M-Enk+ and double-labeled cells in the lateral part of the Mc, medial to the facialnucleus, following a tracer injection in the TMN. Bar: 30 m


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104ENKEPHALIN AND ORO-FACIAL ATONIA DURING PARADOXICAL SLEEP

Figure 2. Series of drawings of 20 m frontal sections from rostral to caudal level of the rostral ventromedial medulla illustrating the location ofsingly M-Enk+ (), singly CTb+ (o) and CTb+/M-Enk+ double-labeled (*) cells in the Mc after tracer injection in the right FN (left column, catQ108) and TMN (right column, cat P115). Each symbol represents one labeled cell body. Abbreviations according to the atlas of Berman (1968):7 (facial nucleus), A (nucleus ambiguus), Gc (nucleus reticularis gigantocellularis), IO (inferior olivary complex), lvs (lateral vestibulospinaltract), Mc (nucleus reticularis magnocellularis), P (pyramidal tract), RM (nucleus raphe magnus), Rpa (nucleus raphe pallidus), rs (rubrospinaltract).


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body (Fig. 1). The specificity of the antibody against M-Enkwas assessed by the absorption test. Specific staining of the M-Enk-like immunoreactive cell bodies was totally blocked whenthe primary antiserum was pre-incubated with an excess (100g-1 mg/ml) of the synthetic peptide.

Data analysis

The distribution of the singly CTb (CTb+), singly M-Enk(M-Enk+) and double-labeled (CTb+/M-Enk+) cells within theMc is illustrated in Figure 2 for one representative injectioncase restricted to the right FN (left column, cat Q108) and one

restricted to the right TMN (right column, cat Q115). For thispurpose, 4 sections at different rostro-caudal levels of the Mcwere observed and drawn at low power magnification (x6.3)with a Leitz Orthoplan microscope equipped with an X/Ysensitive stage and a video camera connected to acomputerized image data analysis system (Biocom, France).The labeled cells were plotted at higher power magnification(x16-25). Drawings were then assembled with AdobeIllustrator 7.0 software on a Macintosh computer. In order toprecisely evaluate and directly compare the enkephalinergicprojections to the FN and TMN, singly CTb+, singly M-Enk+

and double-labeled CTb+/M-Enk+ neurons were counted

bilaterally in the Mc. These counts (Table 1) and theproportions of the different contingents of labeled cells (Table2) are provided for two representative cats for each motornucleus injected (cats S106 and Q108 for the FN and cats P110and Q115 for the TMN).

The photomicrograph was taken with a Leitz microscopeconnected to a camera (Vario-orthoplan) and then scanned. Toget an optimal reproduction of the staining, we modified thecontrast and luminosity of the crude scan with AdobePhotoshop 4.0 on a Macintosh computer. The illustration platewas then printed with a color dye printer (Epson Stylus color).

RESULTS

Inputs to the TMN and FN from the Mc

As previously described, pressure injection of 0.1 l of CTbtypically resulted in very small deposits, with a spread ofapproximately 400 m from the needle point (Fort et al., 1989,1990). Following CTb injection restricted to the FN (n = 5) orthe TMN (n = 2), similar distributions of retrogradely-labeledwithin the brainstem reticular formation were observedbetween the different animals. The lateral medullary reticularformation, mainly the nucleus reticularis parvicellularis (Pc),

105 FORT ET AL.

Table 1

Total (N cells) and Average (Mean SD) Numbers of Singly CTb+, Singly M-Enk+ and Double-Labeled CTb+/M-Enk+

Cells in the Ipsilateral and Contralateral Mc, Following Tracer Injection in the FN or TMN. The counts were based on

two representative CTb injection cases for each motor nucleus.

Singly CTb Singly Enk Double CTb-EnkTotal Mc (Mc-Tot) Lateral Mc (Mc-Lat) Large Cells (in Mc-Lat) in Mc-Lat in Mc-Lat

N cells (16 sections) 243 152 105 332 58FN (Mc ipsi)Mean SD 15.2 4.7 9.5 4.2 6.6 2.4 20.8 7.8 3.6 1.8

N cells (14 sections) 184 121 97 288 63TMN (Mc ipsi)Mean SD 13.1 3.8 8.6 2.7 6.9 2.2 20.6 5.9 4.5 2.4

N cells (16 sections) 69 38 28 304 15FN (Mc contra)Mean SD 4.3 2.5 2.4 2.4 1.8 1.7 19 7.3 0.9 0.9

N cells (14 sections) 41 20 13 298 7TMN (Mc contra)Mean SD 2.9 2.1 1.4 1.2 0.9 0.9 21.3 6.5 0.5 0.7

Table 2Proportions of the Different Populations of Labeled Cells Encountered within the Ipsilateral and Contralateral Mc,

Following Tracer Injection in the Right FN or TMN (based on counts reported in Table 1)

Singly CTb In the Mc-Lat In the Mc-Tot In the Mc-Lat

Proportions Mc-Lat/Mc-Tot Large CTb/Singly CTb Double/Singly Enk Double/Singly CTb Double/Singly CTb Double/Large CTb

FN (Mc ipsi) 62.6% 69.1% 17.5% 23.9% 38.2% 55.2%

TMN (Mc ipsi) 65.8% 80.2% 21.9% 34.2% 52.1% 64.9%

FN (Mc contra) 55.1% 73.7% 4.9% 21.7% 39.5% 53.6%

TMN (Mc contra) 48.8% 65.0% 2.3% 17.1% 35.0% 53.8%


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contained the largest number of CTb+ neurons (not illustrated).A substantial number of CTb+ neurons were also seen in therostral ventromedial medulla, bilaterally with a clear ipsilateraldominance (Table 1). In this region, they occupied a relativelysmall rostro-caudal and medio-lateral extension of the Mc,from the level of the caudal half of the FN to the rostral thirdof the inferior olivary complex (P7.5 to P9 levels according to

the atlas of Berman, 1968) (Fig. 2). A precise analysis furthershowed that the number and pattern of distribution of CTb+

cells were similar after injections in the TMN or FN. Indeed,the mean number of ipsilateral CTb+ cells for a section wasapproximately 15 and 13 cells in the Mc (Mc-Tot) followingtracer injections in the FN and TMN, respectively.Furthermore, approximately two-thirds of these CTb+ cells(Table 2, first column) were clustered in the lateral part of theMc (Mc-Lat). Rostrally, they were just medial and ventro-medial to the FN in the lateral vestibulo-spinal tract (lvs) (Fig.2 A,A' and B,B'). Slightly more caudally, the cluster of CTb+

cells was dorsolateral to the inferior olivary complex anddorsal to the rubro-spinal tract (rs) (Fig. 2 B-C, B'-C'). At the

most caudal level, they were ventral to the lateral part of thenucleus reticularis gigantocellularis (Gc) in an area medial tothe nucleus ambiguus (A) (Fig. 2 D and D'). In all injectioncases considered, the medial part of the Mc contained amoderate number of CTb+ cells while only a small numberwere seen in the raphe magnus and pallidus nuclei.

Of particular interest were also the cytological similaritiesof the CTb+ cells within the Mc-Lat following tracer injectionsin the FN or TMN. Indeed, within this area, a very largemajority of the CTb+ cells (around 70% and 80% for the FNand TMN, respectively; Tables 1 and 2, second column) weremedium to large in size (30 x 20 m), round to ovoid in shape,and multipolar.

M-Enkephalin-immunoreactive neurons projecting to the

TMN and FN

By means of colchicine treatment, two main groups of M-Enk-like immunoreactive (M-Enk+) cell bodies were labeledwithin the rostral ventro-medial medulla: the former in theraphe magnus and pallidus nuclei and the latter in the lateralpart of the Mc (Mc-Lat) (Fig. 2). Within the Mc-Lat, the M-Enk+ cells were numerous (approximately 20 cells for asection, Table 1), situated ventro-medially to the FN and morecaudally, dorsolaterally to the inferior olivary complex.

As illustrated in Figure 2, after all injections in the TMN orFN, the double-labeled (CTb+/M-Enk+) cells formed at the

most rostral level a cluster in the Mc-Lat, medio-ventral to theFN and ventrally to the lateral vestibulo-spinal tract (lvs).Slightly more caudally, the CTb+/M-Enk+ neurons were in theMc-Lat and the adjacent nucleus paragigantocellularis lateralis(PGCL) in and around the lateral vestibulo-spinal tract. Thecaudal extension of the group was located in the Mc-Lat withinthe lvs, as well as more dorsally in the Gc and the Pc just lateralto it. At all levels, the medial Mc contained only occasionalCTb+/M-Enk+ cells. In the Mc-Lat, the mean number ofCTb+/M-Enk+ cells for a section was approximately 4 for theFN and TMN, respectively (Table 1). Of the singly M-Enk+

neurons in this area, around 20% for both the FN and TMN

were retrogradely-labeled (Table 2, third column), while theCTb+/M-Enk+ cells represented approximately 40% and 50%of the CTb+ cells encountered in this area (Table 2, fifthcolumn).

The CTb+/M-Enk+ cells were all medium to large in size (30x 20 m) and round to ovoid in shape (Fig. 1). They accountedfor a large majority of the medium- to large-sized retrogradely

labeled cells within the Mc-Lat (around 55% and 65% for theFN and TMN, respectively; Table 2, sixth column).

DISCUSSION

In this study, we demonstrated that the TMN and FN receivea major enkephalinergic input from neurons in the lateral parof the Mc (Mc-Lat) located in the rostral ventro-mediamedulla. Our detailed comparison of the results further suggesthat the Methionin-enkephalin (M-Enk) positive neuronsprojecting to these two motor nuclei could belong to the samepopulation of cells and might therefore contribute to thesimultaneous hyperpolarization of the FN and TMN

motoneurons during PS episodes. In the following part of thediscussion, we report experimental data, mainly in catssupporting this hypothesis.

It is well known in cats that serotonin is frequently co-localized with M-Enk in neurons of the rostral ventro-mediamedulla (Hunt and Lovick, 1982; Lger et al., 1986). Howeverwe previously observed no or only occasional serotonin-immunoreactive neurons retrogradely labeled in the Mc-Lafollowing CTb injections in the FN or TMN (Fort et al., 19891990). These data indicate that the M-Enk neurons in the McLat are not serotonergic "PS-off cells" (reviewed in Jacobs andFornal, 1993).

Besides, electrophysiological studies in freely-moving cats

reported a few cells in the Mc with a tonic increase of theirfiring rate selectively during PS episodes (namely "PS-on"cells) projecting to the TMN as shown by antidromic activation(Sakai et al., 1979, 1981; Nakamura, 1986). These cells werelocated in the same region as the M-Enk neurons we foundprojecting to the TMN and FN, namely in the Mc-LatMoreover, this region receives a projection from the dorso-medial pontine area responsible for the muscle atonia duringPS (Sakai et al., 1981). Furthermore, it has recently beenreported that the rostral ventro-medial medulla containednumerous C-fos-positive neurons following PS hypersomniainduced by carbachol micro-injections in the dorsal pontinetegmentum (Yamuy et al., 1993). Combining C-fos immuno-

histochemistry and retrograde-tracing with CTb, the sameauthors further found in the Mc-Lat a population of doublelabeled neurons specifically activated during PS and projectingto the TMN (Morales et al., 1996). Therefore, it is tempting tohypothesize that the M-Enk neurons in the lateral Mc withinputs to the FN and TMN correspond to the inhibitory "PS-on" premotoneurons in the cat.

However, it has been demonstrated that the majorcomponent of the suppression of the masseteric and spinalmotor activity during PS is ascribable to a strychnine-sensitivepostsynaptic inhibition during PS (Soja et al., 1987a, 1987bChase et al., 1989; Soja et al., 1991). These results indicate tha



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the amino acid glycine is the principal mediator of thehyperpolarization of motoneurons during PS. The localizationof the glycinergic premotoneurons responsible is still a matterof debate. It was originally hypothesized that, during PS,excitatory neurons in the nucleus reticularis magnocellularistonically stimulate glycinergic premotoneurons localized in theparvocellular reticular nucleus (Pc) for the cranialmotoneurons or the intermediate zone of the spinal cord for thespinal motoneurons (Magoun and Rhines, 1946; Pompeiano,1967; Sakai et al., 1979, 1981). Later, a number of studiessuggested that the glycinergic neurons responsible for thehyperpolarization of cranial and spinal motoneurons could bedirectly located in the Mc (Fort et al., 1989, 1990; Holstege andBongers, 1991; Fort et al., 1993; Yamuy et al., 1993; reviewedin Holstege, 1996). If this hypothesis is correct, Methionin-enkephalin could be co-contained in these glycinergic neurons.However, in recent studies in the rat, it has been shown that thePc provides a strong glycinergic projection to the FN or theTMN and the Mc only a weak one (Li et al., 1996; Rampon etal., 1996; Li et al., 1997). These contradictory results might be

explained by species differences. Another possibility is that theglycinergic neurons responsible for the hyperpolarization ofcranial motoneurons during PS are localized in the Pc. If this isthe case, the M-Enk neurons localized in the Mc-Lat andprojecting to the cranial motoneurons would not beglycinergic. They would facilitate the hyperpolarizationinduced by glycinergic neurons from the Pc.

Finally, numerous neuroanatomical studies in catsdemonstrated that, in addition to the TMN and FN, the Mc-Latsends efferent projections to spinal motoneurons (Sakai et al.,1981; Alstermark et al., 1987; Ohta et al., 1990). It has furtherbeen shown combining retrograde tracing with M-Enkimmunohistochemistry that this projection is also in part

enkephalinergic in nature (Fung et al., 1994). Altogether, thesedata suggest that neurons within the lateral part of the Mc,containing M-Enk, could participate in the hyperpolarizationof the cranial and also of spinal motoneurons during PS in the cat.

Conclusion and new hypothesis

Our experimental data suggest that in the cat theenkephalinergic neurons in the lateral part of the Mc couldparticipate in the hyperpolarization of the cranial motoneuronsduring PS. These neurons could also participate in thehyperpolarization of spinal motoneurons during this state ofsleep. Further anatomical and electrophysiologicalinvestigations focused on this enkephalinergic cell group are

necessary in cats to test this hypothesis.

ACKNOWLEDGMENTS

The investigations in this report were supported byINSERM, CNRS and DRET (grants 90/1615 and 91/130). Wewould like to express our gratitude to Denise Salvert andColette Buda for their skillful technical assistance.

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Facial Nucleus