VITAMIN D
3
IMPROVES RESPIRATORY ADJUSTMENT TO FATIGUE
AND H-REFLEX RESPONSES IN PARAPLEGIC ADULT RATS
J. BIANCO,
a,b1
Y. GUEYE,
b1
T. MARQUESTE,
a
O. ALLUIN,
a
J.-J. RISSO,
c
S. GARCIA,
d
M.-N. LAVAULT,
d
M. KHRESTCHATISKY,
b
F. FERON
b2
* AND
P. DECHERCHI
a2
*
a
Institut des Sciences du Mouvement : Etienne-Jules MAREY (ISM :
EJM), UMR CNRS 6233, Université de la Méditerranée (Aix-Marseille II -
Aix-Marseille Université), Parc Scientifique et Technologique de Luminy -
Faculté des Sciences du Sport de Marseille - CC910 - 163, avenue de
Luminy - 13288 Marseille cedex 09 - France
b
Neurobiologie des Interactions Cellulaires et Neurophysiopathologie
(NICN), CNRS UMR 6184, Université de la Méditerranée (Aix-Marseille II
- Aix-Marseille Université), Faculté de Médecine Nord, Institut Fédératif
de Recherche Jean Roche (IFR11) - 51 boulevard Pierre Dramard -
13916 Marseille cedex 20 - France
c
Département de Recherche Marine et Subaquatique, Institut de Méde-
cine Navale du Service de Santé des Armée (IMNSSA), UMR MD2
PPCOE, Université de la Méditerranée (Aix-Marseille II - Aix-Marseille
Université) - BP610 - 83800 Toulon Armées - France
d
Service Hospitalier d’Anatomie et Cytologie Pathologiques Humaines,
Université de la Méditerranée (Aix-Marseille II - Aix-Marseille Université),
Assistance Publique - Hôpitaux de Marseille, Institut de Cancérologie et
d’Immunologie de Marseille (IFR 137), Faculté de Médecine Nord - 51
boulevard Pierre Dramard - 13916 Marseille cedex 20 - France
Abstract—We previously demonstrated that vitamin D
2
(er-
gocalciferol) triggers axon regeneration in a rat model of
peripheral nerve transection. In order to confirm the regen-
erative potential of this neuroactive steroid, we performed
a study in which vitamin D
3
(cholecalciferol) was delivered
at various doses to paralytic rats. After spinal cord com-
pression at the T10 level, rats were given orally either
vehicle or vitamin D
3
at the dose of 50 IU/kg/day or 200
IU/kg/day. Three months later, M and H-waves were re-
corded from rat Tibialis anterior muscle in order to quantify
the maximal H-reflex (H
max
) amplitude. We also monitored
the ventilatory frequency during an electrically induced
muscle fatigue known to elicit the muscle metaboreflex and
an increase in respiratory rate. Spinal cords were then
collected, fixed and immunostained with an anti-neurofila-
ment antibody. We show here that vitamin D-treated ani-
mals display an increased number of axons within the
lesion site. In addition, rats supplemented with vitamin D
3
at the dose of 200 IU/kg/day exhibit (i) an improved breath-
ing when hindlimb was electrically stimulated; (ii) an H-re-
flex depression similar to control animals and (iii) an in-
creased number of axons within the lesion and in the distal
area. Our data confirm that vitamin D is a potent molecule
that can be used for improving neuromuscular adaptive
mechanisms and H-reflex responses. © 2011 IBRO. Pub-
lished by Elsevier Ltd. All rights reserved.
Key words: vitamin D, monosynaptic Ia afferent reflex, mo-
toneuron recruitment, spasticity, compression, phrenic nerve.
Spinal cord injuries (SCI) that interrupt descending and
ascending pathways induce motor and sensory disorders:
the lack of motoneuronal inputs to muscles induces paral-
ysis and physiological adaptations like respiratory adjust-
ments during muscle fatigue and exercise are impaired
(Decherchi and Dousset, 2003). Usually, after an SCI,
takes place a spasticity syndrome characterized by hyper-
active tendon jerks, increased muscle tone, clonus, unin-
tentional flexor withdrawal and extensor spasm. These
symptoms are very debilitating as they can interfere with
residual motor function, produce pain, disrupt sleep, and,
at times, induce skin break-age (Little et al., 1989). Several
studies have shown that exaggerated cutaneous/flexor re-
flexes (Bennett et al., 1999; Remy-Neris et al., 1999) and
increased tonic stretch reflexes are involved in the produc-
tion of this syndrome (Burke et al., 1970; Powers et al.,
1989; Thilmann et al., 1991). In order to overcome these
post-traumatic events, clinicians and researchers are look-
ing for molecules with neuroprotective and neurotrophic
properties, preferably FDA-approved. Fulfilling all these
criteria, vitamin D is a prime candidate.
Vitamin D is a steroid that acts both as an immuno-
modulator and a neuroactive molecule [for recent reviews,
(Annweiler et al., 2010; Stewart et al., 2010; Fernandes de
Abreu et al., 2009)]. Recently, we showed, in a rat model of
peripheral nerve injury, that ergocalciferol (vitamin D
2
)—
the plant-derived form of vitamin D—increased axon re-
generation and improved the responses of metabosensi-
tive neurons to metabolites such as KCl and lactic acid
(Chabas et al., 2008). In a parallel study, using the same
animal model, we also demonstrated that cholecalciferol
(vitamin D
3
)—the animal-derived form of vitamin D—was
(i) more efficient than ergocalciferol and (ii) induced a
dramatic functional recovery when delivered at the dose of
500 international unit (IU)/kg/day (unpublished data).
These promising results led us to assess the therapeutic
benefit of vitamin D in a model of SCI.
It is well established that, after a trauma, many deaf-
ferented neurons transsynaptically degenerate below and
above the lesion but some motoneurons survive and re-
main functional (Kaelan et al., 1988; Eidelberg et al., 1989;
Bjugn et al., 1997; Chang, 1998; Jimenez et al., 2000;
Button et al., 2008). As a result, spinal segments that are
not fully injured remain able to exhibit functional activity
1
These authors contributed equally.
2
These authors have shared seniority.
*Corresponding author. Tel: +33 (0)4-91-82-84-09 or +33 (0)4-91-69-
89-70; fax: +33 (0)4-91-82-84-09 or +33 (0)4-91-25-89-70.
E-mail address: patrick.decherchi@univmed.fr (P. Decherchi) or
francois.feron@univmed.fr (F. Feron).
Abbreviations: EIF, electrically-induced muscle fatigue; EMG, electro-
myography; GABA, gamma amino-butyric acid; IU, International Unit;
SCI, spinal cord injuries.
Neuroscience 188 (2011) 182–192
0306-4522/11 $ - see front matter © 2011 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2011.04.066
182