Introduction : The systemic
administration of low doses of dopamine (DA)
agonists, such as apomorphine, piribedil,
lisuride and 3-PPP, induces yawning and penile
erection in rats. Such a response is apparently
mediated by the stimulation of central DA
receptors of the D2 type, according to the
nomenclature of Kebabian and Calnell. Indeed,
both penile erection and yawning are induced by
D2 DA agonists, but not by selective Dl DA
agonists such as SKF 38393, and are prevented by
selective D2 DA antagonists such as sulpiride .
Unlike low doses, high doses of D2 DA agonists
induce hypermotility and stereotypy, but
suppress penile erection and yawning.
Experimental evidence has shown that
hypermotility and stereotypy by high doses of D2
DA agonists are due to the stimulation of
postsynaptic DA receptors localized in the
caudate nucleus and in the nucleus accumbens.
On the contrary, the localization of DA
receptors mediating yawning and penile erection
is still controversial. It has been suggested
that yawning induced by DA agonists is mediated
by DA 'autoreceptors', a special kind of DA
receptors located on the nerve endings and cell
bodies of the dopaminergic neuron itself, whose
stimulation leads to the inhibition of neuronal
dopaminergic activity. Such an hypothesis is
supported by studies showing that yawning is
abolished by the destruction of the
nigrostriatal DA system by 6-hydroxydopamine
(6OHDA). However, the above conclusions have
been questioned by recent experimental evidence
suggesting that DA receptors mediating yawning
are postsynaptic DA receptors . As to the DA
receptors mediating penile erection, the problem
is even more complicated, since it has still to
be determined whether or not these DA receptors
are the saine that mediate yawning or another
population of DA receptors. In order to clarify
the above controversy, it would be helpful to
determine the brain area where DA agonists act
to induce pende erection and yawning. In an
attempt to identify such brain area(s), we have
microinjected apomorphine into discrete brain
areas through chronically implanted guide
cannulae. The results show that low doses of
apomorphine and other DA agonists induce penile
erection and yawning when injected into the
paraventricular nucleus of the hypothalamus
(PVN).
[...]
Discussion : The present results show
that nanogram amounts of apomorphine induce
penile erection and yawing when injected into
the hypothalamic PVN. Although spreading of the
drug to hypothalamic areas surrounding the PVN
is possible, it is unlikely that such responses
are mediated by other hypothalamic nuclei since
injection of apomorphine in regions very close
to the PVN, such as the ventromedial and
dorsomedial nucleus and the preoptic area, was
ineffective. Similarly, ineffective were also
injections into the substantia nigra, the
striaturn and nucleus accumbens, the brain areas
that contain the highest levels of DA and that
mediate hypermotility and stereotypy induced by
DA agonists. The ineffectiveness of an
apomorphine injection into the striatum to
elicit yawning is in contrast with previous
studies showing that yawning is induced by the
bilateral injection of apomorphine into the
caudate nucleus. The discrepancy may be
explained by the fact that in these studies
doses of apomorphine (5µg and higher) were
used that were too high. Such doses have
probably resulted in a spread of the drug to the
active site. The present results are also in
contrast with the finding that the destruction
of the nigrostriatal DA system by 6-OHDA
abolishes yawning induced by apomorphine. A
possible explanation for the failure of
apomorphine to induce yawning might be the
development of DA receptor supersensitivity,
that favors the appearance of hypermotility and
stereotypy masking yawning and pende erection.
Alternatively, il might be that an intact
nigrostriatal DA systern is necessary for the
expression of yawning.
As to the possible site of action of
apomorphine in the PVN, il is noteworthy that D2
DA receptors have been detected in this area,
and that the PVN contains the cell bodies of DA
neurons of the A14 group, that constitute, the
so-called incertohypothalamic DA system,
together with those of the Al l and A13 groups.
This system consists of short, locally
projecting neurons whose fibers arborize
extensively soon after they have left their cell
bodies and also project to the anterior and
lateral hypothalamus and preoptic area . Recent
experiments suggest the presence of DA
autoreceptors on the incertohypothalamic DA
neurons controlling DA synthesis. Therefore,
penile erection and yawning might be due to the
autoreceptor-mediated inhibition of such
neurons. However, the finding that penile
erection and yawning were el cited by (+)-3-PPP,
but not by (-)-3-PPP, and that apomorphine
responses were antagonized by SCH 23390 supports
the hypothesis that yawning reflects activation
of postsynaptic DA receptors rather than
autoreceptor-mediated inhibition of DA
transmission. In fact, as previously discussed
for yawning induced by systemically injected
apomorphine, both 3-PPP enantiomers are DA
autoreceptor agonists, but have different
postsynaptic properties: namely, al this site
the (+)-enantiomer is an agonist while the
(-)-enantiorner is an antagonist. (-)-3-PPP,
because of its pre- and postsynaptic action,
would have been more active than the
(+)-enantiomer, if yawning reflected the
inhibition of DA transmission. Similarly, SCH
23390 has been shown to antagonize postsynaptic
DA receptor-mediated effects of apomorphine, but
to be unable to antagonize DA
autoreceptor-mediated responses: SCH 23390 would
have been ineffective in antagonizing the
apomorphine response, if DA autoreceptors in the
PVN behaved as DA autoreceptors in the
nigrostriatal DA system.
Irrespective of their location, DA receptors
mediating yawning and penile erection apparently
are of the D2 type because of their response
being reproduced by the selective D2 agonist LY
171555, but not by the Dl agonist SKF 38393, and
antagonized by sulpiride, a specific D2
antagonist. However, the finding that SCH 23390
antagonized apomorphine-induced yawning and
penile erection is in agreement with recent
observations showing that this rather selective
Dl antagonist paradoxically abolishes other
responses to apomorphine, which are considered
to be mediated by D2 receptors. These responses
also include yawning induced by systemic
apomorphine or LY 171555 administration 13 . An
explanation for this paradox might be sought in
the still unknown relationship between D1 and D2
receptors.
The present results suggest that the
hypothalamic PVN is the target of systemically
injected DA agonists to produce yawning and
pende erection, and that the
incertohypothalamic DA system has a
physiological role in controlling these
behaviors. Il is noteworthy that: (a)
stretching-yawning syndrome and penile erection
can be induced, other than by DA agonists, by
ACTH-derived peptides and by oxytocin, (b) that
the hypothalamic regions surrounding the third
ventricle are the most sensitive brain areas for
the induction of these effects by ACTH, (c) that
the PVN, where oxytocinergic neurons are
located, is the most sensitive site in the brain
for oxytocin-induced penile erection and
yawning. The link between DA, oxytocin and ACTH
in controlling yawning and/or pende erection and
the link between penile erection and yawning are
still obscure.
Pharmacological interactions suggest that DA,
oxytocin and ACTH receptors controlling the
above responses are situated downhill one after
the other in a sequence. Accordingly, blockade
of DA receptors by neuroleptics fails to inhibit
the effect of oxytocin and ACTH whereas blockade
of oxytocin receptors with the potent oxytocin
antagonist, d(CH2)5 Tyr(Me)-Orn-vasotocin,
results in the inactivation of apomorphine and
oxytocin but not ACTH responses. Finally, DA
agonist-induced yawning, like ACTH-and
oxytocin-induced yawning and penile erection, is
abolished by pretreatment with antimuscarinic
drugs. Since yawning also is induced by the
systemic injection of muscarinic agonists it has
been suggested that yawning is a consequence of
an increased cholinergic transmission secondary
to the inhibition of DA release. However,
this hypothesis has not been proved yet by
injecting directly antimuscarinic drugs into
discrete brain areas. Hence the site where
antimuscarinic agents act to abolish yawning is
still unknown. As to a possible interaction
between DA and acetylcholine in the PVN,
cholinergic fibers and terminals as well as
muscarinic receptors have been identified in
this nucleus. However, it is still unknown if a
direct interaction exists between the two
neurotransmitters.
In conclusion, the present results
indicate for the first time that the
incertohypothalamic DA neurons play an important
physiological role in controlling yawning and
pende erection.
- Colosimo C,
Francesco E. Pontieri, Virgilio Gerald H.
Evidente, Katrina Gwinn Hardy, John D.
O'Sullivan, Andrew J. Lees, Andrew J. Hughes,
Joseph H. Friedman, and Jessica Goren Yawning in
Parkinson's disease Neurology 1999 Jan
15;52(2):428
- Eguibar JR
et Moyaho A Inhibition of grooming by
pilocarpirpine differs in high-and low yawning
sublines of Sprague-Dawley rats. Pharmacoology
Biochemistry and Bebavior 1997; 58: 2
317-322
- Moyaho A et al Induced grooming transitions
and open field behaviour differ in high and
low-yavning sublines of Sprague-Dawley rats.
Anim Behav 1995; 50 ; 61-72
- Urba-Holmgren R,
Trucios N, Holmgren B, Eguibar JR, Gavito A,
Cruz G, Santos A Genotypic dependency of
spontaneous yawning frequency in the rat Behav
Brain Res 1990 Oct 30;40(1):29-35
- Urba-Holmgren
R, Santos A, Holmgren B, Eguibar JR Two
inbred rat sublines that differ in spontaneous
yawning behavior also differ in their responses
to cholinergic and dopaminergic drugs Behav
Brain Res 1993 Sep 30;56(2):155-9
- Urba-Holmgren
R, Holmgren B, Rodriguez R, Gonzalez RM
Serotonergic modulation of yawning Pharmacol
Biochem Behav 1979 Sep;11(3):371-2
- Urba-Holmgren
R, Gonzalez RM, Holmgren B Is yawning a
cholinergic response? Nature 1977 May 19 267
(5608): 261-2 et commentaires Cholinergic link
in yawning A Cowan Nature 12/01/78 271
p187-188
- Urba-Holmgren
R, Holmgren B, Leon BA, Ugarte A
Age-dependent changes in serotonergic modulation
of yawning in the rat. Pharmacol Biochem Behav
1992 Oct;43(2):483-6
- Stretchings and
yawnings induced by adrenocorticotrophic
hormone GL Gessa
- Drugs affecting
dopamine neurons ans yawning behavior
Mogilnicka E, Klimek V
- Paraventricular
nucleus lesion prevents yawning and penile
erection induced by apomorphine and oxytocin but
not by ACTH in rats Argiolas A
- Hypophysectomy
prevents yawning and penile erection but not
hypomotility induced by apomorphine Serra
G
- ACTH
and alpha-MSH induced grooming, stretching,
yawning and penile erection in male rats: site
of action in the brain and role of melanocortin
receptors Argiolas A
- Yawning
and penile erection: central
dopamine-oxytocin-adrenocorticotropin
connection Argiolas A
- Reduction
of drug-induced yawning and penile erection by
the activation of GABAa receptors in the
paraventricular nucleus: involvement of nitric
oxide MR Melis, A Argiolas
-
- -Colosimo
C, Francesco E. Pontieri, Virgilio Gerald H.
Evidente, Katrina Gwinn Hardy, John D.
O'Sullivan, Andrew J. Lees, Andrew J. Hughes,
Joseph H. Friedman, and Jessica Goren Yawning in
Parkinson's disease Neurology 1999 Jan
15;52(2):428
- -Dewey RB
Jr, Hutton JT, LeWitt PA, Factor SA A
randomized, double-blind, placebo-controlled
trial of subcutaneously injected apomorphine for
parkinsonian off-state events.Arch Neurol 2001
Sep;58(9):1385-1392
- -Goren,
Friedmann Yawning : an aura for an L Dopa
induced "off" in Parkinson diesease Neurologie
50(3), 823, 1998
- -Mogilnicka E,
Klimek V Drugs affecting dopamine neurons
ans yawning behavior. Pharmacol Biochem Behav
1977; 7; 303-305
- -Zarrindast MR,
Toloui V, Hashemi B Effect of GABAergic
drugs on physostigmine-induced yawning in rats.
Psychopharmacology (Berl) 1995:
122:297-300.
|