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Volume 17, Number 11,
Issue of June 1, 1997
pp. 4473-4485
Copyright ©1997 Society for Neuroscience
Postnatal Development of Serotonergic Innervation,
5-HT1A Receptor Expression, and 5-HT Responses in Rat
Motoneurons
Received Dec. 18, 1996; revised March 19, 1997; accepted March 21, 1997.
Edmund M. Talley,
Negar N. Sadr, and
Douglas A. Bayliss
Department of Pharmacology, University of Virginia,
Charlottesville, Virginia 22908
We compared the electrophysiological responses to serotonin (5-HT)
of neonatal and juvenile rat hypoglossal motoneurons (HMs) by using
intracellular recording techniques in a brainstem slice preparation. In
neonatal HMs ( P8), 5-HT caused a substantial decrease in the
amplitude of spike afterhyperpolarization (AHP) that was associated
with an increase in the minimal repetitive firing frequency
(Fmin). Previous work has shown that
this effect of 5-HT was mediated by the 5-HT1A receptor and
may be secondary to inhibition of N- and P/Q-type calcium channels. In
contrast to results from neonates, we found that 5-HT did not inhibit
the AHP in juvenile HMs ( P20). Application of a cocktail of calcium channel toxins ( -Conotoxin-GVIA and -Agatoxin-IVA) to juvenile HMs substantially inhibited the AHP, indicating that calcium entry through N- and P/Q-type channels supports the AHP in juvenile HMs, as
it does in neonates. In addition, intracellular injection of the
long-lasting GTP analog GTP S induced an agonist-independent increase
in Fmin similar to that seen in neonates in
the presence of 5-HT. Together, these results suggested that
intracellular mechanisms downstream of the 5-HT1A receptor
capable of inhibiting the AHP were intact in juvenile HMs. Therefore,
we investigated the possibility that age-related changes in effects of
5-HT on the AHP resulted from altered expression of the
5-HT1A receptor. To this end, we performed ligand-binding
autoradiography using [3H]8-OH-DPAT, a 5-HT1A
agonist, and in situ hybridization using radiolabeled
oligonucleotide probes specific for the 5-HT1A receptor. The two approaches gave remarkably similar results. The highest levels
of 5-HT1A receptor expression were found in neonatal HMs, with maximal binding and hybridization at approximately postnatal day 7 (P7) and only low levels of receptor expression by P28. Finally,
immunohistochemistry for 5-HT revealed that these developmental changes
in 5-HT1A receptor expression occurred coincident with a
postnatal increase in serotonergic innervation of the hypoglossal nucleus (nXII). Together, these findings indicate that developmental changes occur in the serotonergic innervation of nXII and in the expression of 5-HT1A receptors in HMs during the early
postnatal period, resulting in markedly different effects of 5-HT on
firing behavior in neonatal and juvenile HMs.
Key words:
ontogeny;
hypoglossal;
motoneuron;
raphe;
electrophysiology;
in situ hybridization;
radioligand
binding;
immunohistochemistry
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