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Journal of Neuroscience, Vol 13, 1167-1177, Copyright © 1993 by Society for Neuroscience
Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms
MA Moskowitz, K Nozaki and RP Kraig
Neurosurgery Service, Massachusetts General Hospital, Boston 02114.
The effects of neocortical spreading depression (SD) on the expression of
immunoreactive c-fos protein were examined within the superficial laminae
of trigeminal nucleus caudalis (TNC), a brainstem region processing
nociceptive information. KCl was microinjected into the left parietal
cortex at 9 min intervals over 1 hr, and SD was detected by a shift in
interstitial DC potential within adjacent frontal cortex. The stained cells
in lower brainstem and upper cervical spinal cord were counted on both
sides after tissues were sectioned (50 microns) and processed for c-fos
protein-like immunoreactivity (LI) using a rabbit polyclonal antiserum.
C-fos protein-LI was visualized in the ventrolateral TNC, chiefly in
laminae I and Ilo and predominantly within spinal segment C1-2 (e.g., -1.5
to -4.5 mm from obex) ipsilaterally. SD significantly increased cell
staining within ipsilateral TNC. The ratio of cells in laminae I and Ilo on
the left: right sides was 1.32 +/- 0.13 after 1 M KCl, as compared to 1.06
+/- 0.05 in control animals receiving 1 M NaCl instead of KCl
microinjections (p < 0.01). The ratio was reduced to an insignificant
difference after chronic surgical transection of meningeal afferents and
recurrent SD (1.09 +/- 0.11). Pretreatment with intravenous sumatriptan, a
5-HT1-like receptor agonist that selectively blocks meningeal C-fibers and
attenuates c-fos protein-LI within TNC after noxious meningeal stimulation,
also reduced the ratio to an insignificant difference (1.10 +/- 0.09).
Sumatriptan or chronic surgical transection of meningeal afferents,
however, did not reduce the ability of KCl microinjections to induce SD. On
the other hand, combined hyperoxia and hypercapnia not only reduced the
number of evoked SDs from 6.3 +/- 1.0 to 2.5 +/- 1.2 after 0.15 M KCl
microinjection, but also significantly (p < 0.01) reduced associated c-
fos protein-LI in TNC. These data indicate that multiple neocortical SDs
activate cells within TNC. The increase in c-fos protein-LI, observed
predominantly ipsilaterally, was probably mediated by SD- induced
stimulation of ipsilaterally projecting unmyelinated C-fibers innervating
the meninges. If true, this is the first report demonstrating that
neurophysiological events within cerebral cortex can activate brainstem
regions involved in the processing of nociceptive information via
trigeminovascular mechanisms.
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