The effect of cortical spreading depression, a proposed initiating event for migraine pain, on cortical blood flow (laser Doppler method) and on the spontaneous firing rate and stimulus-evoked responses of trigemino-cervical neurons with craniovascular input was studied in 17 neurons in 8 cats anesthetized with chloralose. Cortical spreading depression, induced via cortical pinprick injury, produced an initial wave of cortical hyperemia (243 ± 57% of control) and a later and smaller phase of oligemia (96 ± 4% of control). Neither the basal discharge rate (6.7 ± 1.7 sec-1) nor the evoked responses to electrical stimulation of the superior sagittal sinus (4.1 ± 0.8 discharges per stimulus) of upper cervical spinal cord neurons was altered over periods of up to 2 h following one, two, or three waves of spreading cortical depression. We conclude that a small number of episodes of cortical spreading depression is not capable of activating C2 cervical spinal cord craniovascular sensory neurons in the cat.
RussellMBOlesenJA nosographic analysis of the migraine aura in a general population.Brain1996;
119:
355–61
2.
PearceJMSIs migraine explained by Leao's spreading depression?Lancet1985;
2:
763–6
3.
LanceJWMechanism and management of headache.
5th ed.London:
Butterworth Scientific,
1993
4.
MoskowitzMANozakiKKraigRPNeocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms.J Neurosci1993;
13:
1167–77
5.
LambertGAMichalicekJCortical spreading depression reduces dural blood flow—a possible mechanism for migraine pain?Cephalalgia1994;
14:
430–6
6.
WolffHGHeadache and other head pain.New York:
Oxford University Press,
1963
7.
IngvardsenBKLaursenHOlsenUBHansenAJPossible mechanism of c-fos expression in trigeminal nucleus caudalis following cortical spreading depression.Pain1997;
72:
407–15
8.
StorerRJButlerPHoskinKLGoadsbyPJA simple method, using 2-hydroxypropyl-beta-cyclodextrin, of administering alpha-chloralose at room temperature.J Neurosci Methods1997;
77:
49–53
9.
StrassmanAMPotrebicSMaciewiczRJAnatomical properties of brainstem trigeminal neurons that respond to electrical stimulation of dural blood vessels.J Comp Neurol1994;
346:
349–65
10.
LambertGAZagamiASBogdukNLanceJWCervical spinal cord neurons receiving sensory input from the cranial vasculature.Cephalalgia1991;
11:
75–85
11.
PiperRDLambertGADuckworthJWCortical blood flow changes during spreading depression in cats.Am J Physiol.1991;
261:
H96–102
12.
MichalicekJGordonVLambertGAAutoregulation in the middle meningeal artery.J Cereb Blood Flow Metab1996;
16:
507–16
13.
NaglerJConfortiNFeldmanSAlterations produced by cortisol in the spontaneous activity and responsiveness to sensory stimulation of single cells in the tuberal hypothalamus of the rat.Neuroendocrinology1973;
12:
52–6
14.
SiegelSCastellanNJJNonparametric statistics for the behavioral sciences.New York:
McGraw-Hill,
1988
15.
ColquhounDLectures on biostatistics.Oxford:
Clarendon Press,
1971
16.
RasmussenBKEpidemiology of migraine. In:
Clifford RoseF, editor.
Towards migraine 2000.
Amsterdam:
Elsevier,
1996;
1–14
17.
LauritzenMJorgensenMBDiemerNHGjeddeAHansenAJPersistent oligemia of rat cerebral cortex in the wake of spreading depression.Ann Neurol1982;
12:
469–74
18.
ShimazawaMHaraHAn experimental model of migraine with aura—cortical hypoperfusion following spreading depression in the awake and freely moving rat.Clin Exp Pharmacol Physiol1996;
23:
890–2
19.
DienerHCMayANew aspects of migraine pathophysiology—lessons learned from positron emission tomography.Curr Opin Neurol Neurosurg1996;
9:
199–201
20.
BoersPLambertGAZagamiASThe response of trigeminal neurons to superior sagittal sinus stimulation is inhibited by 8-hydroxydipropylaminotetralin (8-OH-DPAT). Soc.Neurosci Abstr1997;
23:
1685
21.
KaubeHKeayKAHoskinKLBandlerRGoadsbyPJExpression of c-Fos-like immunoreactivity in the caudal medulla and upper cervical spinal cord following stimulation of the superior sagittal sinus in the cat.Brain Res1993;
629:
95–102
22.
StrassmanAMMinetaYVosBPDistribution of fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood vessels in the rat.J Neurosci1994;
14:
3725–35
23.
StrassmanAMRaymondSABursteinRSensitization of meningeal sensory neurons and the origin of headaches.Nature1996;
384:
560–63
24.
DavisKDDostrovskyJOActivation of trigeminal brain-stem nociceptive neurons by dural artery stimulation.Pain1986;
25:
395–401
25.
StrassmanAMasonPMoskowitzMMaciewiczRResponse of brainstem trigeminal neurons to electrical stimulation of the dura.Brain Res1986;
379:
242–50
26.
KaubeHHoskinKLGoadsbyPJActivation of the trigeminovascular system by mechanical distension of the superior sagittal sinus in the cat.Cephalalgia1992;
12:
133–6
27.
NozakiKBoccaliniPMoskowitzMAExpression of c-fos-like immunoreactivity in brainstem after meningeal irritation by blood in the subarachnoid space.Neuroscience1992;
49:
669–80
28.
TassorelliCJosephSANADPH-diaphorase activity and Fos expression in brain nuclei following nitroglycerin administration.Brain Res1995;
695:
37–44
29.
TassorelliCJosephSASystemic nitroglycerin induces Fos immunoreactivity in brainstem and forebrain structures of the rat.Brain Res1995;
682:
167–81
30.
RussellMBIversenHKOlesenJPresentation of a diagnostic aura diary. In:
OlesenJ, editor.
Headache classification and epidemiology.
New York:
Raven Press,
1994:
87–92
31.
ShimazawaMHaraHWatanoTSukamotoT.
Effects of Ca2+ channel blockers on cortical hypoperfusion and expression of c-fos-like immunoreactivity after cortical spreading depression in rats.
Br J Pharmacol.1995;
115:
1359–68
32.
MoskowitzMAKraigRComment on Ingvardsen, et al.Pain1997;
72:
407–15;
1998; 76: 265–6
33.
IngvardsenBKLaursenHOlsenUBHansenAJReply to Moskowitz, et al.Pain1998;
76:
266–7
34.
GoadsbyPJEdvinssonLEkmanRVasoactive peptide release in the extracerebral circulation of humans during migraine headache.Ann Neurol1990;
28:
183–7
35.
ZagamiASGoadsbyPJEdvinssonLStimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides.Neuropeptides1990;
16:
69–75
36.
PiperRDEdvinssonLEkmanRLambertGACortical spreading depression does not result in the release of calcitonin gene-related peptide into the external jugular vein of the cat: relevance to human migraine.Cephalalgia1993;
13:
180–3
37.
ReuterUWeberJRGoldLArnoldGWolfTDreierJPerivascular nerves contribute to cortical spreading depression-associated hyperemia in rats.Am J Physiol1998;
43:
H1979–87
38.
KorolevaVIBuresJRats do not experience cortical or hippocampal spreading depression as aversive.Neurosci Lett.1993;
149:
153–6
39.
KemperRHAMeijlerWJTerhorstGJTrigeminovascular stimulation in conscious rats.Neuroreport1997;
8:
1123–6
