Increased striatal proenkephalin mRNA subsequent to production of spreading depression in rat cerebral cortex: activation of corticostriatal pathways?

• Published in: Brain research. Molecular brain research. Vol. 61; no. 1; pp. 195 - 202
• Main Authors: Arabia, Anna-Maria, Shen, Pei-Juan, Gundlach, Andrew L
• Format: Journal Article
• Language: English
• Published: Amsterdam Elsevier B.V 30.10.1998; Elsevier
• Subjects: Animals; Biochemistry and metabolism; Biological and medical sciences; Brain; Central nervous system; Cerebral Cortex - chemistry; Cerebral Cortex - drug effects; Cerebral Cortex - metabolism; Cholecystokinin; Cholecystokinin - analysis; Cholecystokinin - genetics; Corpus striatum; Corpus Striatum - chemistry; Corpus Striatum - drug effects; Corpus Striatum - metabolism; Cortical spreading depression; Corticostriatal neurons; Depression, Chemical; Dynorphin; Enkephalin; Enkephalins - analysis; Enkephalins - genetics; Fundamental and applied biological sciences. Psychology; Gene Expression Regulation - drug effects; In Situ Hybridization; In situ hybridization histochemistry; Male; Membrane Potentials - drug effects; Neural Pathways - drug effects; Neural Pathways - physiology; Potassium Chloride - administration & dosage; Potassium Chloride - pharmacology; Prosencephalon - chemistry; Prosencephalon - drug effects; Prosencephalon - metabolism; Protein Precursors - analysis; Protein Precursors - genetics; Rats; Rats, Sprague-Dawley; RNA, Messenger - analysis; RNA, Messenger - biosynthesis; RNA, Messenger - drug effects; Vertebrates: nervous system and sense organs; In situ hybridization histochemistry; Cortical spreading depression; Enkephalin; Dynorphin; Corpus striatum; Corticostriatal neurons; Cholecystokinin; Cerebral cortex; Rat; Rodentia; Central nervous system; Proenkephalin; Basal ganglion; Gene expression; Neuropeptide; Vertebrata; Mammalia; Spreading depression; Brain (vertebrata)
• ISSN: 0169-328X; 1872-6941
• DOI: 10.1016/S0169-328X(98)00189-2

Cortical Spreading Depression (CSD) is a slowly propagating wave of depolarization and negative interstitial DC potential, that when induced in the rat brain extends across the entire homolateral hemisphere. Despite evidence that CSD does not penetrate into subcortical regions, neurochemical changes in areas anatomically connected to cortex have been reported. In this study in situ hybridization histochemistry was used to examine the levels of cholecystokinin (CCK), proenkephalin (ENK) and prodynorphin (DYN) mRNA in cortex and forebrain basal ganglia following KCl-induced CSD. Unilateral CSD was induced by topical application of 3 M KCl (∼10 μl) onto the right parietal cortex for 10 min and rats were then killed 1–6 h and 1–28 days later. CCK mRNA levels were increased ( P<0.01) in the ipsilateral neocortex 3 h after CSD (13% above levels in contralateral side), reached a peak at 2 days (∼70%) and were still elevated at 7 (30%) but not, 14 or 28 days later. Unilateral CSD also produced a rapid and sustained increase ( P<0.05) in ENK mRNA in ipsilateral piriform cortex (from 3 h to 2 days; 70–250% above contralateral), and a delayed increase in caudate putamen and olfactory tubercle at 1 and 2 days (∼25% in both regions), but levels were again equivalent to control at 7 days and beyond. In contrast, no marked changes in neocortical ENK mRNA, or DYN mRNA in both cortex and basal ganglia, were observed under these conditions. These findings demonstrate that CSD has specific, rapid and long-lasting effects on neuropeptide expression in neocortex and subcortical areas. CSD-induced changes in mesostriatal ENK mRNA are proposed to reflect synaptic activation of local neurons via cortical afferent projections.