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The Journal of Neuroscience, July 15, 2000, 20(14):5346-5357

Activity-Dependent Regulation of Substance P Expression and Topographic Map Maintenance by a Cholinergic Pathway

Shichun Tu¹, Christopher M. Butt¹, James R. Pauly², and Elizabeth A. Debski¹

¹ School of Biological Sciences, and ² Division of Pharmaceutical Sciences, College of Pharmacy, University of Kentucky, Lexington, Kentucky 40506

We have assessed the role of activity in the adult frog visual system in modulating two aspects of neuronal plasticity: neurotransmitter expression and topographic map maintenance. Chronic treatment of one tectal lobe with the non-NMDA receptor antagonist, 6-cyano-7-nitroquinoxaline-2,3-dione decreased the percentage of substance P-like immunoreactive (SP-IR) tectal cells in the untreated lobe while disrupting topographic map formation in the treated one. Treatment with the NMDA receptor antagonist D-()-2-amino-5-phosphonovaleric acid (D-AP-5) disrupted the topographic map but had no affect on SP-IR cells. These results indicate that maintenance of the topographic map is dependent on direct input from the glutamatergic retinal ganglion cells, whereas substance P (SP) expression is being regulated by a pathway that relays activity from one tectal lobe to the other. Such a pathway is provided by the cholinergic nucleus isthmi, which is reciprocally connected to the ipsilateral tectum and sends a projection to the contralateral one.

Mecamylamine and atropine, antagonists of nicotinic and muscarinic receptors, respectively, were used together to block all cholinergic activity or alone to block receptor subclass activity. All three treatments decreased SP expression and disrupted the topographic map in the treated tectal lobe. We conclude that both SP expression and topographic map maintenance in the adult optic tectum are activity-dependent processes. Although our results are consistent with the maintenance of the topographic map through an NMDA receptor-based mechanism, they suggest that SP expression is regulated by a cholinergic interaction that depends on retinal ganglion cell input only for its activation.

Key words: NMDA receptor; non-NMDA receptor; muscarinic receptor; nicotinic receptor; neurotransmitter expression; Elvax; optic tectum; retinotectal topography; nucleus isthmi; visual plasticity; neuropeptides; autoradiography; pipiens

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20145346-12$05.00/0

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