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Cerebral Cortex 1994; 4:376-390
© Oxford University Press 1994

research-article

Passive Avoidance Training Induces Enhanced Levels of Immunoreactivity for Muscarinic Acetylcholine Receptor and Coexpressed PKC{gamma} and MAP-2 in Rat Cortical Neurons

E A. der Van Ze, B. R K Douma, B. Bohus and P. G. M. Luiten

Department of Animal Physiology, University of Groningen 9750 AA Haren, The Netherlands

Changes in neocortical immunoreactivity (ir) for mus-carinic acetylcholine receptors (mAChRs), protein ki-nase C{gamma} (PKC{gamma}), microtubule-associtiated protein 2 (MAP-2), and the calcium-binding protein parvabumin(PARV) induced by the performance of a one-trial passive shock avoidance (PSA) task were studied in young adult male Wistar rats. In experiment I, four groups of animals were formed: three control groups (N, naive; H, habituated but nonshocked; and S, habituated and shocked), and a fully trained group (T, habituated and shocked, followed by a retention trial 24h after the footshock). Compared to native animals, the H, S, and T animals all revealed enhanced cortical ir for mAChRs, PKC{gamma}, and MAP-2 in discrete subsets of cortical neurons in layers 2, 3, and 5, while no changes were found for PARV. The neurons displaying enhanced levels of ir are of the pyramidal and nonpyramidal cell type and are arranged in a columnar manner. Immunofluorescent double-labeling experiments for mAChR, PKC{gamma} and MAP-2 revealed that individual cortical neurons localized within the columns display enhanced ir for all three funtionally related proteins. Compared to native animals, all experimental groups revealed significant increases in the total size of cortical areas showing enhanced ir (H, S, and T over N). A further significant increase is found in animals receiving a footshock over nonshocked animals (S over H, respectively). The retention trial, however, did not induce a further increase (T over S). In some of the animals the patterns appeared to be lateralized, in either the left or right hemisphere.

In order to test the role of cholinergic innervation in the induction of enhanced mAChR-ir, unilateral lesions of the nucleus basalis magnocellularis (nbm) were performed in experiment II. Apparently, an intact cholinergic innervation from the nbm is not required for the occurence of the aforementioned columnar patterns. However, when the enhanced columnar patterns in the sensory areas of the cortex are cholinergically deprived, clear deficits in PSA performance are obsereved. These results indicate that although ACh is not a prerequisite for the induction of enhanced ir for mAChRs in Cortical cells, such neurons demand cholinergic neurotransmis-sion for optimal retention of the shock experience. The alterations in ir for coexpressed mAChR, PKC{gamma}, and MAP-2 in a discrete subset of cholinoceptive cortical neurons arranged in characteristic patterns most likely represent part of the neuronal substrate involved in functional cortical plasticity related to PSA training.


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