Serotonergic transmission in the periaqueductal gray matter in relation toaversive behaviour: Morphological evidence for direct modulatory effects on identified output neurons

Intracellular recordings were made from 21 cells in the dorsolateral periaq ueductal gray matter in coronal midbrain slices. In the majority (n = 20) b ath application of 5-hydroxytryptamine (30 or 150 mM) evoked either hyperpo larizing (n = 11) or depolarizing (n = 9) responses. Reconstructions of 11 neurons in the dorsolateral periaqueductal gray matter after filling with b iocytin revealed a population of output neurons whose axons followed a dors olateral trajectory towards the perimeter of the ipsilateral periaqueductal gray matter. In seven cells, the axon could be followed into the adjacent mesencephalic reticular formation. At the light microscopic level, immunost aining for 5-hydroxytryptamine revealed immunoreactive processes throughout the dorsolateral periaqueductal gray matter but no labelled somata or dend rites. Close associations (i.e. no discernible gap) were observed between s erotonergic profiles and the somata and dendrites of biocytin-filled cells. At the ultrastructural level, serial sections through 21 appositions on to biocytin-filled dendrites in three slices revealed 19 true appositions (i. e. having closely parallel plasma membranes with no intervening glial cell profiles) with the biocytin-filled dendrite. Only four of the appositions ( 21%) showed evidence of synaptic specializations which included aggregation s of synaptic vesicles, and some thickening of the apposing membrane. The d ense reaction product in the biocytin-filled cells precluded identification of the ultrastructure of postsynaptic elements. However, examination of co ntacts between 5-hydroxytryptamine-immunoreactive profiles and unlabelled e lements in material taken from the contralateral side of the periaqueductal gray matter (i.e. no biocytin present) or in material taken from perfusion -fixed whole brain, in which ultrastructural preservation was superior comp ared with slices, revealed a similar incidence (21% and 23%, respectively) of synaptic specializations. The data indicate that serotonergic transmission on to output neurons in th e dorsolateral periaqueductal gray matter is largely mediated by non-juncti onal contacts, suggesting that the actions of 5-hydroxytryptamine on these cells are mediated predominantly by volume rather than wiring transmission. (C) 1999 IBRO. Published by Elsevier Science Ltd.