Dendritic arborization and spines of the neurons of the cat and human periaqueductal gray: A light, confocal laser scanning, and electron microscope study

Abstract

Neurons of the periaqueductal gray (PAG) have an extensive dendritic tree which plays an important role in the neuronal circuits supporting the functional activities of this region. The complexity of the local circuits is increased by the occurrence of dendritic spines. We have compared the dendritic and spine organization in the cat with that of man in order to verify whether an inverse relationship exists between dendritic tree extension and spine density and complexity. Sections of cat and human PAG prepared according to the Golgi-Cox method were studied with the conventional light microscope (LM) and the confocal laser scanning microscope (CLSM). The cat PAG was also studied at the electron microscopic level. The light microscopic study provided the morphoquantitative characteristics of the dendritic arborization and spines of the multipolar and fusiform neurons of the human and cat PAG. The CLSM methodology, thanks to the three-dimensional reconstruction of the neurons and the rotation of the reconstructed images, brought into view dendritic branches and spines that could not have been observed at the LM, thereby showing a wider dendritic tree and more numerous spines. The data combined from LM and CLSM demonstrate that in both species most spiny neurons are multipolar and probably projection neurons. In man, the multipolar neurons show a more extensive dendritic tree due to a wider secondary ramification, which would seem to be balanced by more numerous spines in cat. At the electron microscopic level, axo-dendritic synapses are numerous and show symmetrical and asymmetrical junctions in equal proportions; furthermore, the great majority of the spines are in contact with synaptic boutons which contain round vesicles and make predominantly asymmetrical contacts features which indicate excitatory activity. The combined use of different techniques gave a complete picture of the dendritic tree and spines of the neurons of human and cat PAG and showed a wider dendritic surface available for the receipt of the synaptic contacts than had been reported previously. Furthermore, our findings demonstrate that the PAG dendritic spines are important and specific structures in the synaptic complex of the neuropil, suggesting that they might create a local device to modulate and integrate the afferent inputs, probably in an excitatory way. The differences observed in the two species suggest that afferent information might be handled in different ways in human and cat PAG. Anat. Rec. 251:316–325, 1998. © 1998 Wiley-Liss, Inc. © 1998 Wiley-Liss, Inc.