Cerebral Cortex, Vol 7, 359-373, Copyright © 1997 by Oxford University Press
RL Jakab, P Goldman-Rakic and C Leranth
In spite of accumulating evidence on the potent neuromodulatory,
neuroprotective, trophic and memory-enhancing effects of the neuropeptide
substance P (SP) in the cerebral cortex, the excitatory or inhibitory
nature of the cortical SP innervation remains unclear and the postsynaptic
targets of SP fibers are not defined. To obtain further insight into these
issues, we have examined SP-containing axons and their postsynaptic targets
in the prefrontal cortex of adult monkeys with single- and double label
immunocytochemistry combined with light and correlated electron microscopy.
SP fibers in the primate prefrontal cortex, unlike those in the rat cortex,
preferentially innervate cortical layers I, II and upper layer III. Our
results demonstrate for the first time that all SP-immunoreactive boutons
in all cortical layers contain GABA. Of the entire sample of SP boutons,
53% synapse on dendritic shafts, 39% on dendritic spines and 8% on cell
bodies. Another new finding is that synapse-forming SP boutons, in addition
to their known innervation of pyramidal cells, form pericellular baskets
around interneurons in layers II and upper III, a subpopulation of which
contains calbindin D28k. Finally, the study also revealed that SP boutons
frequently participate in 'synaptic triads' with spines which receive
another (asymmetric, putatively excitatory amino acid-utilizing) synapse.
Our findings indicate that SP/GABA axons in the primate prefrontal cortex
modulate excitatory amino acid- mediated neurotransmission and control
feed-forward disinhibitory GABAergic circuits in supragranular cortical
layers.
ARTICLES
Dual role of substance P/GABA axons in cortical neurotransmission: synaptic triads on pyramidal cell spines and basket-like innervation of layer II-III calbindin interneurons in primate prefrontal cortex
Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06520-8063, USA.
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