Journal of Neuroscience, Vol 9, 4333-4354, Copyright © 1989 by Society for Neuroscience
Neuropeptide Y in the cerebral cortex and the caudate-putamen nuclei: ultrastructural basis for interactions with GABAergic and non-GABAergic neurons
C Aoki and VM Pickel
Department of Neurology and Neuroscience, Cornell University Medical College, New York, New York 10021.
In the cerebral cortex and caudate-putamen (CP) nuclei, neuropeptide Y
(NPY) immunoreactivity is detectable within 1-2% of all neurons. The
NPY-immunoreactive neurons are interneuronal and are believed to be mostly
GABAergic in the cerebral cortex but not in the CP nuclei. Thus NPY and
GABA may play different roles in the circuitry within these 2 regions. We
tested this possibility by comparing the ultrastructure of NPY-containing
neurons between (1) cortex (somatosensory and anterior cingulate areas)
versus dorsolateral CP; and (2) GABAergic versus non- GABAergic NPY neurons
within each area. Single coronal sections through the rat forebrain were
dually labeled for GABA and NPY by combining immunoautoradiography with the
immunoperoxidase method. NPY-containing neurons with or without GABA
occurred throughout the rostrocaudal portions of CP and all laminae of
somatosensory and anterior cingulate cortex. Comparisons between the areas
confirmed that somata and terminals dually labeled for GABA and NPY were
more prevalent in the cortex. NPY terminals lacking detectable GABA
immunoreactivity also were found within the cortex, thus suggesting
additional heterogeneity in cortical NPY innervation. The ultrastructural
features of NPY perikarya in both regions were morphologically similar
regardless of whether the cells also contained GABA. Most synaptic inputs
to NPY neurons occurred at distal dendrites. In comparison to neighboring
neurons, synaptic inputs to proximal dendrites and somata of NPY neurons of
cortex and CP were rare, suggesting that fewer and weaker inputs may
modulate the excitability of NPY-containing neurons. In both regions,
nearly all NPY- and NPY-GABA-labeled terminals formed symmetric junctions
suggestive of inhibitory action. The majority of these junctions were with
dendrites containing neither NPY nor GABA. NPY terminals formed few
contacts on proximal dendrites and somata of GABAergic neurons (8% of 179
contacts in cortex; 12% of 73 contacts in CP) which, unlike most
singly-labeled GABAergic neurons, were sparsely innervated. Thus, NPY may
play a more prominent role in modulation of certain GABAergic neurons than
would be predicted by the observed frequency of NPY-to-GABA contacts in the
two regions. One notable regional difference was the greater prevalence in
cortex of axoaxonic associations between NPY-immunoreactive terminals and
other terminals, some of which also contained NPY. These nonsynaptic
associations may be involved in the modulation of (1) the release of NPY by
another transmitter or (2) NPY's modulation of release of other
transmitters in cortex.
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