The intrahippocampal distribution of axon collaterals of individual CA
3 pyramidal cells was investigated in the rat. Pyramidal cells in the
CA3 region of the hippocampus were physiologically characterized and f
illed with biocytin in anesthetized animals. Their axonal trees were r
econstructed with the aid of a drawing tube. Single CA3 pyramidal cell
s arborized most extensively in the CA1 region, covering approximately
two-thirds of the longitudinal axis of the hippocampus. The total len
gth of axon collaterals in the CA3 region was less than in CA1 and the
axon branches tended to cluster in narrow bands (200-800 mu m), usual
ly several hundred microns anterior or posterior to the cell body. The
majority of the recurrent collaterals of a given neuron remained in t
he same subfield (CA3a, b, or c) as the parent cell. CA3a neurons inne
rvated predominantly the basal dendrites, whereas neurons located prox
imal to the hilus (CA3c) terminated predominantly on the apical dendri
tes of both CA1 and CA3 cells. Two cells, with horizontal dendrites an
d numerous thorny excrescences at the CA3c-hilus transitional zone, we
re also labeled and projected to both CA3 and CA1 regions. All CA3 neu
rons projected some collaterals to the hilar region. Proximal (CA3c) n
eurons had numerous collaterals in the hilus proper. One CA3c pyramida
l cell in the dorsal hippocampus sent an axon collateral to the inner
third of the molecular layer. CA3c pyramidal cells in the ventral hipp
ocampus had extensive projections to the inner third of the dentate mo
lecular layer, as well as numerous collaterals in the hilus, CA3, and
CA1 areas, and several axon collaterals penetrated the subiculum. The
total projected axon length of a single neuron ranged from 150 to 300
mm. On the basis of the projected axon length and bouton density (mean
interbouton distance: 4.7 mu m), we estimate that a single CA3 pyrami
dal cell can make synapses with 30,000-60,000 neurons in the ipsilater
al hippocampus. The concentrated distribution of the axon collaterals
(''patches'') indicates that subpopulations of neurons may receive dis
proportionately denser innervation, whereas innervation in the rest of
the target zones is rather sparse. These observations offer new insig
hts into the physiological organization of the CA3 pyramidal cell netw
ork. (C) 1994 Wiley-Liss, Inc.