This study examined the synaptic terminal coverage of primate triceps surae (TS) motoneurons at the electron microscopic level. In three male pigtail macaques, motoneurons were labeled by retrograde transport of cholera toxin-horseradish peroxidase that was injected into TS muscles bilaterally and visualized with tetramethylbenzidine stabilized with diaminobenzidine. Somatic, proximal dendritic, and distal dendritic synaptic terminals were classified by standard criteria and measured. Overall and type-specific synaptic terminal coverages and frequencies were determined. Labeled cells were located in caudal L5 to rostral S1 ventral horn and ranged from 40 to 74 microns in diameter (average, 54 microns). The range and unimodal distribution of diameters, the label used, and the presence of C terminals on almost all cells indicated that the 15 cell bodies and associated proximal dendrites analyzed here probably belonged to alpha-motoneurons. Synaptic terminals covered 39% of the cell body membrane, 60% of the proximal dendritic membrane, and 40% of the distal dendritic membrane. At each of these three sites, F terminals (flattened or pleomorphic vesicles, usually symmetric active zones, average contact length 1.6 microns) were most common, averaging 52%, 56%, and 58% of total coverage and 56%, 57%, and 58% of total number of cell bodies, proximal dendrites, and distal dendrites respectively. S terminals (round vesicles, usually asymmetric active zones, average contact length 1.3 microns) averaged 24%, 29%, and 33% of coverage and 33%, 35%, and 36% of number at these three sites, respectively. Thus, S terminals were slightly more prominent relative to F terminals on distal dendrites than on cell bodies. C terminals (spherical vesicles, subsynaptic cisterns associated with rough endoplasmic reticulum, average contact length 3.5 microns) constituted 24% and 11% of total terminal coverage on cell bodies and proximal dendrites, respectively, and averaged 11% and 6% of terminal number at these two locations. M terminals (spherical vesicles, postsynaptic Taxi bodies, some with presynaptic terminals, average contact length 2.7 microns) were absent on cell bodies and averaged 3% and 7% of total coverage and 2% and 5% of terminals on proximal and distal dendrites, respectively. Except for M terminals, which tended to be smaller distally, terminal contact length was not correlated with location. Total and type-specific coverages and frequencies were not correlated with cell body diameter. Primate TS motoneurons are similar to cat TS motoneurons in synaptic terminal morphology, frequency, and distribution. However, primate terminals appear to be smaller, so that the fraction of membrane covered by them is lower.
The caudal medial accessory subdivision of the inferior olive (cMAO) receives information from the hindlimb from both the gracile nucleus and the lumbosacral spinal cord. This study determined which elements in cMAO serve as the postsynaptic targets of the gracile projection and whether these elements also receive input from the lumbosacral spinal cord. Gracile axons were labeled in cats by anterograde transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP), visualized with tetramethylbenzidine. Convergence of gracile and lumbosacral axons was evaluated by labeling in the same animal, one pathway by WGA-HRP and the other by degeneration. In cMAO, gracile axons synapse with equal probability on dendritic spines and distal dendritic shafts. This termination pattern contrasts markedly with that of other somatosensory inputs to the inferior olive and may account for the greater heterogeneity in responses to somatosensory stimuli displayed by neurons in cMAO. The distal dendritic shafts receiving gracile input were more likely than dendritic spines to receive convergent input from putative inhibitory synapses. The most likely source of these inhibitory synapses is the parasolitary nucleus, a structure that has been shown by others to receive input from the cerebellum. Thus the parasolitary nucleus may serve as an inhibitory relay between the cerebellum and cMAO. The dendritic spines in cMAO that receive input from the gracile nucleus often receive additional input from the lumbosacral spinal cord. This convergence of somatosensory axons on dendritic spines may provide a mechanism through which the unusually complex receptive fields of neurons in cMAO are generated.
Three functional regions of the inferior olive, the caudal medial accessory olive (cMAO) and the caudal and rostral dorsal accessory olive (DAO) receive input from the spinal cord. The present study determined how spinal inputs to cMAO interact with olivary neurons. These inputs were labeled by injections in cat lumbosacral of wheat germ agglutinin conjugated to horseradish peroxidase. The tracer was visualized with tetramethylbenzidine. The morphology of the labeled spino-olivary terminals and the relationship between these terminals and postsynaptic elements were determined. Spino-olivary terminals in cMAO displayed the morphological characteristics classically associated with excitatory synapses. Almost three quarters synapsed on spines, most of which contacted other spines, forming spine clusters. The majority of postsynaptic spines also received convergent input from apparently excitatory, nonlumbosacral afferents. This postsynaptic organization provides several possible benefits for the putative role of cMAO in the control of posture. An earlier study demonstrated that in DAO, almost three quarters of lumbosacral, spino-olivary terminals synapse on dendrites (Molinari: Neuroscience 27:425-435, 1988). Thus, lumbosacral afferents appear to differ fundamentally in the way in which they interact with neurons in cMAO and DAO. These results suggest that the way information is processed may be as important in determining the functional differences between olivary regions as what information is received.
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