Synaptic connectivity between rat striatal spiny projection neurons in vivo: Unexpected multiple somatic innervation in the context of overall sparse proximal connectivity

Abstract The principal neurons of the striatum, the GABAergic spiny projection neurons (SPNs), are connected by local axonal collateral synapses, but the extent of axosomatic synapses between striatal SPNs is unknown. If extensively present, somatic innervation would indicate potential for a subset of strong inhibitory connections, with important consequences for the computational neurodynamics of the striatal spiny projection neuron (SPN) network. We investigated the somatic innervation of 16 somata, and the proportion of postsynaptic targets that were somatic or dendritic, by mapping the axonal arborization of a single presynaptic SPN. A rat striatal SPN was injected intracellularly with biocytin during electrophysiological recording in vivo. This neuron's dendritic anatomy was suggestive of a D1-like SPN. Its local axons, synapses and postsynaptic targets were traced through a block of striatal tissue using 490 serial ultrathin sections and transmission electron microscopy. The biocytin-filled SPN made 47 definitive synapses within the axonal territory analyzed, of which 7 were somatic on SPNs, 34 were dendritic, and 6 were spinous. Thus, 15% of its synapses were axosomatic on other SPNs. Within the axonal territory analyzed, the biocytin-filled SPN innervated two unlabeled SPNs with either three or four somatic synapses each. Two other SPNs were each innervated with one putative somatic synapse. These results provide a definitive anatomical basis for somatic innervation of SPNs by collaterals of a putative D1-like SPN, which is substantially more extensive than previously assumed from indirect electrophysiological estimates of electrotonic location, quantal analysis of selected pairs, and statistical models based on quantitative neuroanatomy.