Differential subcellular localization of forward and feedback interareal inputs to parvalbumin expressing GABAergic neurons in rat visual cortex.

In rat visual cortex, forward and feedback interareal pathways innervate both pyramidal and gamma-aminobutyric acid (GABA)ergic (Johnson and Burkhalter [1996] J. Comp. Neurol. 368:383-398). GABAergic neurons consist of different cell types of which the largest group expresses parvalbumin (PV; Gonchar and Burkhalter [1997] Cereb. Cortex 4:347-358). Here, we report that PV neurons in layers 2/3 are synaptic targets of forward and feedback projections between area 17 and the lateromedial area (LM) of rat visual cortex. In both forward and feedback pathways, approximately 90% of axon terminals in layer 2/3 labeled by tracing with biotinylated dextran amine formed synapses with PV-negative profiles. In both pathways, most of these profiles resembled dendritic spines. Although there were no differences in the innervation of PV-negative targets, the two pathways differed in the innervation of PV-positive neurons. In each pathway, approximately 10% of terminals formed synapses with PV-positive profiles. However, in the forward pathway, the size of the contacted PV-positive profiles was larger than in the feedback pathway. Moreover, in the forward pathway, axon terminals on PV-positive profiles were larger, contained more mitochondria and docked synaptic vesicles than feedback synapses on PV neurons. Our results show that PV neurons provide a major target for area 17 <-> LM forward and feedback pathways terminating in upper layers. In each pathway, the proportion of axons contacting PV neurons is similar. However, both pathways differ in the subcellular localization and morphology of synapses on PV neurons. These asymmetries may contribute to the inequality in the strength of disynaptic inhibition evoked by forward and feedback inputs (Shao and Burkhalter [1996] J. Neurosci. 16:7353-7365).