The connections of local circuit neurons immunoreactive for calcium-binding protein calretinin (CR-ir) were studied in area 17 of the macaque monkey visual cortex. Most CR-ir neurons were located in layers 2 and 3A. They were polymorphic and included bitufted, multipolar, pyramid-shaped neurons with smooth dendrites and Cajal-Retzius cells. The majority of CR-ir neurons were gamma-aminobutyric acid (GABA)-immunopositive (approximately 90%), and compromised about 14% of the total GABAergic neuron population. The axons of CR-ir cells had local arbors within layers 1-3, but the major trunks descended to deep layers 5 and 6 where they formed dense terminal fields within narrow columns (100-150 microns). This specific innervation of layers 5 and 6 appeared as a distinct feature of area 17 as it was not seen in the adjacent area 18. CR-ir boutons (n = 168) were GABA-ir (95%) and formed symmetric synapses. In layers 1-3, the majority of postsynaptic targets (n = 64) were GABAergic local circuit neurons [postsynaptic target distribution: GABA-positive dendrites (67%) and somata (14%), and GABA-negative dendrites (13%) and spines (6%)]. In deep layers, the most synapses (80%; n = 187) were formed with pyramidal cells where they provided a basket-type innervation [postsynaptic target distribution: GABA-positive dendrites (19%) and somata (1%), and GABA-negative dendrites (50%), spines (20%) and somata (10%)]. Unlike other GABAergic neurons, which innervate mainly pyramidal neurons, the CR-ir subpopulation only has pyramids as a preferred target in the deep layers (layers 5 and 6); however, in the superficial layers of the area 17, selectively form synapses mainly with other GABAergic cells. Thus, the CR-ir neurons appear to have a dual function of disinhibiting superficial layer neurons and inhibiting pyramidal output neurons in the deep layers.