Development of forward and feedback connections between areas V1 and V2 of human visual cortex.

We have determined the sequence in which forward connections between visual cortical areas V1 and V2, and feedback connections between V2 and V1 develop in humans. For this purpose Dil was injected into V1 and V2 of postmortem brains of different pre- and postnatal ages. The laminar distribution of labeled fibers and cell bodies in V1 and V2 indicates that forward and feedback connections emerge shortly before birth. The development of both pathways proceeds over several postnatal months such that the laminar termination pattern of forward connections appears relatively mature before feedback connections reach their mature form. At 37 weeks of gestation both forward and feedback connections originate exclusively from deep-layer neurons, which extend axons in deep layers only. By 9 d postnatal, forward connections from V1 to V2, in addition to layers 5 and 6, also arise from neurons in layer 4B of V1. At this stage for the first time forward fibers enter layer 4 at the topographically appropriate location of V2. At 9 d postnatal most feedback fibers from V2 still occupy deep layers of V1 but many, through interstitial growth, elaborate vertical sprouts at regular intervals along the length of horizontal axons. As feedback connections mature, distal segments of horizontal axons are pruned back to branch points and fibers assume L-shaped configurations. By 7 weeks of age forward fibers from V1 enter V2 through deep and superficial layers and provide input to layers 3 and 4. At this stage feedback fibers from V2 have entered layer 4B of V1. By 4 months of age forward connections have assumed all the laminar characteristics of mature connections; that is, they arise from layers 2/3, 4B, 5, and 6 of V1, and terminate in layers 3 and 4 of V2. In sharp contrast, at 4 months of age feedback connections to V1 are still immature, showing terminations in layers 4B, 5, and 6 but no input to layer 2/3. The protracted postnatal emergence of feedback connections is similar to that of local long-range connections within layer 2/3 of V1 (Burkhalter et al., 1993). Since both of these circuits are thought to provide information about the context in which objects are seen, it is interesting to speculate that the late onset of texture segmentation in infants (Atkinson and Braddick, 1992; Sireteanu and Rieth, 1992) may be related to the postnatal maturation of specific intracortical circuits.