In mammals, topographic maps emerge from initially diffuse projections during development. To gain insight into the mechanisms governing the transition from a diffuse projection to a topographic map, we studied topographic specificity of functional connections during development, using the cat corticorubral system as a model. In the adult cat, rubrospinal neurons in the dorsomedial part of the red nucleus (RN) receive input primarily from the forelimb area of the sensorimotor cortex, whereas those in the ventrolateral part receive input primarily from the hindlimb area. During development, axons from the sensorimotor cortex arrive in the RN at embryonic day 50 (E50) (Song et al., 1995a) and are diffusely distributed in the RN until postnatal day 13 (P13) (Higashi et al., 1990). Here, we studied the development of the pattern of functional cortical inputs to individual rubrospinal neurons, using synaptic potentials recorded in vivo. The functional topography in each rubrospinal neuron in developing cats was examined and classified either as adult-like or nonadult-like by comparison with the adult pattern. In preterm kittens from E61 to E65, only about half of the recorded neurons (41%; n ϭ 22) showed adult-like functional topography. This percentage, however, increased to 82% (n ϭ 56) in P1-P8 kittens and to 93% (n ϭ 42) in P13-P28 kittens. These results, in conjunction with the above mentioned anatomical observations, suggest that corticorubral axons make functional synapses nonselectively with rubrospinal neurons before birth. Furthermore, the functional topographic map developed earlier than the anatomical map (ϽP8 vs ϾP13), suggesting that there is a developmental step of selective promotion of synapse formation and/or selective enhancement of synaptic efficacy in topographically appropriate regions in the RN, before the emergence of the mature anatomical map.
Key words: topographic map; sensorimotor cortex; red nucleus; rubrospinal neuron; immature synapse; intracellular recordingTopographic organization in neuronal connections provides a structural basis for parallel processing in the brain. The development of topographic maps, therefore, has been a subject of intense research (for review, see Udin and Fawcett, 1988;Gierer and Muller, 1995;Roskies et al., 1995). In order for a topographic map to form, growth cones must navigate along precise pathways, find their target, and then make synapses with appropriate neurons in the target. The central issue in the formation of topographic maps is, therefore, how axons find input-recipient cells in their target region.This issue has been extensively studied in the retinotectal projections of fish and amphibians. In these species, retinal axons are guided or restricted to the topographically correct tectal regions without errors from the outset of innervation (Sakaguchi and Murphey, 1985;Stuermer, 1988). Interactions between retinal axons and tectal neurons via position-specific molecules have been suggested to be involved in such precise guidance (for review, see St...