Dendritic development and preferential growth into synaptogenic fields: a quantitative study of Golgi-impregnated spinal motor neurons

Abstract

Branching patterns of dendrites may be modulated by the way in which dendritic growth cone filopodia come into initial synaptic relationships with afferent axons. This synaptotropic hypothesis of dendritic branching predicts that dendritic growth will be directed preferentially into regions containing numerous prospective presynaptic elements. The developing mouse spinal cord provides a natural experiment to test this prediction, because synapses are found exclusively within the marginal zones bordering the motor columns during the early (E11-14) period of synaptogenesis. During this time, therefore, most motor dendritic growth would be expected to be directed laterally or ventrally into the marginal zones, whereas internally directed growth should become more prevalent later, when synaptogenesis begins to take place within the intermediate zone, i.e., the motor columns proper. A computer-assisted three dimensional reconstruction system has been used to test these expectations in Golgi preparations of developing mouse (C57BL/6J) spinal cords ranging in age from E13 through P1. Mean dendritic lengths and branch densities are significantly greater for marginal zone dendrites than for intermediate zone dendrites at early ages (E13-14), but there are no significant differences in these measures at later stages of development (P0,1). These findings are interpreted as meaning that motor dendritic growth is initially biased into the marginal zone by synaptogenic afferents and that this preferential distribution is progressively lost as synapses develop within the intermediate zone to attract or to stabilize internally directed dendritic growth. Thus the findings of this study are consistent with predictions of the synaptotropic hypothesis of dendritic branching.