Postnatal development of thalamic recipient neurons in the monkey striate cortex: II. Influence of afferent driving on spine acquisition and dendritic growth of layer 4C spiny stellate neurons.

This study uses Golgi-impregnated material to examine the effects of altering the nature of afferent driving on the maturation of spines and dendrites on thalamic recipient spiny stellate neurons in layers 4C alpha and beta of the monkey striate cortex. These two laminae receive input from different sets of thalamic afferents with different functional properties. The development of dendritic spine and dendritic branch populations on these neurons in experimental animals is compared to the same features on similar groups of neurons in a series of normal animals described in the preceding study (Lund and Holbach, '91). Three conditions of rearing were used to alter afferent driving from normal: complete darkness (with in some cases return to normal diurnal light-dark cycle), bilateral eye lid suture, and monocular eye lid suture. Some of the normal and dark-reared infant monkeys were examined behaviorally for visual capacity in an earlier study (Regal et al., '76). All conditions of abnormal afferent driving caused changes from the normal developmental patterns of spine and dendritic arbor growth in these first-order neurons of the cortex and each condition differed in the nature of change produced. Major findings of this study are: 1 Vigorous spine acquisition and dendritic growth occurs under all conditions of visual deprivation on alpha and beta neurons. Eventual spine and dendritic attrition occurs under at least conditions of bilateral or monocular lid suture to produce a rather constant adult morphology. We assume, therefore, that visually driven activity is a modulator or shaper of the developmental process for thalamic recipient neurons of visual cortex, rather than being an initiator, terminator, or driving force for their maturation. 2 An innate “clock” whose nature is unknown but is apparently not driven by visual input, initiates and terminates a period of growth of the thalamic recipient neurons between birth and 30–32 weeks of age. 3 Factors controlling dendritic arbor growth and retraction are different from those controlling spine synapse addition or attrition. 4 Whereas the alpha and beta neurons normally show quite different early growth patterns between birth and 30 weeks of age, when both eyes are simultaneously deprived of vision, an early temporal and numerical convergence occurs in patterns of spine population development on the two groups of neurons. This convergent pattern assumes a different form in dark-reared and lid-sutured animals. This suggests that the different patterns of development normally seen in the alpha and beta neurons depend on receiving different patterns of afferent driving, not on innate differences between alpha and beta neurons or links to different afferent axon populations independent of activity patterns. 5 Monocular suture was found to affect aspects of spine acquisition and dendritic growth of layer 4C neurons after 30 weeks of age. This may be due to a lack of development of layer 4C synaptic connections normally supporting binocular interactions in more superficial layers.