Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study

Abstract

The distribution of geniculocortical afferents serving the left and right eyes was studied in abult cats and in kittens of various ages. Methods used were autoradiography of transneuronally transported 3 H‐proline injected into one eye, and physiological recordings. In the adult cat, patches of label in layer IV corresponding to ocular dominance columns were seen both ipsilateral and contralateral to the injected eye. Between the patches, however, grain density was substantially above background, especially on the contralateral side. Similarly, in the contralateral lateral geniculate nucleus (LGN) there was substantial labelling of neuronal cell bodies in lamina A1, which receives no innervation from the injected eye. Such spillover of radioactivity into the inappropriate laminae of the LGN was measured in autoradiographs of semithin sections, and its effect on the cortical labelling pattern calculated. Spillover appeared to account quantitatively for the labelling seen between patches in the cortex. It was concluded that the geniculocortical afferents for the ipsilateral and contralateral eyes are equally and almost completely segregated from each other at the centers of columns, although there is extensive overlap at the borders. This pattern is consistent with the physiological pattern of ocular dominance in layer IV. In kittens studied at one to two weeks of age, radioactive label formed a continuous band in layer IV on both sides of the brain. On the ipsilateral side, this appearance could not be accounted for by spillover in the LGN, but reflected a continuous, non‐columnar distribution of afferents. Physiological recordings at this age showed most cells in layer IV to be nearly equally responsive to stimulation of either eye, in contrast to the adult pattern. Periodic variations in grain density were first noted at three weeks, and a pattern similar to that of the adult was reached by about six weeks of age. On the contralateral side the uniform labelling pattern seen in the 1‐ to 2‐week‐old kittens was uninterpretable, owing to the very great spillover of radioactivity in the contralateral LGN, but the physiology suggested that the contralateral afferents, too, were uniformly distributed in layer IV. The results suggest that the earliest functional connections formed by geniculocortical afferents have a uniform, non‐columnar arrangement in layer IV, and that the formation of the adult pattern is likely to involve the breakage and reformation of synaptic connections. This process appears to be similar to that described for the monkey (Hubel et al., '77; Rakic, '76), except that the beginning of segregation is postponed until postnatal life.