Orderly anomalous retinal projections to the medial geniculate, ventrobasal, and lateral posterior nuclei of the hamster

Abstract Experiments were performed to determine (1) under what conditions early brain surgery can cause sensory afferents to the thalamus to form connections at abnormal thalamic sites and (2) the extent to which such ectopic projections are receptotopically organized. In newborn Syrian hamsters, two of the retina's principal synaptic targets, the superior colliculus and dorsal lateral geniculate nucleus, were destroyed, respectively, by a direct lesion and by retrograde degeneration following a lesion of the occipital cortex. In the same brains, alternative terminal space for the retinofugal axons was made available in auditory (medial geniculate) or somatosensory (ventrobasal) thalamic nuclei by lesions of ascending auditory or somatosensory pathways, respectively; additional terminal space was made in the lateral posterior nucleus by degeneration of afferents from the superior colliculus. The projections of the contralateral retina were traced in neonatally operated adults by making one or two small peripheral retinal lesions and intraocular injections of 3 H‐proline 5 days and 1 day, respectively, prior to sacrifice. The neonatal surgery reliably produced anomalous crossed retinal projections to the partially deafferented structures. These projections terminate preferentially at the nuclear surfaces. Computer reconstructions from serial sections demonstrated several signs of spatial order suggestive of receptotopic organization in the anomalous retinothalamic projections. In order of increasing stringency, these signs (which are not mutually exclusive) are: (1) In each nucleus, a restricted retinal sector gives rise to a limited part of the abnormal projection. (2) In each nucleus, different parts of the retina give rise to different parts of the anomalous projection. (3) In each nucleus, there is a more or less consistent polarity of the anomalous connection. Each small retinal sector appears to be represented along a “line of projection” in each of its abnormal thalamic targets, as it normally is in the dorsal and ventral lateral geniculate nuclei and in the superior colliculus. In some brains, some of the abnormal projections produce only a partial representation of the retina. However, in a single animal, a retinal sector not represented in the anomalous projections to one nucleus can contribute to the abnormal connections with another nucleus. In additional experiments, an attempt was made to direct developing auditory and somatosensory fibers normally terminating in the medial geniculate and ventrobasal nuclei, respectively, to anomalous thalamic targets. The axons were deprived of some of their normal thalamic sites of termination and alternative terminal space was made available in another thalamic sensory nucleus. These experiments failed to produce reliable evidence of ectopic auditory or somatosensory thalamic projections. The anomalous retinal projections to nuclei that normally recieve little (lateral posterior) or no (medial geniculate, ventrobasal) optic tract input, show that the preference of retinal axons for their normal targets is relative, not absolute. The orderliness of the ectopic projections opposes the hypothesis that the formation of retinotopic connections depends upon the matching of a set of signals distributed among the retinofugal fibers and a corresponding set of cues unique to the normal terminal fields of optic axons. The results are consistent with the formation of receptotopic connections by interactions among developing axons and suggest the action of additional factors that determine the terminal sites and organization of central neuronal connections.