Topography and extent of visual-field representation in the superior colliculus of the megachiropteran Pteropus

Abstract

It has been proposed that flying foxes (genus Pteropus) have a primate-like pattern of representation in the superficial layers of the superior colliculus (SC), whereby the visual representation in this structure is limited by the same decussation line that limits the retino-geniculo-cortical projection (Pettigrew, 1986). To test this hypothesis, visual receptive fields were plotted based on single- and multi-unit recordings in the SC of ten flying foxes. A complete representation of the contralateral hemifield was observed in the SC. Although the binocular hemifield of vision in Pteropus is 54 deg wide, receptive-field centers invaded the ipsilateral hemifield by only 8 deg, and the receptive-field borders by 13 deg. This invasion is similar to that observed at the border between visual areas V1 and V2 in the occipital cortex. The extent of the ipsilateral invasion was not affected by a lesion that completely ablated the occipital visual areas, thus suggesting that this invasion may be consequence of a zone of nasotemporal overlap in the retinal projections to the two colliculi. Neurones located in the superficial layers typically responded briskly to stimulation of both eyes, with a bias towards the contralateral eye. After cortical lesions the neuronal responses to the ipsilateral eye were depressed, and the ocular-dominance histograms shifted towards an even stronger dominance by the contralateral eye. However, cells located in the rostral pole of the SC remained responsive to the ipsilateral eye after cortical lesions. Responses in the stratum opticum and stratum griseum intermediale were more severely affected by cortical lesions than those in the stratum griseum superficiale. Our results demonstrate that the SC in flying foxes retain some generalized mammalian characteristics, such as the stronger direct projections of the contralateral eye and the location of the upper, lower, central, and peripheral representations in the SC. Nonetheless, the extent of visual representation in the SC demonstrates a specialized, primate-like pattern. These observations are consistent with the hypothesis that megachiropterans are members of a group that branched off early during the differentiation of primates from basal mammals.