Topographic organisation of extrastriate areas in the flying fox: implications for the evolution of mammalian visual cortex.

The organisation of extrastriate cortex was studied in anaesthetised flying foxes (Pteropus poliocephalus) by using multiunit recording techniques. Based on the visuotopic organisation and response characteristics, the cortex immediately rostral to the second visual area (V2) was subdivided into two fields: visual area 3 (V3) laterally and the occipitoparietal area (OP) medially. Area V3 is a 1.0-1.5 mm wide strip of cortex that represents the entire contralateral hemifield as a mirror image of the representation found in V2. The representation of the vertical meridian and the area centralis form the rostral border of V3. In area OP, receptive fields are much larger than those of V3 and form a separate visuotopic map, with the upper quadrant represented rostral to the lower quadrant. Multiunit clusters in the cortex rostral to area OP (posterior parietal area) respond to both visual and somatosensory stimuli. Farther laterally, in the cortex rostral to V3, the occipitotemporal area (OT) was found to form yet another map of the visual field. Similar to the middle temporal area in primates, area OT in the flying fox forms a first-order representation of the visual field, with the lower quadrant represented medially, the upper quadrant represented laterally, the area centralis represented caudally, and the visual field periphery represented rostrally. The cortex surrounding area OT rostrally and ventrally is also visually responsive but could not be subdivided due to the large receptive fields. Finally, visual responses were elicited from an area adjacent to the peripheral representation in the first visual area (V1) in the splenial sulcus. These results demonstrate that nearly half of the flying fox cortex is related to vision, which contrasts with that of microchiropteran bats, in which auditory areas predominate. A comparison of the flying fox with other mammals suggests that several areas, including homologues of V1, V2, V3, OT, and the splenial area, may have originated early in mammalian evolution and have been inherited by most present-day eutherians. However, studies in other species will be needed to distinguish patterns of common ancestry from parallel evolution. Copyright 1999 Wiley-Liss, Inc.