Optical imaging reveals retinotopic organization of dorsal V3 in New World owl monkeys

Abstract

Optical imaging of intrinsic responses to visual stimuli in extrastriate cortex of owl monkeys provided evidence for the dorsal half of the third visual area, V3. Visual stimuli were used to selectively activate locations in dorsolateral V2 and the rostrally adjoining presumptive V3. Consistent with the proposed retinotopies of dorsal V2 and dorsal V3, small bars of drifting gratings along the horizontal meridian of the contralateral hemifield activated cortex along the V2͞V3 border, whereas such stimuli along the vertical meridian activated cortex along the rostral border of V3. Stimuli in limited locations in the lower visual quadrant revealed mirror reversals of retinotopy in dorsal V2 and V3, whereas stimuli in the upper visual quadrant failed to activate either region. Brain sections processed for cytochrome oxidase from the same cases provided architectonic borders of V2 that matched those indicated by the optical imaging. The results support the concept that a narrow dorsal V3 exists in monkeys. V3d borders dorsal V2 and contains a smaller, mirror-image representation of the lower visual quadrant.T he visual cortex of monkeys and other primates is widely recognized as containing a number of visual areas, each specialized to contribute uniquely to visual function (see refs. 1-3 for review). However, of the several dozen visual areas proposed to exist in monkeys, only three areas, the first and second areas, V1 and V2, and the middle temporal area (MT, V5), are well established as valid subdivisions with known architectonic characteristics, retinotopy, types of modular organization, response characteristics to visual stimuli, and patterns of connections (see ref.3). Recently we provided architectonic and connectional evidence for the existence of a third visual area, V3 (see Fig. 1a), in prosimian primates (4), New World monkeys (5, 6), and Old World macaque monkeys (7). Although Zeki (8) and Cragg (9) long ago provided connectional evidence for V3 in macaque monkeys, and evidence from microelectrode mapping experiments accumulated for macaques (10, 11) and large New World cebus monkeys (12, 13), that evidence has been open to other interpretations (e.g., see Fig. 1b; see refs. 3 and 7 for review).The goal of the present study was to address the issue of the validity of V3 with another method of revealing the organization of visual cortex, the use of optical imaging of intrinsic cortical signals evoked by stimuli in different locations in the visual field. In a manner similar to that of functional MRI in humans (e.g., refs. 14-17), optical imaging has the potential of revealing global patterns of retinotopic organization of extrastriate cortex of monkeys. Optical imaging has been used recently to study features of retinotopic organization of V1 in several species of mammals (18-21), but this method has not been widely applied to extrastriate cortex yet. In the present study, we explored the retinotopy of the presumptive dorsal V3 region in owl monkeys using optical images of intrinsic signals. This study wa...

Optical imaging of visually evoked responses in prosimian primates reveals conserved features of the middle temporal visual area

“…) monkeys, microelectrode recordings from both New World and Old World monkeys have previously demonstrated that a majority of neurons in MT are well tuned for orientation (19)(20)22), although this is not widely recognized. Our data in bush babies also demonstrate that regions surrounding MT, including both the MT crescent and medial superior temporal area, contain cells selective for orientation as reported by others in owl monkeys and macaque monkeys (4,34,35).…”

“…The three bush babies (greater galagos, now referred to as O. garnetti) used in this study were handled according to an approved protocol from the Vanderbilt University Animal Care and Use Committee. Basic procedures have been described (4). Briefly, bush babies were initially anesthetized with isoflurane (2-4% in O 2 ), and paralysis was induced by i.v.…”

The case for a dorsal V3 in the ‘third-tier’ of primate visual cortex: a reply to ‘the case for a dorsomedial area in the primate ‘third-tier’ visual cortex’

“…1 in their commentary), are not found using intrinsic signal imaging. Rather, imaging shows a clear lower field only representation along the outer V2 border with a single horizontal meridian (along the outer border of V2) and a single foveal representation, all consistent with a V3d [9] (for more details, see figs 3 and 4 in the original review [1]). …”

Pulvinar contributions to the dorsal and ventral streams of visual processing in primates

“…In early studies from our laboratory, we did not recognize V3 and included the territory of V3 in other visual areas (see Kaas and Lyon, 2001). However, now we feel that the issue is largely resolved (Lyon, 2007), as a series of anatomical studies provided strong evidence for V3 (including ventral and dorsal halves) in prosimian galagos (Lyon and Kaas, 2002a) four species of New World monkeys 2002b;Lyon, et al, 2002) and Old World macaque monkeys (Lyon and Kaas, 2002c). V1 and V2 both have connections that associate them with both the dorsal and ventral visual streams, but more of their outputs are directed into the ventral stream (Kaas, 2004a).…”