Electrophysiological Imaging of Functional Architecture in the Cortical Middle Temporal Visual Area ofCebus apellaMonkey

Abstract

We studied the spatial organization of directionally selective neurons in the cortical middle temporal visual area (area MT) of the Cebus monkey. We recorded neuronal activity from multielectrode arrays as they were stepped through area MT. The set of recording sites in each array penetration described a plane parallel to the cortical layers. At each recording site, we determined the preferred direction of motion. Responses recorded at successive locations from the same electrode in the array revealed gradual changes in preferred direction, along with occasional directional reversals. Comparisons of responses from adjacent electrodes at successive locations enabled electrophysiological imaging of the two-dimensional pattern of preferred directions across the cortex. Our results demonstrate a systematic organization for directionality in area MT of the New World Cebus monkey, which is similar to that known to exist in the Old World macaque. In addition, our results provide electrophysiological confirmation of map features that have been documented in other cortical areas and primate species by optical imaging. Specifically, the tangential organization of directional selectivity is characterized by slow continuous changes in directional preference, as well as lines (fractures) and points (singularities) that fragment continuous regions into patches. These electrophysiological methods also allowed a direct investigation of neuronal selectivities that give rise to map features. In particular, our results suggest that inhibitory mechanisms may be involved in the generation of fractures and singularities.

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

“…Nearly full-hemifield (40°) stimuli strongly activated most of MT, whereas stimuli restricted to smaller portions of the contralateral hemifield activated restricted areas of MT in a global retinotopic pattern. Overall, these results are remarkably similar to optical imaging results reported for MT of owl monkeys, a New World monkey (3), results that are highly consistent with data from microelectrode recording experiments in New World cebus monkeys (17) and Old World macaque monkeys (18)(19)(20)(21)(22)(23)(24). As prosimian and anthropoid (monkeys, apes, and humans) lines of primate evolution diverged Ͼ60 million years ago, and New World and Old World monkeys separated some 40 million years ago (2), the basic features of MT organization appear to have emerged at least 60 million years ago, and these features have been conserved in three major lines of primate evolution.…”

“…Our results demonstrate a systematic representation of direction of stimulus movement in MT of bush babies that is similar to that demonstrated by using optical imaging in New World owl monkeys (3) and by electrophysiological recording in New World cebus monkeys (17). In Old World macaque monkeys, directionally selective cells also are clearly organized into columns in MT (22,36).…”

Distribution of neurofilament proteins in the lateral geniculate nucleus, primary visual cortex, and area MT of adult Cebus monkeys

“…The presence of neurofilament protein has been correlated with stabilization of the axonal cytoskeleton in large neurons with high conduction velocity, an important cellular feature in detection of movement (Campbell et al, 1991;Hof and Morrison, 1995). Our data in Cebus corroborate these ideas: strong labeling is seen for SMI-32 in layers 4B and 6 in V1, layers that project directly to MT (Rosa et al, 1993), an area that presents a systematic organization for direction of motion selectivity (Zeki, 1974;Albright, 1984;Diogo et al, 2002Diogo et al, , 2003. Nonetheless, further studies are needed to clarify the role of SMI-32-ir cells in layers 2/3 of V1.…”

Distinct Functional Organizations for Processing Different Motion Signals in V1, V2, and V4 of Macaque

“…Specifically, the major direct ascending magnocellular signal inputs to MT come from spiny-stellate neurons of layer 4B and pyramidal neurons of layer 6 in V1 (Movshon and Newsome, 1996;Yabuta et al, 2001;Nassi and Callaway, 2009). The indirect stream travels via pyramidal cells in layer 4B and 6 of V1 to V2 thick stripes before arriving at MT (DeYoe and Van Essen, 1985;Shipp and Zeki, 1985;Sincich and Horton, 2005;Nassi and Callaway, 2009), where direction-selective neurons are known to cluster into columns Malonek et al, 1994;Diogo et al, 2003;Xu et al, 2004). It should be noted that V2 thick stripes also receive some parvocellular inputs from layer 2/3 of V1 (Federer et al, 2009;Sincich et al, 2010), which most likely contribute to the orientation selectivity within the thick stripes (Fig.…”