Four Projection Streams from Primate V1 to the Cytochrome Oxidase Stripes of V2

Abstract

In the primate visual system, areas V1 and V2 distribute information they receive from the retina to all higher cortical areas, sorting this information into dorsal and ventral streams. Therefore, knowledge of the organization of projections between V1 and V2 is crucial to understand how the cortex processes visual information. In primates, parallel output pathways from V1 project to distinct V2 stripes. The traditional tripartite division of V1-to-V2 projections was recently replaced by a bipartite scheme, in which thin stripes receive V1 inputs from blob columns, and thick and pale stripes receive common input from interblob columns. Here, we demonstrate that thick and pale stripes, instead, receive spatially segregated V1 inputs and that the interblob is partitioned into two compartments: the middle of the interblob projecting to pale stripes and the blob/interblob border region projecting to thick stripes. Double-labeling experiments further demonstrate that V1 cells project to either thick or pale stripes, but rarely to both. We also find laminar specialization of V1 outputs, with layer 4B contributing projections mainly to thick stripes, and no projections to one set of pale stripes. These laminar differences suggest different contribution of magno, parvo, and konio inputs to each V1 output pathway. These results provide a new foundation for parallel processing models of the visual system by demonstrating four V1-to-V2 pathways: blob columns-to-thin stripes, blob/interblob border columns-to-thick stripes, interblob columns-to-pale lateral stripes, layer 2/3-4A interblobs-to-pale medial stripes.

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

“…In a flattened section of V2 taken from a representative example of macaques (Fig. 3A), the cycle of three different CO compartments-the pale, thick and thin stripes-was clearly revealed, as previously reported (Horton and Hubel, 1981;Livingstone and Hubel, 1983;Tootell et al, 1983;DeYoe and Van Essen, 1985;Shipp and Zeki, 1985;Levitt et al, 1994b;Malach et al, 1994;Xiao and Felleman, 2004;Sincich and Horton, 2005;Federer et al, 2009;Lim et al, 2009). We spatially aligned the functional domains mapped with optical imaging for different visual features with those CO-stained stripes in V2 after reconstruction of lesions.…”

“…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. 9).…”

Parallel feedback pathways in visual cortex of cats revealed through a modified rabies virus

“…For primate, an extensive body of evidence suggests that V2 projects to both the dorsal and the ventral streams but from separate, architectonically defined compartments (CO stripes; Shipp and Zeki, 1985;Sincich and Horton, 2005;Federer et al, 2009;Nassi and Callaway, 2009). Therefore, based on the evidence reported here, it would seem that cat area 18 and primate V2 play very different roles in the two species' dorsal/ventral pathways.…”

“…Such studies provide considerable support for the idea that these two streams are segregated and relay in parallel through early primate cortical areas V1-V3 and onward to distinct higher order areas of both processing streams (Shipp and Zeki, 1985;Merigan and Maunsell, 1993;Sincich and Horton, 2005;Federer et al, 2009;Nassi and Callaway, 2009). However, for primate V3, differing functional and connectional results have been used to argue for more involvement in either the dorsal (Burkhalter et al, 1986;Felleman and Van Essen, 1987;Nassi and Callaway, 2006;Lyon et al, 2010) or the ventral Rosa and Tweedale, 2000;Rosa and Manger, 2005) stream.…”

Representation of the visual field in the primary visual area of the marmoset monkey: Magnification factors, point‐image size, and proportionality to retinal ganglion cell density

“…The marmoset is one of the smallest living primates, with a brain that is less than 1/12 the volume of a macaque brain, and 1/180 the volume of the human brain (Stephan et al, 1981). There have been many studies of the organization of the visual system in the marmoset, including the retina (e.g., Troilo et al, 1993;Goodchild et al, 1996;Wilder et al, 1996;Silveira et al, 1999;Chan et al, 2001;Szmajda et al, 2005Szmajda et al, , 2008Springer et al, 2011), lateral geniculate nucleus (LGN, e.g., Spatz, 1978;Fritschy and Garey, 1986;Yeh et al, 1995;Kremers and Weiss, 1997;Martin et al, 1997;White et al, 1998White et al, , 2001Felisberti and Derrington, 2001;Solomon et al, 2002Solomon et al, , 2010Webb et al., 2002), V1 (e.g., Fritsches and Rosa, 1996;Bourne et al, 2002;Zinke et al, 2006;Buzas et al, 2008;, and extrastriate cortex (e.g., Krubitzer and Kaas, 1990;Rosa et al, 1997aRosa et al, ,b, 2000Rosa et al, , 2005Rosa et al, , 2009Schiessl, 2006, 2009;Lui et al, 2006Lui et al, , 2007aFederer et al, 2009;Jeffs et al, 2009Jeffs et al, , 2012Solomon et al, 2011). The present results build on earlier reports of the global visuotopy (Fritsches and Rosa, 1996) and local precision (McLoughlin...…”