Local Circuits of V1 Layer 4B Neurons Projecting to V2 Thick Stripes Define Distinct Cell Classes and Avoid Cytochrome Oxidase Blobs

Abstract

Decades of anatomical studies on the primate primary visual cortex (V1) have led to a detailed diagram of V1 intrinsic circuitry, but this diagram lacks information about the output targets of V1 cells. Understanding how V1 local processing relates to downstream processing requires identification of neuronal populations defined by their output targets. In primates, V1 layers (L)2/3 and 4B send segregated projections to distinct cytochrome oxidase (CO) stripes in area V2: neurons in CO blob columns project to thin stripes while neurons outside blob columns project to thick and pale stripes, suggesting functional specialization of V1-to-V2 CO streams. However, the conventional diagram of V1 shows all L4B neurons, regardless of their soma location in blob or interblob columns, as projecting selectively to CO blobs in L2/3, suggesting convergence of blob/interblob information in L2/3 blobs and, possibly, some V2 stripes. However, it is unclear whether all L4B projection neurons show similar local circuitries. Using viral-mediated circuit tracing, we have identified the local circuits of L4B neurons projecting to V2 thick stripes in macaque. Consistent with previous studies, we found the somata of this L4B subpopulation to reside predominantly outside blob columns; however, unlike previous descriptions of local L4B circuits, these cells consistently projected outside CO blob columns in all layers. Thus, the local circuits of these L4B output neurons, just like their extrinsic projections to V2, preserve CO streams. Moreover, the intra-V1 laminar patterns of axonal projections identify two distinct neuron classes within this L4B subpopulation, including a rare novel neuron type, suggestive of two functionally specialized output channels.

Functionally specific optogenetic modulation in primate visual cortex

“…In primates, visual perception is mediated by brain circuits composed of nodes linked together in specific networks ( 1 , 2 ). As revealed by anatomical tracing ( 3 – 10 ) and neuronal cross-correlation ( 11 – 14 ) studies, the anatomical substrates for processing of different features are mediated by connections between functionally specific cortical nodes (also termed columns, domains, and patches). In macaque monkey primary visual cortex (V1), ocular dominance (OD) columns (eye-specific nodes, ∼400 µm) tend to link to same-eye OD columns ( 3 , 5 ), and orientation columns (orientation-specific nodes, ∼200 µm) tend to link to other columns of similar orientation preference ( 1 – 3 , 6 , 7 ).…”

Functional interactions among neurons within single columns of macaque V1

“…A wealth of evidence indicates that layer 2/3 neurons provide a major source of output to other neocortical areas (reviewed in Callaway, 1998 ; Douglas and Martin, 2004 ; Felleman and Van Essen, 1991 ; Harris and Shepherd, 2015 ; Thomson and Lamy, 2007 ). In macaque V1, layer 2/3 neurons send projections to higher visual areas such as V2 ( Livingstone and Hubel, 1984 ; Rockland, 1992 ; Sincich and Horton, 2005 ) and V4 ( Yukie and Iwai, 1985 ), and receive inputs from all the deeper cortical layers, including layers 4cα, 4cβ, 4A, 4B, 5, and 6 ( Blasdel et al, 1985 ; Callaway, 1998 ; Callaway and Wiser, 1996 ; Fitzpatrick et al, 1985 ; Kisvarday et al, 1989 ; Lachica et al, 1992 ; Lund and Boothe, 1975 ; Sawatari and Callaway, 2000 ; Vanni et al, 2020 ; Wiser and Callaway, 1996 ; Yarch et al, 2017 ; Yoshioka et al, 1994 ; Figure 7a ). Consequently, one might predict that a predominant proportion of projections to 2/3 neurons from other layers might be forward ones ( Callaway, 1998 ; Mejias et al, 2016 ; Schmidt et al, 2018 ).…”

Functional Connections Among Neurons within Single Columns of Macaque V1

“…A wealth of evidence indicates that layer 2/3 neurons provide a major source of output to other neocortical areas (reviewed in Callaway, 1998; Douglas & Martin, 2004; Felleman & Van Essen, 1991; Harris & Shepherd, 2015; Thomson & Lamy, 2007)). In macaque V1, layer 2/3 neurons send projections to higher visual areas such as V2 (Livingstone & Hubel, 1984; Rockland, 1992; Sincich & Horton, 2005) and V4 (Yukie & Iwai, 1985), and receive inputs from all the deeper cortical layers, including layer 4C, 4C β , 4A, 4B, 5 and 6 (Blasdel, Lund, & Fitzpatrick, 1985; Callaway, 1998; Callaway & Wiser, 1996; Fitzpatrick, Lund, & Blasdel, 1985; Kisvarday, Cowey, Smith, & Somogyi, 1989; Lachica, Beck, & Casagrande, 1992; Jennifer S Lund & Boothe, 1975; Sawatari & Callaway, 2000; Vanni, Hokkanen, Werner, & Angelucci, 2020; Wiser & Callaway, 1996; Yarch, Federer, & Angelucci, 2017; Yoshioka, Levitt, & Lund, 1994) (Fig. 7a).…”