Very-long-range disynaptic V1 connections through layer 6 pyramidal neurons revealed by transneuronal tracing with rabies virus

Abstract

Neurons in primary visual cortex (V1) integrate across the representation of the visual field through networks of long-range projecting pyramidal neurons. These projections, which originate from within V1 and through feedback from higher visual areas, are likely to play a key role in such visual processes as low contrast facilitation and extraclassical surround suppression. The extent of the visual field representation covered by feedback is generally much larger than that covered through monosynaptic horizontal connections within V1, and, although it may be possible that multisynaptic horizontal connections across V1 could also lead to more widespread spatial integration, nothing is known regarding such circuits. In this study, we used injections of the CVS-11 strain of rabies virus to examine disynaptic long-range horizontal connections within macaque monkey V1. Injections were made around the representation of 5° eccentricity in the lower visual field. Along the opercular surface of V1, we found that the majority of connected neurons extended up to 8 mm in most layers, consistent with twice the typically reported distances of monosynaptic connections. In addition, mainly in layer 6, a steady presence of connected neurons within V1 was observed up to 16 mm away. A relatively high percentage of these connected neurons had large-diameter somata characteristic of Meynert cells, which are known to project as far as 8 mm individually. Several neurons, predominantly in layer 6, were also found deep within the calcarine sulcus, reaching as far as 20° of eccentricity, based on estimates, and extending well into the upper visual field representation. Thus, our anatomical results provide evidence for a wide-ranging disynaptic circuit within V1, mediated largely through layer 6, that accounts for integration across a large region of the visual field.

In Vivo Identification of Thick, Thin, and Pale Stripes of Macaque Area V2 Using Submillimeter Resolution (f)MRI at 3 T

“…2). This border was located along the posterior lip of the LS, and matches the reported anatomical location of the V1/ V2d border (Gattass et al 1981;Roe and Ts'o 1997;Lyon et al 2014). The retinotopic definition of the rostral border of V2d is less straightforward in macaque monkeys, since a noncontinuous retinotopic organization has been reported immediately Monkey V2 Stripes Identified With (f)MRI Li et al | 549 rostral to V2d (Gattass et al 1988).…”

Plasticity in the Structure of Visual Space

“…The separations between testing locations were 0, 0.4, or 0.8 degrees larger than the separations between training locations. These visual field separations correspond to a cortical separation of 10–14 mm in human V1 ( Schira et al, 2007 ) and overlap with the reported extent of lateral connections in primate visual cortex ( Ringo, 1991 ; Burkhalter et al, 1993 ; Kaas, 2000 ; Levitt and Lund, 2002 ; Voges, et al, 2010 ; Ahmed et al, 2012 ; Lyon et al, 2014 ). Moreover, at an eccentricity of 6 degrees, the number of neurons activated by a point stimulus (cortical point image) should be minimal ( Van Essen et al, 1984 ; Harvey and Dumoulin, 2011 ), thereby favoring the activation of distinct groups of neurons.…”

“…After training, we observed a significant contraction in the perceived distance between the training locations, with the degree of contraction dependent on the training separation (repeated-measures ANOVA; effect of training on perceived distance: F (1,29) = 41.473, p < 10 −6 ; quadratic trend in interaction between training effect and training separation: F (1,29) = 7.632, p = 0.010. The contraction was maximal at a training separation of 4.4 degrees, which corresponds to a cortical separation of 12 mm in human V1 ( Schira et al, 2007 ) and falls within the extent of V1 lateral connections ( Ringo, 1991 ; Burkhalter et al, 1993 ; Kaas, 2000 ; Levitt and Lund, 2002 ; Voges, et al, 2010 ; Ahmed et al, 2012 ; Lyon et al, 2014 ). Because of the mirror-symmetry of human retinotopic organization, V1 is the only early visual cortical region whose ventral part (representation of upper visual field) and dorsal part (representation of lower visual field) are contiguous, whereas the ventral and dorsal parts of other early visual cortical regions (e.g., V2, V3) are segregated by V1 ( Sereno et al, 1995 ; Brewer and Barton, 2012 ; Wang et al, 2014 ).…”

Laminar multi-contrast fMRI at 7T allows differentiation of neuronal excitation and inhibition underlying positive and negative BOLD responses

“…The blue line represents the horizontal connections between different regions in V1. Previous research has shown that the deeper layers (layer 6) have stronger and more extensive horizontal connections (Liu et al, 2014; Srivastava et al, 2022). The green line and pink line respectively represent our two hypotheses for the negative signal of fovea.…”