Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis)

Abstract

The intrinsic connectivity of striate cortex was investigated by injecting horseradish peroxidase (HRP) into this area in tree shrews. Such HRP injections demonstrated periodically organized, stripelike connections within area 17. These stripes occur in layers I-IIIA and consist of a small number or retrogradely filled neurons, some clearly pyramidal, together with HRP-labeled axon terminals. HRP-filled axons trunks run between labeled stripes, interconnecting adjacent and distant regions of the stripe pattern. Correlation with Golgi-stained tissue suggests that these stripes are horizontally interconnected by pyramidal neurons with long intracortical axon collaterals (followed for distances over 1 mm from the soma). The HRP-labeled strips measure about 230 micrometers in width, with a center-to-center repeat distance of 450--500 micrometers. They have been mapped over an 8 mm2 area of striate cortex and would thus seem capable of effecting lateral interactions over considerable portions of the retinotopic map. In their dimensions and overall pattern, these anatomical stripes resemble the 2-deoxyglucose (2-DG) bands resulting from visual stimulation of trees shrews with stripes of a single orientation. While the functional role of the HRP-labeled stripes is unclear, their similarities with the 2-DG pattern raise the intriguing possibility that they may be related to orientation selectivity. The striking regularity of these extensive lateral interconnections emphasizes the importance of horizontal intralaminar connections within the cortex.

Lack of Patchy Horizontal Connectivity in Primary Visual Cortex of a Mammal without Orientation Maps

“…This clustered connectivity is evident in both anterograde axonal staining (Gilbert and Wiesel, 1979;Rockland et al, 1982;Bosking et al, 1997) and retrograde labeling of cells that project to a small area of V1 (Callaway and Katz, 1990;Ruthazer and Stryker, 1996;Bosking et al, 2000). In squirrel, we found 1-2 mm horizontal connections, but there was little evidence of patchy and periodic connectivity in quantitative analyses of retrogradely labeled cells.…”

“…In many sensory and high-level cortical areas, including V1 of primates (Malach et al, 1993), carnivores (Gilbert and Wiesel, 1983), and tree shrews (Rockland et al, 1982), long-range horizontal axons ramify in periodic, patchy patterns across the cortical surface. This clustered connectivity is evident in both anterograde axonal staining (Gilbert and Wiesel, 1979;Rockland et al, 1982;Bosking et al, 1997) and retrograde labeling of cells that project to a small area of V1 (Callaway and Katz, 1990;Ruthazer and Stryker, 1996;Bosking et al, 2000).…”

Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

“…We focused our analyses on the basal dendritic trees of supragranular pyramidal cells for several reasons. Of particular interest to us are horizontally projecting intrinsic axonal patches that arise from these cells and project to the basal dendritic trees of neighboring pyramidal cells (Gilbert and Wiesel, 1979, 1983; Rockland and Lund, 1982, 1983; Rockland et al, 1982; Livingstone and Hubel, 1984; Martin and Whitteridge, 1984; Rockland, 1985; Kisvárday et al, 1986; McGuire et al, 1991; Fujita and Fujita, 1996). As many as 80–95% of the horizontal projection synapses of individual supragranular pyramidal cells are formed with other nearby supragranular pyramidal cells (Kisvárday et al, 1986; McGuire et al, 1991) in reciprocally connected patches (Kisvárday and Eysel, 1992).…”

How Does Connectivity Between Cortical Areas Depend on Brain Size? Implications for Efficient Computation

“…µm (Rumberger et al 2001), for tree shrew ξ = 230 µm (Rockland et al 1982), for cat ξ = 300 µm (Luhmann et al 1986), for macaque ξ = 230 µm (Amir et al 1993), for human ξ = 400 µm (Burkhalter and Bernardo 1989). The gray matter volumes were taken form Stephan et al, 1981.…”