From Neural Arbors to Daisies

Abstract

Pyramidal neurons in layers 2 and 3 of the neocortex collectively form an horizontal lattice of long-range, periodic axonal projections, known as the superficial patch system. The precise pattern of projections varies between cortical areas, but the patch system has nevertheless been observed in every area of cortex in which it has been sought, in many higher mammals. Although the clustered axonal arbors of single pyramidal cells have been examined in detail, the precise rules by which these neurons collectively merge their arbors remain unknown. To discover these rules, we generated models of clustered axonal arbors following simple geometric patterns. We found that models assuming spatially aligned but independent formation of each axonal arbor do not produce patchy labeling patterns for large simulated injections into populations of generated axonal arbors. In contrast, a model that used information distributed across the cortical sheet to generate axonal projections reproduced every observed quality of cortical labeling patterns. We conclude that the patch system cannot be built during development using only information intrinsic to single neurons. Information shared across the population of patch-projecting neurons is required for the patch system to reach its adult state.

On the dynamics of cortical development: synchrony and synaptic self-organization

“…This system, composed of relatively long-range, largely excitatory (Hirsch and Gilbert, 1991; McGuire et al, 1991) patchy connections (Gilbert and Wiesel, 1979; Rockland and Lund, 1983) is ubiquitous in cortex (Muir and Douglas, 2011) and has a functional relationship to OP. Patchy connections develop before sensory afferents reach the cortex (Price, 1986; Callaway and Katz, 1990; Durack and Katz, 1996; Ruthazer and Stryker, 1996) but do not arise or terminate in the vicinity of OP singularities.…”

“…Patchy connections develop before sensory afferents reach the cortex (Price, 1986; Callaway and Katz, 1990; Durack and Katz, 1996; Ruthazer and Stryker, 1996) but do not arise or terminate in the vicinity of OP singularities. Instead, near singularities, connections are apparently diffuse and local (Sharma et al, 1995; Yousef et al, 2001; Mariño et al, 2005; Buzás et al, 2006; Muir and Douglas, 2011). Patchy connections link areas of common OP (“like-to-like”) over distances several times the diameter of a macrocolumn (Gilbert and Wiesel, 1989; Buzás et al, 2006; Muir et al, 2011), are periodic on roughly the same interval as OP, and are largely patch-reciprocal (Rockland and Lund, 1983; Angelucci et al, 2002).…”

Further Work on the Shaping of Cortical Development and Function by Synchrony and Metabolic Competition

“…We were also able to explain the emergence of superficial patch connections “like to like” (Gilbert and Wiesel, 1989; Muir et al, 2011) with patch-sparing of macrocolumn centers (Sharma et al, 1995; Muir and Douglas, 2011), and the later absence of cortical responses to stimuli of which the subject is deprived (Blakemore and Van Sluyters, 1975). …”

“…A related puzzle concerns the superficial patch system, composed of relatively long-range, largely excitatory (Hirsch and Gilbert, 1991; McGuire et al, 1991) patchy connections (Gilbert and Wiesel, 1979; Rockland and Lund, 1983), ubiquitous in cortex (Muir and Douglas, 2011) and, in V1, reciprocally connected and, at least in maps with limited resolution, linking areas of common OP (“like-to-like”) (Rockland and Lund, 1983; Angelucci et al, 2002). Work with a higher resolution method indicates that patch boutons are also distributed to cells of differing OP, as well as those with similar OP (Martin et al, 2014).…”

“…Patch cells distribute their boutons most densely to other patch cells in the patch of their cell bodies of origin, distributing other boutons to further patches with regular separation, delivering fewer boutons per patch for axons with longer ranges (Binzegger et al, 2007). They do not arise or terminate near OP singularities, and instead, near singularities connections are short, diffuse, and local (Sharma et al, 1995; Yousef et al, 2001; Mariño et al, 2005; Buzás et al, 2006; Muir and Douglas, 2011). Just as for maps of response properties, there is variation of patchy connection orderliness between cortical areas, those areas higher in the hierarchy being more disordered than V1 (Muir et al, 2011).…”