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

Abstract

We describe a model for cortical development that resolves long-standing difficulties of earlier models. It is proposed that, during embryonic development, synchronous firing of neurons and their competition for limited metabolic resources leads to selection of an array of neurons with ultra-small-world characteristics. Consequently, in the visual cortex, macrocolumns linked by superficial patchy connections emerge in anatomically realistic patterns, with an ante-natal arrangement which projects signals from the surrounding cortex onto each macrocolumn in a form analogous to the projection of a Euclidean plane onto a Möbius strip. This configuration reproduces typical cortical response maps, and simulations of signal flow explain cortical responses to moving lines as functions of stimulus velocity, length, and orientation. With the introduction of direct visual inputs, under the operation of Hebbian learning, development of mature selective response "tuning" to stimuli of given orientation, spatial frequency, and temporal frequency would then take place, overwriting the earlier ante-natal configuration. The model is provisionally extended to hierarchical interactions of the visual cortex with higher centers, and a general principle for cortical processing of spatio-temporal images is sketched.

Keywords: cortical development; cortical information flow; cortical response properties; synaptic organization; synchronous oscillation.

Figure 1

Simulated electrocortical activity in the excited cortex, from Wright (2010). (A) Power spectrum of a local field potential time-series, shown in (B). (C) and (D) Cell firing correlations, vs. time-lag. Dashed line—cells remote from each other. Solid lines—cells adjacent to each other. (C) Between excitatory cells. (D) Between excitatory and inhibitory cells.

Figure 2

Simulated background electrocortical activity, in conditions of low cortical excitation. Graphical format is the same as in Figure 1.

Figure 3

Simulated and real maps of orientation preference in V1, from Wright et al. (2006). Top: Simulation. Colors of the spectrum, from red to violet, represent average OP of V1 neurons for slow-moving visual lines of orientation 0 − π. Adjacent macrocolumns, of diameter ~300 μm are set within a hexagonal frame (the patch system) with OP forming color wheels about OP singularities. Orientations and chiralities of the color wheels are arranged to approach a minimum total of angular disparity from mirror reflection of OP between each macrocolumn and its neighbors. Bottom: Real OP. Visualized in the tree shrew by Bosking et al. (1997). Superficial patchy connections are demarcated in black by a selective stain. Scale of macrocolumns is approximate to that of the simulation.

Figure 4

Equilibrium distribution of synaptic activity, and the impact of visual inputs disrupting equilibrium from Wright and Bourke (2013). Top: equilibrium disposition of saturated and sensitive synapses. Black circles represent cell bodies and dendrites. Synapses are indicated as saturated (solid) or sensitive (dashed) terminations of axons. Reciprocal connections between α-patches (patchy connections) form the hexagonal array. (Other connections, although shown as unidirectional, are also reciprocal.) A representative pair of connections from α-cells to the β-patch is displayed in the upper-and lower-aspects of the figure. At the center of the figure, saturated and sensitive synapses show the network's analogy to a Möbius-strip within a β-patch (macrocolumn). To the right, representative links from the central macrocolumn to cells at homologous positions in neighboring macrocolumns. Bottom: exposed to strong transient signals conveyed over the superficial patch system, summing with direct visual inputs conveyed to the cRF, the equilibrium configuration breaks down. The green bar represents the field of excitation of cells by the contextual signals, within which cells also directly excited in the cRF, fire at high rates.

Figure 5

Top: Simulation of OD columns in accord with Wright and Bourke (2008). Bottom: Real OD columns, visualized by Obermayer and Blasdel (1993). Color coding of OP and scale as for Figure 3. Black lines demarcate alternation of OD between columns. Fine black lines in the lower figure trace the way OP is aligned so it matches orthogonally across OD column boundary.

Figure 6

The effect of increasing stimulus speed on apparent OP, for a bar of length 6 units, oriented at 45° to its direction of motion, and traveling left to right. Examples shown are freeze-frames, from separate simulation movies, at similar positions in the visual stimulus' transit across the macrocolumn. From left to right, in each example, the bar speed/wave speed is 0.1, 0.5, 1.0, 1.5, respectively.

Figure 7

Change in apparent OP, and standard error of the estimate, as a function of bar speed to wave speed, for lines at different orientations to their directions of motion. Bar length 6 units.

Figure 8

Projection of a complex object (a double bar) from V1 (bottom) to a large macrocolumn in, e.g., V2 (top). Brightened dots show the intersections of lines, producing more frequent enhanced responses to stimulus angles in V2 than V1.