Interareal coordination of columnar architectures during visual cortical development

Abstract

The formation of cortical columns is often conceptualized as a local process in which synaptic microcircuits confined to the volume of the emerging column are established and selectively refined. Many neurons, however, while wiring up locally are simultaneously building macroscopic circuits spanning widely distributed brain regions, such as different cortical areas or the two brain hemispheres. Thus, it is conceivable that interareal interactions shape the local column layout. Here we show that the columnar architectures of different areas of the cat visual cortex in fact develop in a coordinated manner, not adequately described as a local process. This is revealed by comparing the layouts of orientation columns (i) in left/right pairs of brain hemispheres and (ii) in areas V1 and V2 of individual brain hemispheres. Whereas the size of columns varied strongly within all areas considered, columns in different areas were typically closely matched in size if they were mutually connected. During development, we find that such mutually connected columns progressively become better matched in size as the late phase of the critical period unfolds. Our results suggest that one function of critical-period plasticity is to progressively coordinate the functional architectures of different cortical areas-even across hemispheres.cerebral cortex | critical period | postnatal development | visual cortex | orientation columns A general principle of cerebral cortical organization states that the neocortex is subdivided into numerous functionally and anatomically distinct areas (1, 2). In evolution, the subdivision into distinct areas arose concurrently with the invention of the neocortex in the first mammals (3), and the multiplication of functional areas appears as the central process that increases neocortical functionality in later mammalian evolution (3,4). In all mammalian brains, multiple functional areas are interconnected within a brain hemisphere, and also across hemispheres, by a dense network of intrahemispheric and callosal interareal connections (2, 5, 6). These connections constitute a large fraction of the cerebral white matter and are likely to physically shape cortical morphology during the growth of the brain (7). Although many cortical areas appear specialized for particular-information processing steps, most functions of cortical processing involve the activation of distributed processing networks that span many anatomically distinct areas. The interactions among these areas are structured such that even the most simple sensory stimuli activate large groups of neurons distributed over multiple areas in a coordinated and temporally overlapping manner (5,(8)(9)(10).Over the past two decades, the important role of distributed nerve-cell networks for sensory perception or the planning and execution of movements utilizing behavioral contextual information has been increasingly taken into account (8, 10-13). In contrast, the role of interareal networks for the developmental specification of the functional processi...

Parallel development of orientation maps and spatial frequency selectivity in cat visual cortex

“…Previous studies using 2-deoxyglucose showed that the size of isoorientation domains in area 17 was smaller than that in area 18 in cats (Lowel et al, 1987;Kaschube et al, 2009). Here, we found that the periodicity of orientation arrangements, which is inversely proportional to the iso-orientation domain size, gradually increased as the stimulus spatial frequency increased.…”

“…Previous studies using 2‐deoxyglucose showed that the size of iso‐orientation domains in area 17 was smaller than that in area 18 in cats (Lowel et al. , 1987; Kaschube et al. , 2009).…”

Universality in the Evolution of Orientation Columns in the Visual Cortex

“…These requirements are consistent with the physiological action of nonlocal influences in the visual cortex (12, 25) but hard to reconcile with the notion that pinwheels are quasi-isolated local circuit elements. The relevant genes controlling their formation are thus expected to concern the regulation of lateral axon outgrowth and the setting of overall synaptic input balance (14, 25). Genetic or experimental perturbations that restrict neuronal interactions in the visual cortex to the range of an individual hypercolumn are predicted to induce the breakdown of spatially complex orientation maps into pinwheel sparse or crystal-like patterns.…”

Can Retinal Ganglion Cell Dipoles Seed Iso-Orientation Domains in the Visual Cortex?

“…Tangential to the visual cortical layers, orientation preference changes smoothly and progressively [2] except at the centers of so-called pinwheels where neurons exhibiting the whole range of orientation preferences are located in close vicinity [2,3]. The progression of orientation preferences across the visual cortical surface (Orientation preference map, OPM) appears as organized by a semiregularly spaced system of pinwheels and adjacent columns preferring the same orientation over roughly a millimeter distance [4][5][6][7][8][9][10][11][12]. Most models for the emergence of OPMs during postnatal development assume that their layout is determined by intracortical mechanisms (e.g.…”