Area-specific laminar distribution of cortical feedback neurons projecting to cat area 17: Quantitative analysis in the adult and during ontogeny

Abstract

Corticocortical pathways can be classified as feedback and feedforward, in part according to the laminar distribution of the parent cell bodies. Here, we have developed exhaustive sampling procedures to determine unambiguously this laminar distribution. This shows that individual extrastriate areas in the adult cat have highly stereotyped proportions of supragranular layer neurons with respect to the total population of neurons back-projecting to area 17. During development, these adult laminar patterns emerge from an initially uniform radial distribution through a process of selective reorganization, which is highly specific to each area. Injections of fluorescent retrograde tracers were made in area 17. In areas 19, 20, posteromedial lateral suprasylvian area, and anteromedial lateral suprasylvian area, we defined a projection zone as the region containing retrogradely labeled neurons. In the neonate, counts of labeled neurons throughout the projection zones show constant percentages of 40% in the supragranular layers. During development, there is an area-specific reduction in the percentage of supragranular labeled neurons generating the laminar distributions characteristic of each area. Numbers of labeled neurons were estimated at different eccentricities of the projection zone. This finding indicates that during development there is a relative decrease in the numbers of labeled neurons of the periphery of the projection zone in the supragranular layers but not in the infragranular layers. This decrease is accompanied by a relative decrease in the dimensions of the supragranular projection zone with respect to the infragranular projection zone. These findings suggest that each extrastriate area precisely adjusts the proportions of supragranular layer neurons back-projecting to striate cortex in part by developmental changes in the divergence-convergence values of individual neurons. This shaping of corticocortical connectivity occurs relatively late in postnatal development and could, therefore, be under epigenetic control.

Neuronal Circuits of the Neocortex

“…The distance rule governing the hierarchical relationships of cortical areas may well be an organizing principle of monkey neocortex. Evidence supporting this view comes from the laminar organization of afferents in the frontal lobe (Barbas 1986) and the somatosensory cortex (Batardiere et al 1998). These results have potentially important consequences for how we view the influence and role of the inter-areal connections to the local cortical circuits.…”

Multisensory anatomical pathways

“…However, the non-visual projections to the peripheral V1 can be as large as the projection arising from the motion visual area MT/V5 (Falchier et al, 2002), which is known to exert an influential impact on V1 responses (Hupé et al, 1998). In addition, all of these heteromodal connections do not consist in scattered projecting neurons, but rather have a topological organization (Batardiere et al, 1998) with a relatively compact projection zones probably linked to cortical functional modules. For example, in the cat, the auditory projection from area PAF is organized with respect to the retinotopic organization of the primary visual cortex (Hall and Lomber, 2008).…”

Projection from Visual Areas V2 and Prostriata to Caudal Auditory Cortex in the Monkey

“…The present study shows that the reciprocal projections from visual areas to auditory cortex arise from mainly infragranular cells. Although anterograde tracer experiments are still lacking to confirm the features of this projection, this pattern of retrograde labeling is consistent with a feedback laminar organization (Rockland and Pandya 1979;Maunsell and Van Essen 1983;Kennedy and Bullier 1985;Weller and Kaas 1985;Barbas 1986;Boussaoud et al 1990;Felleman and Van Essen 1991;Distler et al 1993;Batardiere et al 1998;Grant and Hilgetag 2005). Projections from early visual and other sensory modalities to auditory cortex were found to be organized similarly in the gerbil (Budinger et al 2008).…”