Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex

Abstract

The laminar location of the cell bodies and terminals of interareal connections determines the hierarchical structural organization of the cortex and has been intensively studied. However, we still have only a rudimentary understanding of the connectional principles of feedforward (FF) and feedback (FB) pathways. Quantitative analysis of retrograde tracers was used to extend the notion that the laminar distribution of neurons interconnecting visual areas provides an index of hierarchical distance (percentage of supragranular labeled neurons [SLN]). We show that: 1) SLN values constrain models of cortical hierarchy, revealing previously unsuspected areal relations; 2) SLN reflects the operation of a combinatorial distance rule acting differentially on sets of connections between areas; 3) Supragranular layers contain highly segregated bottom-up and top-down streams, both of which exhibit point-to-point connectivity. This contrasts with the infragranular layers, which contain diffuse bottom-up and top-down streams; 4) Cell filling of the parent neurons of FF and FB pathways provides further evidence of compartmentalization; 5) FF pathways have higher weights, cross fewer hierarchical levels, and are less numerous than FB pathways. Taken together, the present results suggest that cortical hierarchies are built from supra- and infragranular counterstreams. This compartmentalized dual counterstream organization allows point-to-point connectivity in both bottom-up and top-down directions.

Visual areas exert feedforward and feedback influences through distinct frequency channels

“…The spectrum of GC influences of site 1 onto site 2 quantifies, per frequency, the variance in site 2 that is not explained by the past of site 2, but by the past of site 1. For our example pair of areas, the influence of V1 onto DP is a feedforward influence 4 and it exceeded the feedback influence in the theta and gamma bands, while the feedback predominated in the beta band (Fig. 1c).…”

“…These asymmetries have been used to arrange the visual cortical areas into a hierarchy 1,4 , which has influenced many theories of cognition and brain function 5,6 .…”

“…In addition, it is well established that feedforward and feedback connections follow a characteristic pattern with regard to cortical layers: Feedforward connections target the granular layer 1 ; they originate preferentially in supragranular layers, and this preference is stronger for projections traversing more hierarchical levels, i.e. it is quantitatively related to the hierarchical distance 4 .…”

“…Feedback connections avoid targeting the granular layer 1 ; they originate preferentially in the infragranular layers, and again, this preference is stronger for projections traversing more hierarchical levels and is thereby quantitatively related to hierarchical distance 4 . These asymmetries have been used to arrange the visual cortical areas into a hierarchy 1,4 , which has influenced many theories of cognition and brain function 5,6 .…”

“…When retrograde tracer is injected into a target area, the target-projecting neurons are labelled in different source areas. If a source area is providing feedforward (feedback) input to the target area, the proportion of supragranular labelled neurons (relative to supragranular plus infragranular labelled neurons) is high (low) 4 . This SLN metric quantifies the degree to which an inter-areal anatomical connection is feedforward or feedback (Fig.…”