Precision Estimates of Macroscale Network Organization in the Human and Their Relation to Anatomical Connectivity in the Marmoset Monkey

Abstract

Precision estimates of network organization from functional connectivity MRI in the human and tract-tracing data in the marmoset monkey converge to reveal an orderly macroscale gradient of sequential networks across the cerebral cortex. Parallel networks begin with a sequence of multiple nested sensory-motor networks in both species progressing to more distributed association networks in rostral prefrontal and temporal association zones, which are expanded and differentiated in the human. From this perspective, the spatially-distributed motif encountered in association networks appears to be on a continuum with primary sensory-motor networks. Network motifs supporting sophisticated forms of human cognition may arise from specializations of distributed anatomical networks formed in an ancestor at least 45 million years ago.

Keywords: anatomical networks; cortical organization; functional connectivity; gradient; homology.

Figure 1.. Relative positions of areas in the human and marmoset.

In order to appreciate candidate homologous networks between the marmoset and human it is useful to orient using area landmarks. (Top) A lateral view of the human brain illustrates several classical Brodmann areas (BA)[43]. Acknowledging more modern specification of areas in these zones is possible (V2 and V3 only partially correspond to Brodmann’s 18/19), the relative positions of these areas compared to marmoset are informative. Zones of frontal cortex that are occupied by motor and premotor regions are marked by (I). The vast expanse of frontal cortex in the human is rostral to motor zones (II). (Bottom) A lateral view of the marmoset brain illustrates areas using distinct (more modern) criteria. The V1/V2/V3 label does not include V3a. What this comparison illustrates is that the relative positions of areas are conserved between species but also that the extensive frontal association zones in the human fall within a relatively compressed zone in the marmoset, while early retinotopic visual areas are disproportionately expanded in the marmoset as contrast to the human. Both humans and marmosets possess rostral prefrontal areas that are likely directly homologous (BA10 and A10). Comparisons of networks must consider the relative expansion and compression of cortical zones between the two primate species. The human cortex labels are based on [43] with MT labelled based on [44]. The marmoset areas reference the Paxinos et al. [45] atlas. See also [27].

Figure 2.. Direct contrast of human and marmoset network candidates.

(Example 1) The left columns display networks in the human based on functional connectivity MRI with seed regions in frontal cortex (white circles) next to candidate homologous networks in the marmoset based on retrograde label patterns from tracer injections in frontal cortex (blue arrows). (Example 2) The right columns display independent data replicating the human networks (in a second participant) and convergent retrograde label patterns for similarly localized injections in additional marmosets. The networks reveal a macroscale gradient in both the human and marmoset that progresses from a primarily local network to more distributed networks. Labels A-F illustrate the major gradient as the network estimates progress from motor (top) to frontal pole (bottom) seed regions. Tracer injections are plotted as if they are within the left hemisphere but variably come from individual cases with some right injections. Human functional connectivity MRI is from the left hemisphere and shows correlation using z values after r-to-z transform with a threshold for z > 0.2. Marmoset data show individually labelled cell bodies with black dots. The tracer injection cases are labeled in the bottom right as annotated in the Marmoset Brain Connectivity Atlas[14,30]. Area labels reference the Paxinos et al. [45] atlas. The human participants are two separate individuals from [8].

Figure 3.. Canonical networks reveal homologous topography in temporal and parietal cortex.

(I) Projection patterns from three groupings of frontal tracer injections reveal candidate homologues of the dorsal attention network (green), the frontoparietal control network (blue), and the default network (red) in the marmoset (also referred to as the apex transmodal network [13]). The surface is rotated to visualize temporal and parietal association cortex. White lines are positioned in the same locations across images radiating outward from area MT to aide visualization, with areas MT, AIP, OPt, LIP, TPO and TE3 indicated for reference. Additional lines point to areas A8aV, A47L, and A10 in frontal cortex. Labels D through E illustrate the caudal to rostral macroscale gradient that corresponds to the labels in Figure 1. (II) Human functional connectivity MRI estimates of the candidate homologous networks are illustrated within the two separate individuals using similar network colors to the marmoset. Frontal seed regions are displayed in white circles. In both parietal and temporal association cortex, the relative positions of network regions are conserved between the marmoset and human. The approximate location of the MT+ complex is indicated, with the green colored region located toward aMT (see also 14]). Human functional connectivity MRI shows correlation using z values after r-to-z transform with a threshold for z > 0.2. Labels D-F highlight the caudal-to-rostral gradient of networks in association cortex. An asterisk labels the posterior parietal region at or near Opt in the marmoset and the candidate corresponding default network component in the human.

Figure 4.. Canonical networks reveal homologous topography in frontal cortex.

(I) Projection patterns from three groupings of temporal and parietal tracer injections reveal candidate homologues of the dorsal attention network (green), the frontoparietal control network (blue), and the default network (red) in the marmoset. Posterior injections allow visualization of the relations between networks in frontal cortex. White lines are positioned in the same locations in frontal cortex across images to aide visualization. (II) Human functional connectivity MRI estimates of the candidate homologous networks are illustrated within the two separate individuals using similar network colors to the marmoset. Temporal cortex seed regions are displayed in white circles. Human functional connectivity MRI shows correlation using z values after r-to-z transform with a threshold for z > 0.2. Labels D-F highlight the caudal-to-rostral gradient of networks in prefrontal association cortex with a apex prefrontal network prominently including midline frontal regions in both species. An asterisk labels the posterior parietal region at or near Opt in the marmoset and the candidate corresponding default network component in the human.