A proposed structural connectivity matrices approach for the superior fronto-occipital fascicle in the Harvard-Oxford Atlas comparative framework following the Pandya comparative extrapolation principle

Abstract

A key set of connections necessary for the most complex brain functions are the long association cortico-cortical fiber tracts. These pathways have been described by the Dejerines and others using post mortem histological or brain dissection techniques. Given methodological limitations, these fiber connections have not been delineated completely in humans. Although the stem portions of fiber tracts have been identified in humans, their precise origins and terminations remain to be determined. By contrast, the origins and terminations as well as the stems of long cortico-cortical association fiber pathways in monkeys have been detailed in the macaque monkey brain using experimental tract tracing methods. Deepak Pandya made major contributions to the delineation of fiber tracts in the monkey brain. In the early 1990s, he compared his observations in monkeys with the original descriptions in humans by the Dejerines. With the advent of diffusion-weighted imaging, Dr. Pandya extended this line of investigation to the human brain with Dr. Nikos Makris. In this translational analysis of long association cortico-cortical fiber tracts, they applied a principle of extrapolation from monkey to human. In the present study, we addressed the reasoning and the complex methodology in translating brain structural connectivity from monkey to human in one cortico-cortical fiber tract, namely the superior fronto-occipital fascicle, which was delineated in both species by Dr. Pandya and colleagues. Furthermore, we represented this information in the form of connectional matrices in the context of the HOA2.0-ComPaRe framework, a homological monkey-to-human translational system used in neuroimaging.

Keywords: DTI; Harvard-Oxford Atlas; dMRI; fiber bundle; superior fronto-occipital fascicle; tractography.

Figure 1:

Strategy for the validation of diffusion MRI tractography in human brains using monkey tract tracing data, fiber pathway stem location in monkey and human white matter, and cortical parcellation in humans and monkey brains. The dashed arrow denotes the lack of validated origins and terminations of human brain fiber pathways. Figure modified from (Rushmore et al., 2020a).

Figure 2:

The nominal structural connectivity matrix (NSCM) of the sFOF for humans and monkeys represented as symmetric adjacency matrices. Upper: Connectional data obtained prior to the advent of diffusion tensor imaging (Pre-dMRI era). Middle: Connectional information derived from dMRI-based tractography of the human brain (dMRI era). Lower: Connectional data for the sFOF from experimental tract tracing methods in the monkey brain. See Table 1 for abbreviations.

Figure 3:

The nominal structural connectivity matrix (NSCM) of the sFOF represented with respect to cortical parcellation units for lateral and medial brain surfaces (A) and corresponding circular network diagrams (B). Upper: Connectional data in the human brain obtained prior to the advent of diffusion tensor imaging (Pre-dMRI era). Parcellation units (Caviness et al., 1996) connected by the sFOF are denoted in blue (A) and by connecting lines (B). Middle: Connectional data for the sFOF from dMRI-based tractography studies. Lower: Parcellation units connected by the sFOF in the monkey (Rushmore et al., 2022). See Table 1 for abbreviations.

Figure 4:

The topographic structural connectivity matrix (TSCM) of the sFOF in which the location of the sFOF stem is specified according to its location in hemispheric white matter sectors (columns) and originating from parcellation units (rows). White matter sectors and gray matter parcellation units are based on the HOA white and gray matter parcellation system for the human brain (Caviness et al., 1996; Makris et al., 1999; Meyer et al., 1999). It should be noted that for a complete definition of a fiber tract, two matrices are required: the topographic matrix, as described here, and the nominal matrix (e.g., Figures 2 and 3). The topographic matrix denotes the precise topography of the stem of the fiber tract in the hemispheric white matter, whereas the nominal matrix specifies its origins and terminations.

Figure 5:

In this figure, the morphologic and topographic similarity of the sFOF stem between monkey (A, C) and human (B, D) is depicted. Specifically, the stem of the sFOF has a longitudinal orientation and elongated shape in the anterior-posterior dimension and is located medial to the corona radiata, lateral or superior-lateral to the lateral ventricle and the body of the corpus callosum, and superior-lateral to the head and body of the caudate nucleus. A, B: Schematic figures illustrating the location of the stem of the sFOF (green) in the monkey brain (A) and in the human brain (B). The topological relationship of the sFOF stem in both figures is shown with respect to the corpus callosum (CC), the lateral ventricle and the caudate nucleus. The two coronal sections in A and B have been modified, respectively, from the monkey brain atlas of Schmahmann and Pandya (2006) and the human brain atlas of Dejerine and Dejerine-Klumpke (Dejerine and Dejerine-Klumpke, 1895). C, D: The stem of the sFOF is shown in the context of parasagittal MRI images modified from Schmahmann et al. (2007) in the monkey brain and Makris et al. (2007) in the human brain. Abbreviations: AC – anterior commissure; CC – corpus callosum; PC – posterior commissure.