Topographic Mapping as a Basic Principle of Functional Organization for Visual and Prefrontal Functional Connectivity

Abstract

The organization of region-to-region functional connectivity has major implications for understanding information transfer and transformation between brain regions. We extended connective field mapping methodology to 3-D anatomic space to derive estimates of corticocortical functional organization. Using multiple publicly available human (both male and female) resting-state fMRI data samples for model testing and replication analysis, we have three main findings. First, we found that the functional connectivity between early visual regions maintained a topographic relationship along the anterior-posterior dimension, which corroborates previous research. Higher order visual regions showed a pattern of connectivity that supports convergence and biased sampling, which has implications for their receptive field properties. Second, we demonstrated that topographic organization is a fundamental aspect of functional connectivity across the entire cortex, with higher topographic connectivity between regions within a functional network than across networks. The principle gradient of topographic connectivity across the cortex resembled whole-brain gradients found in previous work. Last but not least, we showed that the organization of higher order regions such as the lateral prefrontal cortex demonstrate functional gradients of topographic connectivity and convergence. These organizational features of the lateral prefrontal cortex predict task-based activation patterns, particularly visual specialization and higher order rules. In sum, these findings suggest that topographic input is a fundamental motif of functional connectivity between cortical regions for information processing and transfer, with maintenance of topography potentially important for preserving the integrity of information from one region to another.

Gradient organisation of functional connectivity within resting state networks is present from 25 weeks gestation in the human fetal brain

“…Gradated organisation of functional connectivity is thought to be integral to efficient information processing and transfer via local processing streams across the brain (Laughlin & Sejnowski, 2003;Margulies et al, 2016;O'Rawe & Leung, 2020). In this study, we show that robust gradient organisations of functional connectivity are already established within the majority of RSNs in the fetal cortex from 25 GW.…”

“…This can be characterised as a connectivity gradient such that adjacent locations of the cortex are functionally connected to similar or overlapping cortical areas (Bernhardt et al, 2022;Goldberg, 1989;Haak et al, 2018;Margulies et al, 2016;Sepulcre et al, 2012). This gradient organisation of functional connectivity is now thought to be a fundamental property of the mature human brain which underlies efficient complex neural processing and information integration (Bernhardt et al, 2022;Huntenburg et al, 2018;Kaas, 1997;Laughlin & Sejnowski, 2003;O'Rawe & Leung, 2020). Gradient organisations of functional connectivity within networks, known as connectopic maps, can be used to probe the specificity of connections within a network, for example, the widely recognised topographic organisation of activity and connections within the primary sensory and motor cortices (e.g., somatotopic, tonotopic and retinotopic) (Haak et al, 2018;Park et al, 2021).…”

Distinct lateral prefrontal regions are organized in an anterior-posterior functional gradient

“…Overall, our results support the notion that functionally-dissociable areas in the DLPFC are organized along the anterior-posterior axis in a functional gradient. This type of organization has been observed in other brain systems, such as the visual system, where individual regions (V1, V2, V4, IT), which are anatomically and functionally distinct from each other, are arranged along an anterior-posterior functional gradient, with more anterior regions having larger receptive fields and more complex response selectivities (Freud et al, 2017;Hubel and Wiesel, 1959;Lerner, 2001;O'Rawe and Leung, 2020;Tsao et al, 2006). The ability to record large numbers of neurons simultaneously across multiple brain regions in behaving animals provides an important resource for systems neuroscience research (Dotson et al, 2018;Mitz et al, 2017).…”

Gradient organisation of functional connectivity within resting state networks is present from 25 weeks gestation in the human fetal brain

“…This can be characterised as a connectivity gradient such that adjacent locations of the cortex are functionally connected to similar or overlapping cortical areas (Bernhardt et al, 2022 ;Goldberg, 1989 ;Haak et al, 2018 ;Margulies et al, 2016 ;Sepulcre et al, 2012 ). This gradient organisation of functional connectivity is now thought to be a fundamental property of the mature human brain which underlies efficient complex neural processing and information integration (Bernhardt et al, 2022 ;Huntenburg et al, 2018 ;Kaas, 1997 ;Laughlin & Sejnowski, 2003 ;O'Rawe & Leung, 2020 ). Gradient organisations of functional connectivity within networks, known as connectopic maps, can be used to probe the specificity of connections within a network, for example, the widely recognised topographic organisation of activity and connections within the primary sensory and motor cortices (e.g., somatotopic, tonotopic and retinotopic) (Haak et al, 2018 ;Park et al, 2021).…”