Differential functional connectivity underlying asymmetric reward-related activity in human and nonhuman primates

Abstract

The orbitofrontal cortex (OFC) is a key brain region involved in complex cognitive functions such as reward processing and decision making. Neuroimaging studies have reported unilateral OFC response to reward-related variables; however, those studies rarely discussed this observation. Nevertheless, some lesion studies suggest that the left and right OFC contribute differently to cognitive processes. We hypothesized that the OFC asymmetrical response to reward could reflect underlying hemispherical difference in OFC functional connectivity. Using resting-state and reward-related functional MRI data from humans and from rhesus macaques, we first identified an asymmetrical response of the lateral OFC to reward in both species. Crucially, the subregion showing the highest reward-related asymmetry (RRA) overlapped with the region showing the highest functional connectivity asymmetry (FCA). Furthermore, the two types of asymmetries were found to be significantly correlated across individuals. In both species, the right lateral OFC was more connected to the default mode network compared to the left lateral OFC. Altogether, our results suggest a functional specialization of the left and right lateral OFC in primates.

Viewing Ambiguous Social Interactions Increases Functional Connectivity between Frontal and Temporal Nodes of the Social Brain

“…Faces were just part of the complex scenes being presented, and the monkeys were not explicitly required to track the faces for reward. Further, it has been argued by the coauthors that these regions within PFC (including lateral orbital sulcus) are less concerned with face-processing per se, and more concerned with linking choices (as represented by any type of stimuli, including but not limited to faces) and outcomes ( Chau et al, 2015 ; Lopez-Persem et al, 2020 ; Sallet et al, 2020 ). It is thus conceivable that while there might have been activation to face stimuli (over no actors) in frontal cortex, it did not achieve a sufficient signal-to-noise ratio to surpass our statistical threshold.…”

Imaging evolution of the primate brain: the next frontier?

“…An HCP-like multimodal neuroimaging approach would enable addressing brain lateralisations at the microarchitecture, connectomics, and functional levels as well as their interdependencies. For instance, in the orbitofrontal cortex, even when both hemispheres are similar at the cytoarchitectonic level ( Mackey and Petrides, 2010 ), rs-fMRI analysis can reveal hemispheric differences in connectivity within the default-mode network ( Lopez-Persem et al, 2020 ), in both humans and macaques. Studying the evolution of brain lateralisation in primate models would benefit from the reuse of MRI data progressively made available thanks to new open data initiatives ( Milham et al, 2018 , 2020 ).…”

Default Mode Network spatial configuration varies across task domains

“…Since those observations, many further functions were shown to be associated to this network. Other than self-referential and emotional processes (Buckner and Carroll, 2007; D’Argembeau et al, 2010; Denny et al, 2012; Engen et al, 2017; Fingelkurts et al, 2020; Fossati et al, 2003; Knyazev et al, 2020; Molnar-Szakacs and Uddin, 2013; Northoff et al, 2006; Northoff and Bermpohl, 2004; Ochsner et al, 2005, 2004; Satpute and Lindquist, 2019; Uddin et al, 2007), the DMN turned out to be related to memory and mental time-travel (Addis et al, 2007; Cabeza et al, 1997; Foster et al, 2012; Kim, 2016; Murphy et al, 2018; Rugg and Vilberg, 2013; Schacter et al, 2008, 2007; Spreng et al, 2015; Svoboda et al, 2006; Yang et al, 2013), mental simulation and scene construction (Gerlach et al, 2011; Hassabis et al, 2007; Hassabis and Maguire, 2007; Spreng and Grady, 2010), theory of mind (ToM) and social cognition (Amft et al, 2015; Mar, 2011; Mars et al, 2012; Mwilambwe-Tshilobo and Spreng, 2021; Rilling et al, 2004; Ruby and Decety, 2004; Saxe and Kanwisher, 2003; Saxe and Powell, 2006; Spreng and Andrews-Hanna, 2015), moral judgment (Bzdok et al, 2012; Greene et al, 2001; Harrison et al, 2008; Pujol et al, 2008), semantic processing (Binder et al, 1999, 2009; Chiou et al, 2020; Evans et al, 2020; Lanzoni et al, 2020), and reward mechanisms (Lopez-Persem et al, 2020; Martins et al, 2021; Xue et al, 2009). However, most of these psychological functions can still be somewhat associated with the resting state (Wen et al, 2020).…”