Distributed representation of context by intrinsic subnetworks in prefrontal cortex

Abstract

Human prefrontal cortex supports goal-directed behavior by representing abstract information about task context. The organizational basis of these context representations, and of representations underlying other higher-order processes, is unknown. Here, we use multivariate decoding and analyses of spontaneous correlations to show that context representations are distributed across subnetworks within prefrontal cortex. Examining targeted prefrontal regions, we found that pairs of voxels with similar context preferences exhibited spontaneous correlations that were approximately twice as large as those between pairs with opposite context preferences. This subnetwork organization was stable across task-engaged and resting states, suggesting that abstract context representations are constrained by an intrinsic functional architecture. These results reveal a principle of fine-scaled functional organization in association cortex.fMRI | resting-state | rule | cognitive control | functional organization T he cerebral cortex exhibits functional organization at multiple spatial scales. At a coarse scale, the cortex is parcellated into functional areas (1, 2) that coordinate as networks through longrange connections (3-5). These areas represent and compute information with functional circuitry that is organized more finely. Some fine-scaled, intrinsic principles have been described in detail, particularly for sensory cortex (6, 7). In contrast, the subregional organization of prefrontal cortex (PFC), which gives rise to higherorder processes, including attention, decision-making, and goaldirected action (8, 9), remains largely uncharacterized. Whether PFC representations are encoded within an equipotential system or constrained by an intrinsic functional architecture is currently unknown.Sensory cortex can be mapped by parametrically varying stimulus attributes and measuring changes in the neural response, but complex and dynamic response properties limit the effectiveness of this approach for mapping PFC and other association regions. An alternate strategy is to leverage spontaneous variability in neural activity. Neural responses to repeated presentations of sensory stimuli, or in the absence of stimulation and explicit task demands, exhibit variability that is attributed to ongoing spontaneous activity (10-13). Traditional analyses consider spontaneous activity to be noise, but there is increasing evidence that shared spontaneous variability is a signature of functional organization (14). Analyses of spontaneous correlations have been used to identify multiple large-scale functional networks (4,5,15) and boundaries between functional areas (2, 16-18) in human and nonhuman primate association cortex. The spontaneous correlation structure also mirrors established fine-scaled principles of functional organization in visual cortex, such as preferences for retinotopic position (19) and stimulus orientation (20). We therefore leveraged spontaneous activity to examine the finescaled functional organization of human PFC.We focus...

Functional connectivity of task context representations in prefrontal nodes of the multiple demand network

“…These subnetworks are task specific and seem to be specialized for the particular demands and requirements of a concrete task. Our result confirms the earlier report by Waskom and Wagner ( 2017 ) that lateral prefrontal cortex voxels coding for particular task relevant stimulus features show stronger functional connectivity during subsequent rest. We here show that this is also true for the subsets of voxels from the multiple demand networks, both within and between the nodes of this network.…”

“…In vivo parcellation studies have shown that connectivity similarity analyses allow to further break up these territories into smaller fields, each with a unique connectivity profile resembling the organization of the larger network to which they belong, but uniquely different across individuals and species (Goulas et al 2012 , 2017 ; Sallet et al 2013 ; Braga and Buckner 2017 ). Our current findings, together with those of some other studies (Park et al 2017 ; Waskom and Wagner 2017 ), go a step further by showing that even within this connectionally more homogeneous fields, unique and function-specific subpatterns of connectivity can be demonstrated to exist.…”

“…They found stronger functional coupling between multiple demand voxels tuned to the same task than voxels with non-matched preferences, even when the task executed was not the task to which the voxels were tuned. A further step in demonstrating the stability of task context-specific assemblies was recently provided by Waskom and Wagner ( 2017 ). They showed that voxels in the larger inferior frontal sulcus cortex that contributed to decoding attention to a particular stimulus dimension (i.e.…”

In V4, pair-wise synchrony and correlations depend on the structure of the population code

“…As correlations with the pool are stronger than across pools, they have as effect to amplify the signal within the pool and to help a reliable transmission of the signal. On a coarser spatial and temporal scale, it has been demonstrated that patterns of spontaneous activity reflect the functional architecture of the cortex [24,25,26], including the representation of abstract information, such as rules or goals [27]. Finding the same organization in V4 on a smaller spatial scale and during active classification of stimuli opens up the possibility that correlation structure also actively supports processing of stimuli in abstract categorization tasks.…”

Just above chance: is it harder to decode information from human prefrontal cortex BOLD signals?

“…MVPA has been applied to fMRI data from all over the brain, and the prefrontal cortex is no exception. Several studies have reported statistically reliable classification of task rule and other task-relevant variables from regions within prefrontal cortex [36][37][38][39][40][41] .…”