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A structural and functional subdivision in central orbitofrontal cortex.

ABSTRACT: Economic choice requires many cognitive subprocesses, including stimulus detection, valuation, motor output, and outcome monitoring; many of these subprocesses are associated with the central orbitofrontal cortex (cOFC). Prior work has largely assumed that the cOFC is a single region with a single function. Here, we challenge that unified view with convergent anatomical and physiological results from rhesus macaques. Anatomically, we show that the cOFC can be subdivided according to its much stronger (medial) or weaker (lateral) bidirectional anatomical connectivity with the posterior cingulate cortex (PCC). We call these subregions cOFCm and cOFCl, respectively. These two subregions have notable functional differences. Specifically, cOFCm shows enhanced functional connectivity with PCC, as indicated by both spike-field coherence and mutual information. The cOFCm-PCC circuit, but not the cOFCl-PCC circuit, shows signatures of relaying choice signals from a non-spatial comparison framework to a spatially framed organization and shows a putative bidirectional mutually excitatory pattern.

SUBMITTER: Wang MZ

PROVIDER: S-EPMC9232485 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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A structural and functional subdivision in central orbitofrontal cortex.

Wang Maya Zhe MZ Hayden Benjamin Y BY Heilbronner Sarah R SR

Nature communications 20220624 1

Economic choice requires many cognitive subprocesses, including stimulus detection, valuation, motor output, and outcome monitoring; many of these subprocesses are associated with the central orbitofrontal cortex (cOFC). Prior work has largely assumed that the cOFC is a single region with a single function. Here, we challenge that unified view with convergent anatomical and physiological results from rhesus macaques. Anatomically, we show that the cOFC can be subdivided according to its much str ...[more]

PMID: 35750659

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Project description:Neuromodulators such as dopamine can alter the intrinsic firing properties of neurons and may thereby change the configuration of larger functional circuits. The primate orbitofrontal cortex (OFC) receives dopaminergic input from midbrain nuclei, but the role of dopamine in the OFC is still unclear. Here we tested the idea that dopaminergic activity changes the pattern of connectivity between the OFC and the rest of the brain and thereby reconfigures functional networks in the OFC. To this end, we combined double-blind, placebo-controlled pharmacology [D2 receptor (D2R) antagonist amisulpride] in humans with resting-state functional magnetic resonance imaging and clustering methods. In the placebo group, we replicated previously observed parcellations of the OFC into two and six subregions based on connectivity patterns with the rest of the brain. Most importantly, while the twofold clustering did not differ significantly between groups, blocking D2Rs significantly changed the composition of the sixfold parcellation, suggesting a dopamine-dependent reconfiguration of functional OFC subregions. Moreover, multivariate decoding analyses revealed that amisulpride changed the whole-brain connectivity patterns of individual OFC subregions. In particular, D2R blockade shifted the balance of OFC connectivity from associative areas in the temporal and parietal lobe toward functional connectivity with the frontal cortex. In summary, our results suggest that dopamine alters the composition of functional OFC circuits, possibly indicating a broader role for neuromodulators in the dynamic reconfiguration of functional brain networks.SIGNIFICANCE STATEMENT A key role of any neuromodulator may be the reconfiguration of functional brain circuits. Here we test this idea with regard to dopamine and the organization of functional networks in the orbitofrontal cortex (OFC). We show that blockade of dopamine D2 receptors has profound effects on the functional connectivity patterns of the OFC, yielding altered connectivity-based subdivisions of this region. Our results suggest that dopamine changes the connectional configuration of the OFC, possibly leading to transitions between different operating modes that favor either sensory input or recurrent processing in the prefrontal cortex. More generally, our findings support a broader role for neuromodulators in the dynamic reconfiguration of functional brain networks and may have clinical implications for understanding the actions of antipsychotic agents.

Project description:The orbitofrontal cortex (OFC) and hippocampus share striking cognitive and functional similarities. As a result, both structures have been proposed to encode "cognitive maps" that provide useful scaffolds for planning complex behaviors. However, while this function has been exemplified by spatial coding in neurons of hippocampal regions-particularly place and grid cells-spatial representations in the OFC have been investigated far less. Here we sought to address this by recording OFC neurons from male rats engaged in an open-field foraging task like that originally developed to characterize place fields in rodent hippocampal neurons. Single-unit activity was recorded as rats searched for food pellets scattered randomly throughout a large enclosure. In some sessions, particular flavors of food occurred more frequently in particular parts of the enclosure; in others, only a single flavor was used. OFC neurons showed spatially localized firing fields in both conditions, and representations changed between flavored and unflavored foraging periods in a manner reminiscent of remapping in the hippocampus. Compared with hippocampal recordings taken under similar behavioral conditions, OFC spatial representations were less temporally reliable, and there was no significant evidence of grid tuning in OFC neurons. These data confirm that OFC neurons show spatial firing fields in a large, two-dimensional environment in a manner similar to hippocampus. Consistent with the focus of the OFC on biological meaning and goals, spatial coding was weaker than in hippocampus and influenced by outcome identity.SIGNIFICANCE STATEMENT The orbitofrontal cortex (OFC) and hippocampus have both been proposed to encode "cognitive maps" that provide useful scaffolds for planning complex behaviors. This function is exemplified by place and grid cells identified in hippocampus, the activity of which maps spatial environments. The current study directly demonstrates very similar, though not identical, spatial representatives in OFC neurons, confirming that OFC-like hippocampus-can represent a spatial map under the appropriate experimental conditions.

Dataset Information

A structural and functional subdivision in central orbitofrontal cortex.

Publications

A structural and functional subdivision in central orbitofrontal cortex.

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