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Beta traveling waves in monkey frontal and parietal areas encode recent reward history.

ABSTRACT: Brain function depends on neural communication, but the mechanisms of this communication are not well understood. Recent studies suggest that one form of neural communication is through traveling waves (TWs)-patterns of neural oscillations that propagate within and between brain areas. We show that TWs are robust in microarray recordings in frontal and parietal cortex and encode recent reward history. Two adult male monkeys made saccades to obtain probabilistic rewards and were sensitive to the (statistically irrelevant) reward on the previous trial. TWs in frontal and parietal areas were stronger in trials that followed a prior reward versus a lack of reward and, in the frontal lobe, correlated with the monkeys' behavioral sensitivity to the prior reward. The findings suggest that neural communication mediated by TWs within the frontal and parietal lobes contribute to maintaining information about recent reward history and mediating the impact of this history on the monkeys' expectations.

SUBMITTER: Zabeh E

PROVIDER: S-EPMC10480436 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Beta traveling waves in monkey frontal and parietal areas encode recent reward history.

Zabeh Erfan E Foley Nicholas C NC Jacobs Joshua J Gottlieb Jacqueline P JP

Nature communications 20230905 1

Brain function depends on neural communication, but the mechanisms of this communication are not well understood. Recent studies suggest that one form of neural communication is through traveling waves (TWs)-patterns of neural oscillations that propagate within and between brain areas. We show that TWs are robust in microarray recordings in frontal and parietal cortex and encode recent reward history. Two adult male monkeys made saccades to obtain probabilistic rewards and were sensitive to the ...[more]

PMID: 37669966

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Project description:In primates, working memory function depends on activity in a distributed network of cortical areas that display different patterns of delay task-related activity. These differences are correlated with, and might depend on, distinctive properties of the neurons located in each area. For example, layer 3 pyramidal neurons (L3PNs) differ significantly between primary visual and dorsolateral prefrontal (DLPFC) cortices. However, to what extent L3PNs differ between DLPFC and other association cortical areas is less clear. Hence, we compared the properties of L3PNs in monkey DLPFC versus posterior parietal cortex (PPC), a key node in the cortical working memory network. Using patch-clamp recordings and biocytin cell filling in acute brain slices, we assessed the physiology and morphology of L3PNs from monkey DLPFC and PPC. The L3PN transcriptome was studied using laser microdissection combined with DNA microarray or quantitative PCR. We found that in both DLPFC and PPC, L3PNs were divided into regular spiking (RS-L3PNs) and bursting (B-L3PNs) physiological subtypes. Whereas regional differences in single-cell excitability were modest, B-L3PNs were rare in PPC (RS-L3PN:B-L3PN, 94:6), but were abundant in DLPFC (50:50), showing greater physiological diversity. Moreover, DLPFC L3PNs display larger and more complex basal dendrites with higher dendritic spine density. Additionally, we found differential expression of hundreds of genes, suggesting a transcriptional basis for the differences in L3PN phenotype between DLPFC and PPC. These data show that the previously observed differences between DLPFC and PPC neuron activity during working memory tasks are associated with diversity in the cellular/molecular properties of L3PNs.SIGNIFICANCE STATEMENT In the human and nonhuman primate neocortex, layer 3 pyramidal neurons (L3PNs) differ significantly between dorsolateral prefrontal (DLPFC) and sensory areas. Hence, L3PN properties reflect, and may contribute to, a greater complexity of computations performed in DLPFC. However, across association cortical areas, L3PN properties are largely unexplored. We studied the physiology, dendrite morphology and transcriptome of L3PNs from macaque monkey DLPFC and posterior parietal cortex (PPC), two key nodes in the cortical working memory network. L3PNs from DLPFC had greater diversity of physiological properties and larger basal dendrites with higher spine density. Moreover, transcriptome analysis suggested a molecular basis for the differences in the physiological and morphological phenotypes of L3PNs from DLPFC and PPC.

Dataset Information

Beta traveling waves in monkey frontal and parietal areas encode recent reward history.

Publications

Beta traveling waves in monkey frontal and parietal areas encode recent reward history.

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