Highlights d A methodology to dissect the architecture of complex behavior patterns d Foraging patterns are built from finite, genetically controlled modules of behavior d Different modules are linked to different economic behavior patterns d Parental alleles of the Prader-Willi syndrome gene Magel2 regulate distinct modules SUMMARY Complex ethological behaviors could be constructed from finite modules that are reproducible functional units of behavior.Here, we test this idea for foraging and develop methods to dissect rich behavior patterns in mice. We uncover discrete modules of foraging behavior reproducible across different strains and ages, as well as nonmodular behavioral sequences. Modules differ in terms of form, expression frequency, and expression timing and are expressed in a probabilistically determined order. Modules shape economic patterns of feeding, exposure, activity, and perseveration responses. The modular architecture of foraging changes developmentally, and different developmental, genetic, and parental effects are found to shape the expression of specific modules. Dissecting modules from complex patterns is powerful for phenotype analysis. We discover that both parental alleles of the imprinted Prader-Willi syndrome gene Magel2 are functional in mice but regulate different modules. Our study found that complex economic patterns are built from finite, genetically controlled modules.

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SUMMARYDopa decarboxylase (DDC) regulates the synthesis of monoaminergic neurotransmitters and is linked to psychiatric and metabolic disorders. Ddc exhibits complex genomic imprinting effects that have not been functionally studied. Here, we investigate different noncanonical imprinting effects at the cellular level with a focus on Ddc. Using allele-specific reporter mice, we found Ddc exhibits dominant expression of the maternal allele in subpopulations of cells in 14 of 52 brain regions, and dominant paternal or maternal allele expression in adrenal cell subpopulations. Maternal versus paternal Ddc allele null mutations differentially affect offspring social, foraging and exploratory behaviors. Machine learning analyses of naturalistic foraging in Ddc−/+ and +/− offspring uncovered finite behavioral sequences controlled by the maternal versus paternal Ddc alleles. Additionally, parental Ddc genotype is revealed to affect behavior independent of offspring genotype. Thus, Ddc is a hub of maternal and paternal influence on behavior that mediates diverse imprinting and parental effects.HIGHLIGHTSDopa decarboxylase (Ddc) allelic expression resolved at the cellular levelCells differentially express maternal versus paternal Ddc allelesMaternal and paternal Ddc alleles control distinct behavioral sequencesParental Ddc genotype affects offspring independent of mutation transmissioneTOCAllelic reporter mice and machine learning analyses reveal dopa decarboxylase is affected by diverse imprinting and parental effects that shape finite behavioral sequences in sons and daughters.

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Foraging involves innate decision heuristics that are adapted for the wild but can cause economically irrational cognitive biases in some contexts. The mechanisms underlying cognitive biases are poorly understood but likely involve genetic mechanisms. Here, we investigate foraging in fasted mice using a naturalistic paradigm and uncover an innate "second-guessing" cognitive bias that involves repeatedly investigating a former depleted food patch instead of consuming available food. Second guessing is economically irrational because it incurs energetic costs in place of caloric benefits. Since learning and memory are involved, we tested roles for Arc and found that Arc-/- mice lack second guessing, which causes increased food consumption in males during foraging. Using unsupervised machine learning, decompositions of Arc-/- and +/+ mouse behavior show that Arc affects discrete foraging sequences involved in second-guessing and later stages of memory. Thus, revealing a genetic basis for this bias and ethological role for Arc in a naturalistic behavior.