Biology subjects

Okuyama, T.

Publications and source records attributed to Okuyama, T..

7 recordsLinked to original sources

bioRxiv2025

Genetic heterogeneity alleviates behavioral trade-off between exploration and vigilance in Drosophila

Trade-offs between conflicting behaviors fundamentally constrain animal performance, yet group living can alter how such trade-offs are expressed and alleviated. Here, we disentangled the effects of aggregation and heterogeneity, both arising from group living, on the exploration-vigilance trade-off in Drosophila. Using 78 genetically distinct strains from the Drosophila Genetic Reference Panel, we compared behavioral responses of single individuals, homogeneous groups (six individuals from the same strain), and heterogeneous groups (three individuals from each of two distinct strains) under predator-like looming stimuli. Pareto optimization analysis revealed that aggregation increased both exploratory and vigilance behavior, thereby exposing the underlying exploration-vigilance trade-off. In contrast, heterogeneity enhanced group performance beyond expected levels, alleviating the cost of balancing exploration and vigilance. To identify the phenotypic basis of this alleviation, we developed a phenome-wide higher-level association study (PheHAS) that screened 190 phenotypes across strain pairs. We found that heterogeneity in activity patterns and morphological traits promoted trade-off alleviation, whereas similarity in infection responses also contributed, suggesting that social facilitation may contribute. Our study provides the first explicit demonstration that aggregation and heterogeneity exert distinct effects on a group-level behavioral trade-off and introduces PheHAS as a generalizable framework for identifying the phenotypic bases underlying diversity effects in animal groups.

animal behavior and cognition↗

bioRxiv2024

Genetic heterogeneity induces nonadditive behavioural changes in Drosophila

The formation and dynamics of group behaviours are important topics in ecology and evolution. Although several theoretical studies assume homogeneity among individuals, real-world organisms often display remarkable behavioural diversity within groups. This study investigated the synergistic impact of genetic heterogeneity on group behaviour and reveals the behavioural underpinnings of diversity effects using 83 genetically distinct strains of Drosophila melanogaster. Various indices of foraging behaviour, including movement speed, search comprehensiveness, spatial preference and stopping time, were measured using homogeneous (single strain) and heterogeneous (mixing two distinct strains) groups of flies. The heterogeneous groups exhibited significant increases in spatial preference and stopping time compared with the homogeneous groups, suggesting that genetic heterogeneity induces nonadditive changes in group behaviour. Furthermore, the magnitude and direction of the behavioural change varied among different combinations. Multiple regression analysis showed that the phenotypic distance in some traits between mixed strains could explain the emergence of diversity effects on group behaviour. Specifically, interindividual heterogeneity in the locomotor activity level showed a positive correlation with diversity effects. These results emphasise the importance of intraspecific diversity in group dynamics and suggest that genetic heterogeneity can improve group performance through the acquisition of novel behavioural traits.

animal behavior and cognition↗

bioRxiv2024

Sexual representation of social memory in the ventral CA1 neurons

Recognizing familiar individuals is crucial for adaptive social interactions among animals. However, the multidimensional nature of social memory encompassing sexual information remains unelucidated. We found that neurons in the ventral CA1 region (vCA1) of the mouse hippocampus encoded the identities and social properties, specifically sex and strain, of familiar conspecifics by using both rate and theta-based temporal coding. Optogenetic reactivation of social memories of females, but not males, induced place preference. Ablation of the upstream hippocampal dorsal CA2 region (dCA2) or the medial amygdala (MeA) disrupted the representation of sex and the sexual dichotomy of social memory valence. Selective reactivation of overlapping neural populations of distinct female social memories representing the female sex was sufficient to induce preference. Thus, vCA1 neurons employ dual coding schemes to represent the identities and social properties of familiar conspecifics as a cohesive memory. One-Sentence SummarySocial memory in the mouse ventral hippocampus maps the identities and social properties of familiar conspecifics.

neuroscience↗

bioRxiv2024

Conditional knockout of Shank3 in the ventral CA1 by quantitative in vivo genome-editing impairs social memory

Individuals with autism spectrum disorder (ASD) have a higher prevalence of social memory impairment. A series of our previous studies revealed that hippocampal ventral CA1 (vCA1) neurons possess social memory engram and that the neurophysiological representation of social memory in the vCA1 neurons is disrupted in ASD-associated Shank3 knockout mice. However, whether the dysfunction of Shank3 in vCA1 causes the social memory impairment observed in ASD remains unclear. In this study, we found that vCA1-specific Shank3 conditional knockout (cKO) by the adeno-associated virus (AAV)- or specialized extracellular vesicle (EV)-mediated in vivo gene editing was sufficient to recapitulate the social memory impairment in male mice. Furthermore, the utilization of EV-mediated Shank3-cKO allowed us to quantitatively examine the role of Shank3 in social memory. Our results suggested that there is a certain threshold for the proportion of Shank3-cKO neurons required for social memory disruption. Thus, our study provides insight into the population coding of social memory in vCA1, as well as the pathological mechanisms underlying social memory impairment in ASD.

neuroscience↗

bioRxiv2024

The ventral hippocampus and nucleus accumbens underlie long-term social memory about female conspecifics in male mice

For many social animals, including humans, the ability to remember and recognize conspecifics (i.e., having social memory), especially a mating partner, is essential for adaptive reproductive strategies. Our previous studies have shown that social memory about same-sex conspecifics, namely male-to-male social memory, is stored in hippocampal ventral CA1 (vCA1) neurons and that neural projections from the vCA1 to the nucleus accumbens (NAc) are crucial for social discriminatory behavior. However, how the memory of an opposite-sex conspecific, specifically male-to-female social memory, and how the social memory modulates sexual behavior in males remain unknown. Herein, we investigated the ultrasonic vocalizations (USVs) and socially approaching behavior of males toward a female before and after social memory formation. We found that the total duration of USVs was reduced when the male mice interacted with a familiar female. This reduction in USV emission was blocked by optogenetic inhibition of vCA1 neurons, as well as D1- and D2-dopamine receptor (D1R and D2R) expressing neurons in the NAc. Furthermore, fiber photometry recordings in the NAc revealed that the activities of both D1R and D2R neuronal populations were altered during social interaction with familiar or novel females after the process of familiarization. The response of D1R-neurons was reduced only when interacting with familiar females. In contrast, although responses of D2R-neurons were reduced toward both familiar and novel females after social memory formation, the reduction towards novel females was significantly more pronounced compared to that towards familiar females. Our findings suggested that the activities of both vCA1 neurons and D1R- and D2R-expressing NAc neurons in males were differentially modulated by the presence of social memory about females during adaptive reproductive strategies. Significance StatementLong-term social memory about females modulates male sexual behavior, specifically ultrasonic vocalization emissions, mediated by hippocampal ventral CA1 and dopamine receptor expressing neurons in the nucleus accumbens.

neuroscience↗

bioRxiv2022

Epigenetically distinct synaptic architecture in clonal compartments in the teleostean dorsal pallium

The dorsal telencephalon (i.e. the pallium) exhibits high anatomical diversity across vertebrate classes. The mammalian dorsal pallium accommodates a six layered-structure, the neocortex, whereas the teleostean dorsal pallium possesses various compartmentalized structures among species. The development, function and evolution of the fish dorsal pallium remain unillustrated. Here, we analyzed the structure and epigenetic landscapes of cell lineages in the telencephalon of medaka fish (Oryzias latipes) which possesses a clearly delineated dorsal pallium (the Dd2 region). We found that different pallial regions, including Dd2, are formed by mutually exclusive clonal units, and that each pallium compartment exhibits a distinct epigenetic landscape. In particular, Dd2 possesses a unique open chromatin pattern that preferentially targets synapse-related genes. Indeed, Dd2 shows a high density of synapses, which might reflect strong plasticity. Finally, we identified several transcription factors as candidate regulators for the Dd2, which are partially shared with the human neocortex and hippocampus.

neuroscience↗

bioRxiv2021

Disrupted social memory ensembles in the ventral hippocampus underlie social amnesia in autism-associated Shank3 mutant mice

The ability to remember conspecifics is critical for adaptive cognitive functioning and social communication, and impairments of this ability are hallmarks of autism spectrum disorders (ASDs). Although hippocampal ventral CA1 (vCA1) neurons are known to store social memories, how their activities are coordinated remains unclear. Here we show that vCA1 social memory neurons, characterized by enhanced activity in response to memorized individuals, were preferentially reactivated during sharp-wave ripples (SPW-Rs). Spike sequences of these social replays reflected the temporal orders of neuronal activities within theta cycles during social experiences. In ASD model Shank3 knockout mice, the proportion of social memory neurons was reduced, and neuronal ensemble spike sequences during SPW-Rs were disrupted, which correlated with impaired discriminatory social behavior. These results suggest that SPW-R-mediated sequential reactivation of neuronal ensembles is a canonical mechanism for coordinating hippocampus-dependent social memories and its disruption underlies the pathophysiology of social memory defects associated with ASD.

neuroscience↗