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Okanoya, K.

Publications and source records attributed to Okanoya, K..

At least 19 recordsLinked to original sources

DiverScan: attention-guided exploratory analysis of animal behaviour across diverse comparative experiments

High-throughput tracking yields rich time-series data of animal behaviour, yet extracting biological insight remains a bottleneck, even for simple control--treatment comparisons. Existing analyses struggle to pinpoint the multiple, nonlinearly intertwined differences hidden in the data and fail to generalise across diverse recording set-ups. Here we present DiverScan, a deep-learning framework for attention-guided exploratory analysis of behavioural time series. DiverScan disentangles condition-dependent behavioural differences by pairing a loss function tailored to data exploration with an attention-branch architecture, and highlights condition-specific behavioural features visually and with explanatory text generated by a large language model. DiverScan is validated on a synthetic benchmark and on datasets from seven laboratories spanning multiple species and both single- and multi-animal behaviour. Beyond recovering known phenotypes, we demonstrate that DiverScan helps researchers generate new hypotheses across these diverse datasets. Available as Jupyter notebooks with a graphical user interface and flexible input formats, DiverScan can integrate into existing behavioural-analysis pipelines.

animal behavior and cognition↗

A sensorimotor brain circuit for transforming aversive experiences into emotional states

Innately aversive experiences produce emotional states which control behavior as well as long term associative memories1-3. Brainstem regions engage innate defensive reactions1,3-7, but it is unclear how the nervous system transduces external aversive experiences into higher order, emotional representations in the forebrain to instruct learning and modulate behavior. The prevailing view is that the sensory properties of aversive experiences activate forebrain emotional processing1,3,8-10, but classical theories proposed that internal bodily reactions to unpleasant events produce feeling states11,12. Here we identify a brainstem cuneiform (CnF) circuit which conveys information about both the external sensory causes and internal motor reactions related to aversive events to the lateral/basal nuclei of the amygdala (LA/B), a brain region which stores emotional memories, to enhance ongoing defensive behaviors and regulate associative memory formation. Glutamatergic CnF neurons project directly to LA/B and receive afferent inputs from aversive-sensory and aversive-motor brain regions. Notably, LA/B neurons encode a sensorimotor state in response to noxious stimuli, with both sensory and motor features transmitted through the CnF-to-LA/B pathway. Finally, optogenetic perturbation experiments showed that during aversive experiences, the CnF-LA/B circuit instructs emotional memory formation and enhances the intensity of ongoing defensive behaviors. These findings reveal how the nervous system constructs an aversive sensorimotor state in the amygdala used for regulating the strength of emotional behaviors and producing memory formation. This demonstrates a clinically relevant brain mechanism for the regulation of emotional processing by both external traumatic events and the accompanying bodily reactions.

neuroscience↗

Rats spontaneously show categorical responses toward familiar or unfamiliar conspecifics in a habituation-dishabituation task using multiple habituation stimuli

Discriminating between familiar and unfamiliar conspecifics is a fundamental aspect of social recognition. Previous studies have shown that familiarity strongly influences rat social behavior, and that rats can be trained to discriminate between olfactory cues from cage-mates and non-cage-mates in a digging task. However, such discrimination did not occur in a lever-pressing task using live conspecifics as stimuli. In the present study, we investigated whether rats could discriminate social familiarity in a simple, less-demanding and naturalistic context using whole-animal stimuli. We employed a habituation-dishabituation paradigm in which multiple cage-mate or non-cage-mate individuals were presented during the habituation phase. We examined whether rats would habituate to the familiarity category among these multiple stimuli and subsequently show dishabituation when the stimulus class switched (cage-mate to non-cage-mate or vice versa). During the habituation phase, exploratory responses declined over successive sessions, suggesting habituation to the common element among multiple cage-mates or non-cage-mates, i.e., familiarity/unfamiliarity. When all subjects were considered together, clear dishabituation was not observed, indicating individual variation in habituation. However, a post-hoc analysis restricted to subjects showing sufficient habituation revealed significant dishabituation to the stimulus class switch. These findings suggest that rats can spontaneously classify multiple conspecifics according to their familiarity without training. Rats may flexibly employ different forms of social recognition and information such as individual identity or familiarity-based heuristics to guide adaptive social behavior in varying contexts. HighlightsO_LIWe tested familiarity discrimination in rats by habituation-dishabituation task C_LIO_LIMultiple cage-mate or non-cage-mate stimuli were presented during habituation C_LIO_LIExploratory responses decreased as habituation sessions progressed C_LIO_LIDishabituation occurred in individuals who exhibited sufficient habituation C_LIO_LIRats showed categorical responses toward familiarity or unfamiliarity C_LI

animal behavior and cognition↗

Neural entrainment predicts the anticipatory P300 component during musical meter perception: An EEG study using dual-meter sound stimuli

Meter, the organization of beats into regular groupings, is a core element of music perception that arises from the interplay between the bottom-up processing of acoustic features and top-down attentional mechanisms. To disentangle this interplay, we previously developed dual-meter stimuli consisting of band-limited noise bursts that varied in center frequency and duration, with one feature following a triple-meter pattern and the other a quadruple-meter pattern. The perceived meter thus switches between the two by shifting attention from one acoustic feature to another, even when the physical stimulus remains identical. Using these stimuli, we investigated whether directing attention to specific acoustic features is associated with neural entrainment and anticipatory processing of the perceived metrical structure, and whether the former predicts the latter, by recording electroencephalogram (EEG) signals while isolating the effects of acoustic differences. We found that EEG spectral profiles shifted toward the metrical structure of the attended feature, and that the P300 component, an index of anticipatory processing, tended to be larger when the metrical structure was disrupted than when it remained intact, although both measures varied considerably across individuals. Critically, linear regression analysis revealed that participants whose neural entrainment more closely tracked the attended metrical structure exhibited significantly larger P300 responses to metrical violations. These findings suggest that attending to specific acoustic features links neural entrainment with anticipatory processing, which may underlie meter perception.

neuroscience↗

How does immediate auditory feedback coupled to locomotion influence the spontaneous actions of rats?

Sense of agency is a subjective experience that is difficult to examine in animals and preverbal infants. In animals and infants, the sensory monitoring of self-motion, which is the basis of this sense, and the contingency between self-motion and sensory feedback are investigated. Here, we performed experiments on rats using locomotor movements and auditory feedback of pulsed sounds with real-time changes in pulse interval corresponding to the velocity of locomotion, and tested whether rats change their locomotion depending on the degree of contingency between locomotion and auditory feedback. The results showed that rats increased their locomotion distance when the pulse interval of sound changed in accordance with the velocity of locomotion. However, this effect was not long-lasting. This study provides a simple and convenient method to examine the awareness of the contingency between self-motion and auditory feedback in a wide range of animal species without long-term training, and is expected to be a useful tool for comparisons with humans.

animal behavior and cognition↗

Beyond dichotomy: diversity of rat's ultrasonic vocalizations

Rats emit ultrasonic vocalizations (USVs) in diverse contexts, and these USVs are thought to serve many biological functions, such as socio-coordinating and alarming functions. In particular, rat USVs have been established as a good model for studying emotional expressions. Since the discovery of USVs in rats, it has gradually been revealed that two families of juvenile and adult rat USVs with distinct acoustic features are closely linked to different affective states: 50-kHz (high-short) calls are associated with positive affective states, whereas 22-kHz (low-long) calls are associated with negative affective states. Although various subtypes within high-short and low-long calls have been proposed and used, most studies adopt the dichotomous framework of first dividing USVs into high-short or low-long calls. The diversity of rat USVs may have been overlooked due to this high-short / low-long dichotomous framework, as such labeling could discourage reporting of actual measured acoustic properties. Considering that several recent studies claim to have found new USV categories outside this framework, we conducted a systematic survey of descriptions of rat USVs in the literature. We identified 15 articles reporting USVs that are outside the dichotomous framework. Our results support the existence of diverse USVs beyond the dichotomy, highlighting the importance of research on a broader range of vocalizations that might reflect complex affective states beyond the simple distinction between positive and negative.

animal behavior and cognition↗

Interval timing clock property in the rat granular retrosplenial cortex

The rodent granular retrosplenial cortex (gRSC), densely interconnected with the hippocampal formation and the anterior thalamic nuclei, plays an important role in learning and memory. We had revealed that small pyramidal neurons in the superficial layers of the rat gRSC exhibit late-spiking (LS) firing properties. It has been suggested that neural circuits containing LS neurons can encode time intervals on the order of seconds, known as "interval timing". To test the possibility that the rat gRSC is involved in the processing of interval timing, we employed a trace fear conditioning paradigm in which the conditioned stimulus (CS) and the unconditioned stimulus (US) were temporally separated. First, we examined the effect of cytotoxic lesions made in the RSC prior to trace fear conditioning. We found that intact rats exhibited freezing behavior after CS tone presentation, whereas lesioned rats did not exhibit such freezing behavior. Next, we conducted in vivo chronic or acute recordings of neural activity from the rat gRSC in a test session conducted one week after the conditioning. In both recordings, we observed a distinct spike activity in which there was a transient increase in the firing rate around the presentation of the CS tone, followed by a rapid suppression and then ramping activity (a gradual elevation of the firing rate) until the next CS presentation. This "ramping activity" is thought to be one way in which interval timing is represented in the brain. Post stimulus histogram analysis revealed the existence of ramping activity in the gRSC, which reached its peak at various time intervals after the onset of the CS tone. Interestingly, this activity was specifically observed in response to the CS tone but not to the non-CS tone. Moreover, in naive rat gRSC (no trace fear conditioning), no such ramping activity was observed. These results indicate that gRSC neurons can encode time information on the order of tens to hundreds of seconds, integrating incoming sensory input with past memory traces.

neuroscience↗

Familiarity modulates preference for joint feeding with conspecifics in rats

Rats are highly social mammals that form social groups of various sizes. Interestingly, they are known to show prosocial behaviors, and are socially tolerant of other conspecifics as they feed together, but the specificity of their prosociality has not been fully understood. Here, we investigated what degree rats showed social choice, i.e., preferential joint feeding even with unfamiliar animals by performing a simple feeding site choice task. In the task, subjects were tested to choose between the feeding site where they fed with other rats (social option) or the other site where they could feed alone (solitary option). The results showed that social option choices increased particularly when the partner was a single non-cagemate rat. This result means that high social preference for other individuals occurs spontaneously, even when they are feeding with unfamiliar non-cagemates. This high degree of social tolerance would lead to the suppression of aggressive behavior as well as enhancement of affiliative relationships even in situations when the rats met with unfamiliar conspecifics for the first time. HighlightsO_LIRats are highly socially tolerant mammals as they feed with conspecifics together. C_LIO_LIWe explored how the presence of conspecifics affects feeding site choices in rats. C_LIO_LISocial choices increased when the partners were non-cagemates. C_LIO_LISocial choices decreased as the number of non-cagemates increased. C_LIO_LIJoint feeding with a single non-cagemate is observed particularly frequently. C_LI

animal behavior and cognition↗

An exploratory study of behavioral traits and the establishment of social relationships in female laboratory rats

There is growing evidence that social relationships influence individual fitness through various effects. Clarifying individual differences in social interaction patterns and determinants for such differences will lead to better understanding of sociality and its fitness consequences for animals. Behavioral traits are considered one of the determining factors of social interaction. The purpose of this study was to explore the effects of individual behavioral traits on social relationship building in rats, a highly social species. Initially, the following behavioral characteristics were measured in individuals: tameness (glove test), activity (open field test), exploration (novel object test), sociability (three-chamber test), and boldness (elevated plus maze test). We then used DeepLabCut to behaviorally track three groups of four individuals (12 total) and analyze social behaviors such as approach and avoidance behaviors. Principal component analysis based on behavioral test results detected behavioral traits interpreted as related to exploration, boldness, activity, and tameness, but not sociability. In addition, behavioral tracking results showed consistent individual differences in social behavior indices such as isolation time and partner preference. Furthermore, we found that different components were correlated with different phases of social behavior; exploration and boldness were associated with the early stages of group formation, whereas activity was associated with later stages of relationship building. From these results, we derived hypothesize that personality traits related to the physical and social environment have a larger influence in the relationship formation phase, and the behavioral trait of activity becomes important in the maintenance phase of relationships. Future studies should examine this hypothesis by testing larger group sizes and ensuring there is no bias introduced into group composition.

animal behavior and cognition↗

Spectral consistency in sound sequence affects perceptual accuracy in discriminating subdivided rhythmic patterns

Musical compositions are distinguished by their unique rhythmic patterns, determined by subtle differences in how regular beats are subdivided. Precise perception of these subdivisions is essential for discerning nuances in rhythmic patterns. While musical rhythm typically comprises sound elements with a variety of timbres or spectral cues, the impact of such spectral variations on the perception of rhythmic patterns remains unclear. Here, we show that consistency in spectral cues affects perceptual accuracy in discriminating subdivided rhythmic patterns. We conducted online experiments using rhythmic sound sequences consisting of band-passed noise bursts to measure discrimination accuracy. Participants were asked to discriminate between a swing-like rhythm sequence, characterized by a 2:1 interval ratio, and its more or less exaggerated version. This task was also performed under two additional rhythm conditions: inversed-swing rhythm (1:2 ratio) and regular subdivision (1:1 ratio). The center frequency of the band noises was either held constant or alternated between two values. Our results revealed a significant decrease in discrimination accuracy when the center frequency was alternated, irrespective of the rhythm ratio condition. This suggests that rhythm perception is not only shaped by temporal structure but also affected by spectral properties.

neuroscience↗

Dopaminergic neurons dynamically update sensory values during navigation

Updating the value of sensory cues through experiences is a critical element of adaptive behavior. Although dopaminergic neurons (DANs) achieve this by driving associative learning, whether they contribute to assessment of sensory values outside the context of association remains largely unexplored. Here we show in Drosophila that DANs in the mushroom body encode the innate value of odors and constantly update the current value by inducing plasticity during olfactory navigation. Simulation of neuronal activity in a network based on the connectome data reproduced the characteristics of DAN responses, proposing a concrete circuit mechanism for computation. Notably, odors alone induced value- and dopamine-dependent changes in the activity of mushroom body output neurons, which store the current value of odors, as well as the behavior of flies steering in a virtual environment. Thus, the DAN circuit known for discrete, associative learning also continuously updates odor values during navigation in a non-associative manner.

neuroscience↗

Discrimination of conspecific head orientations and learning set formation in Bengalese finches

Animals detect others gaze direction, such as predators, prey, and courtship mates, to enable adaptive behavior. However, head movements play a more significant role in gaze shifts in birds than eye movement because of the flat eye shape. Additionally, most birds with laterally placed eyes usually turn the lateral face to the target. Therefore, we used Bengalese finches to examine whether songbirds can discriminate between conspecific frontal and lateral faces and divide head orientations in different angles into two categories. In experiments, birds were trained by operant conditioning to discriminate stimuli consisting of conspecific frontal and lateral head images. Eight out of nine birds finished discrimination training and test sessions. The results indicate that Bengalese finches can discriminate gaze direction by the head orientations. Furthermore, as the number of stimuli set increased, fewer trials were needed to achieve the criteria, which suggests that birds have developed a learning set during the training. However, we did not find a clear discrimination boundary for head orientation categorization.

animal behavior and cognition↗

Female Bengalese finches recognize their fathers song as sexually attractive

Birdsong is an important communication signal used in mate choice. In some songbirds, only males produce songs while females do not. Female birds are sensitive to inter- and intra-species song variation. Some aspects of female song preference depend on developmental experiences. For example, in Bengalese finches and zebra finches, adult females prefer the song to which they were exposed early in life, such as the fathers song. However, it is unclear whether such song preference in females is sexually motivated. The purpose of our study is to test if female Bengalese finches recognize their fathers song as sexually attractive. We measured copulation solicitation displays during playbacks of the fathers song vs. unfamiliar conspecific songs and found that across individuals, the fathers song elicited more displays than other songs. In addition, we analyzed if a birds response to a given song could be predicted by the level of similarity of that song to the fathers song. The results suggest that preference for the fathers song in this species is actually relevant to mate choice. Although more precise control is necessary in future studies to elucidate the process of preference development, our results imply the significance of early-life experience in shaping female song preference.

animal behavior and cognition↗

Arousal-dependent auditory response in the brain of Bengalese finches as measured by gene expression

Songbirds use auditory feedback to maintain their own songs. Juveniles also memorize a tutor song and use memory as a template to make up their own songs through auditory feedback. A recent electrophysiological study revealed that HVC neurons respond to BOS playback only in low arousal, sleeping, or anesthetized conditions. One outstanding question is how does auditory suppression occur in the brain? Here, we determined how arousal affects auditory responses simultaneously in the whole brain and over the song neural circuit in Bengalese finches, using the immediate early gene egr-1 as a marker of neural activity. Our results showed that auditory responses in the low-arousal state were less susceptible to gating, which was also confirmed by gene expression, and that the suppression may be weaker than observed in previous zebra finch studies. This may be because the Bengalese finch is a domesticated species. In addition, our results suggest that information may flow from the MLd.I of the midbrain to higher auditory regions. Altogether, this study presents a new attempt to explore the auditory suppression network by simultaneously investigating the whole brain using molecular biology methods.

neuroscience↗

Effects of domestication on neophobia: A comparison between the domesticated Bengalese finch (Lonchura striata var. domestica) and its wild ancestor, the white-rumped munia (Lonchura striata)

Bengalese finches (Lonchura striata var. domestica) have more complex song traits than their wild ancestors, white-rumped munias (Lonchura striata). Domesticated finches are likely able to allocate more resources to song development rather than allocating resources to mechanisms aimed at coping with predation, which are no longer needed under domesticated conditions. Here, we aimed to examine the effects of changes in selection pressure due to domestication on the behaviour of Bengalese finches and to contemplate the possible evolutionary mechanisms underlying these changes. To do so, we compared neophobic responses to novel-object conditions as an assessment of reactions to potential predators. We studied groups of Bengalese finches and white-rumped munias and found that Bengalese finches were more likely to eat the food provided to them under novel-object conditions. Bengalese finches had a shorter latency time to eat, and this latency time was less affected by the novel object in the case of Bengalese finches compared to white-rumped munias. Therefore, Bengalese finches have reduced neophobic responses due to domestication. The behavioural strategies of white-rumped munias appear to be more suitable for natural environments, which include unpredictable risks, whereas Bengalese finches have likely adapted their behaviour to the conditions of artificial selection.

animal behavior and cognition↗

Decreased synthesis and variable gene transcripts of oxytocin in a domesticated avian species

The Bengalese finch was domesticated more than 250 years ago from the wild white-rumped munia. Similar to other domesticated species, Bengalese finches show a reduced fear response and have lower corticosterone levels, compared to white-rumped munias. Bengalese finches and munias also have different song types. Since oxytocin (OT) has been found to be involved in stress coping and auditory processing, we tested whether the OT sequence and brain expression pattern and content differ in wild munias and domesticated Bengalese finches. We identified intra-strain variability in the untranslated regions of the OT sequence in Bengalese finches in comparison to the munia OT. Several of these changes fall in specific transcription factor binding sites, which show either a conserved or a relaxed evolutionary trend in the avian lineage, and in vertebrates in general. Although in situ hybridization in several hypothalamic nuclei did not reveal significant differences in the number of cells expressing OT between the two strains, real-time quantitative PCR showed significantly lower OT mRNA expression in the diencephalon of the Bengalese finches relative to munias. Our study thus points to a decreased OT synthesis in the domestic strain compared with the wild strain in birds. This is an opposite pattern from that found in some domesticated mammals, suggesting that different processes of OT function might have occurred in mammals and birds under domestication.

neuroscience↗

Domestication effects on aggressiveness: Comparison of biting motivation and bite force between wild and domesticated finches

Domesticated animals evolve unique traits, known as domestication phenotypes or the domestication syndrome, due to their adaptation to a captive environment and changes in selection pressures. After being tamed, the Bengalese finch (Lonchura striata var. domestica) has undergone behavioural and physiological trait changes that differ from those of its wild ancestor, the white-rumped munia (Lonchura striata). The Bengalese finch has complex songs, lower fear response, and lower corticosterone levels than those in the white-rumped munia. We hypothesized that domesticated finches increase the effort to reproduce in lieu of maintaining fitness for survival as needed in the wild. Aggressiveness and bite performance affect survival rates and reproductive success, and are good indicators of adaptability in the natural environment. Therefore, we compared the aggressiveness and biting force of white-rumped munias with those of Bengalese finches to explore the evolutionary mechanisms of behavioural changes due to domestication. We found that the Bengalese finch had decreased aggressiveness (incidence of aggressive biting birds and the number of bite responses) and bite force than those in the white-rumped munia due to domestication. Therefore, we believe they could allocate more resources for breeding that would otherwise be needed for coping with predators through aggression.

animal behavior and cognition↗

Domestication effects on immune response: comparison of cell-mediated immune competence in wild and domesticated Bengalese finch

Domesticated Bengalese finch (Lonchura striata var. domestica) lack natural selection pressures and consequently have more complex songs and altered behavioural and psychological traits when compared to their wild ancestor, the white-rumpud munia (Lonchura striata). Clarifying the sexual traits and life history trade-offs in Bengal finches will be help to improve our understanding of the evolution of complex songs and domesticated traits. Here, we have assessed the immune competence of the Bengalese finch and the white-rumped munia using phytohemagglutinin (PHA) tests to create an index of cell-mediated immune responses. We found that the Bengalese finch had a significantly larger immunocompetence than the white-rumped munia, indicating that they devote more resources to both immunity and reproduction. Thus, there is no trade-off but a positive relationship between immunocompetence and reproductive traits, which may be related to the release from natural selection pressures. These results will be useful in understanding the mechanisms by which domestication-induced changes due to a lack of natural selection pressure affect behavioural and physiological changes.

zoology↗