Pub Date : 2024-08-30DOI: 10.1101/2024.08.29.609864
Josh J Arbon, Noa Truskanov, Emily Stott, Guillam E McIvor, Alex Thornton
Social tolerance is crucial in facilitating the evolution of cooperation and social cognition, but it is unknown whether animals can optimise their social tolerance through learning. We presented wild jackdaws (Corvus monedula) with a novel social information problem using automated feeders: to access food, adults had to inhibit their tendency to displace juveniles and instead show tolerance by occupying an adjacent perch. Adults learned to tolerate juveniles, generalising across juveniles as a cohort and in an unrewarded context, demonstrating learning of a new information-use strategy.
{"title":"Wild jackdaws learn social tolerance to exploit new information","authors":"Josh J Arbon, Noa Truskanov, Emily Stott, Guillam E McIvor, Alex Thornton","doi":"10.1101/2024.08.29.609864","DOIUrl":"https://doi.org/10.1101/2024.08.29.609864","url":null,"abstract":"Social tolerance is crucial in facilitating the evolution of cooperation and social cognition, but it is unknown whether animals can optimise their social tolerance through learning. We presented wild jackdaws (Corvus monedula) with a novel social information problem using automated feeders: to access food, adults had to inhibit their tendency to displace juveniles and instead show tolerance by occupying an adjacent perch. Adults learned to tolerate juveniles, generalising across juveniles as a cohort and in an unrewarded context, demonstrating learning of a new information-use strategy.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"21 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211768","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-30DOI: 10.1101/2024.08.29.610243
Leo CLEMENT, Sebastian Schwarz, Antoine Wystrach
Desert ants are excellent navigators. Each individual learns long foraging routes meandering between the trees and bushes in their natural habitat. It is well-known how the insect brain memorizes and recognizes views, and how this recognition can guide their way. However, little is known about the rule that guide spatial learning in the first place. Here we recorded the paths of desert ants navigating in their natural habitat under various displacement conditions. We demonstrate that ants learn continuously the routes they travel and memorize them in one trial, without the need for reward or punishment, and even if these routes are meandering and do not lead to places of interest: a concept called "latent learning", which is typically associated with the formation of map-like representation in vertebrates. Yet, the failure of ants to solve simple artificial navigation tasks -even with the goal being clearly visible- reveals that they relied on egocentric visual memories without map-like representation of the surrounding space. Our results unveil the rules governing the formation and recall of latent memories. A model shows that it can be implemented in the insect's Mushroom bodies brain area through dynamic interactions between short- and long-lasting memories.
{"title":"Latent learning without map-like representation of space in navigating ants","authors":"Leo CLEMENT, Sebastian Schwarz, Antoine Wystrach","doi":"10.1101/2024.08.29.610243","DOIUrl":"https://doi.org/10.1101/2024.08.29.610243","url":null,"abstract":"Desert ants are excellent navigators. Each individual learns long foraging routes meandering between the trees and bushes in their natural habitat. It is well-known how the insect brain memorizes and recognizes views, and how this recognition can guide their way. However, little is known about the rule that guide spatial learning in the first place. Here we recorded the paths of desert ants navigating in their natural habitat under various displacement conditions. We demonstrate that ants learn continuously the routes they travel and memorize them in one trial, without the need for reward or punishment, and even if these routes are meandering and do not lead to places of interest: a concept called \"latent learning\", which is typically associated with the formation of map-like representation in vertebrates. Yet, the failure of ants to solve simple artificial navigation tasks -even with the goal being clearly visible- reveals that they relied on egocentric visual memories without map-like representation of the surrounding space. Our results unveil the rules governing the formation and recall of latent memories. A model shows that it can be implemented in the insect's Mushroom bodies brain area through dynamic interactions between short- and long-lasting memories.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"46 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211776","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-30DOI: 10.1101/2024.08.30.610446
Veronika A. Rohr-Bender, Krisztina Kupan, Guadalupe Lopez-Nava, Wolfgang Forstmeier, Anne Hertel, Vitali Razumov, Katrin Martin, Bart Kempenaers, Clemens Kuepper
Intraspecific variation provides the substrate for the evolution of organisms. Ruffs show exceptional phenotypic variation in physiology, appearance and behaviour linked to variation between sexes and male alternative reproductive tactics (ARTs). The male ARTs are associated with the evolution of separate morphs, which are encoded by an autosomal supergene. However, the effects of the supergene on females and chicks are much less well understood. In particular, it is still unknown, whether females also show morph-specific behavioural variation, when behavioural differences emerge during ontogeny, and whether behavioural differences can be detected outside of the breeding context. To address these knowledge gaps, we repeatedly measured the activity in an unfamiliar environment, also known as exploration behaviour, of 109 hand-raised young ruffs throughout their first two years of life. We used automated tracking in an open field arena, and quantified the distance moved within 10 minutes to examine behavioural differences between sexes, morphs and individuals. The activity of young ruffs rapidly increased during the first month after their crouching reflex, a response to potential threats, subsided. Repeatability of individual activity was initially low but increased throughout juvenile ontogeny and was high (R = 0.5) from day 21 onwards. Variation in activity was clearly sex-linked with females moving more than males, indicating potential energetic trade-offs accompanying the strong sexual size dimorphism. In contrast, morph differences in activity remained inconsistent and elusive, both in females and in males. Our results indicate that in species where much of the known behavioural variation is linked to mating tactics, a non-reproductive behaviour can show between-individual variation and clear sex differences, whereas morph differences appear less pronounced.
{"title":"Sex and morph variation in activity from early ontogeny to maturity in ruffs (Calidris pugnax)","authors":"Veronika A. Rohr-Bender, Krisztina Kupan, Guadalupe Lopez-Nava, Wolfgang Forstmeier, Anne Hertel, Vitali Razumov, Katrin Martin, Bart Kempenaers, Clemens Kuepper","doi":"10.1101/2024.08.30.610446","DOIUrl":"https://doi.org/10.1101/2024.08.30.610446","url":null,"abstract":"Intraspecific variation provides the substrate for the evolution of organisms. Ruffs show exceptional phenotypic variation in physiology, appearance and behaviour linked to variation between sexes and male alternative reproductive tactics (ARTs). The male ARTs are associated with the evolution of separate morphs, which are encoded by an autosomal supergene. However, the effects of the supergene on females and chicks are much less well understood. In particular, it is still unknown, whether females also show morph-specific behavioural variation, when behavioural differences emerge during ontogeny, and whether behavioural differences can be detected outside of the breeding context. To address these knowledge gaps, we repeatedly measured the activity in an unfamiliar environment, also known as exploration behaviour, of 109 hand-raised young ruffs throughout their first two years of life. We used automated tracking in an open field arena, and quantified the distance moved within 10 minutes to examine behavioural differences between sexes, morphs and individuals. The activity of young ruffs rapidly increased during the first month after their crouching reflex, a response to potential threats, subsided. Repeatability of individual activity was initially low but increased throughout juvenile ontogeny and was high (R = 0.5) from day 21 onwards. Variation in activity was clearly sex-linked with females moving more than males, indicating potential energetic trade-offs accompanying the strong sexual size dimorphism. In contrast, morph differences in activity remained inconsistent and elusive, both in females and in males. Our results indicate that in species where much of the known behavioural variation is linked to mating tactics, a non-reproductive behaviour can show between-individual variation and clear sex differences, whereas morph differences appear less pronounced.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"79 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211777","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-30DOI: 10.1101/2024.08.29.610309
Georgia Sandars, Jake Stephen Brooker, Zanna Clay
Behavioural contagion—the onset of a species-typical behaviour soon after witnessing it in a conspecific—forms the foundation of behavioural synchrony and cohesive group living in social animals. Although past research has mostly focused on negative emotions or neutral contexts, the sharing of positive emotions in particular may be key for social affiliation. We investigated the contagion of two socially affiliative interactive behaviours, grooming and play, in chimpanzees. We collected naturalistic observations of N = 41 sanctuary-living chimpanzees at Chimfunshi Wildlife Orphanage, conducting focal follows of individuals following observations of a grooming or play bout, compared with matched controls. We then tested whether the presence and latency of behavioural contagion was influenced by age, sex, rank, and social closeness. Our results offer evidence for the presence of grooming and play contagion in sanctuary-living chimpanzees. Grooming contagion appeared to be influenced by social closeness, whilst play contagion was more pronounced in younger individuals. These findings emphasise that contagion is not restricted to negatively valenced or self-directed behaviours, and that the predictors of contagious behaviour are highly specific to the behaviour and species in question. Examining the factors that influence this foundational social process contributes to theories of affective state matching and is key for understanding social bonding and group dynamics.
行为传染--在目睹同种动物的典型行为后很快就会出现这种行为--是社会动物行为同步和群体生活凝聚力的基础。尽管过去的研究大多集中在负面情绪或中性环境上，但积极情绪的分享尤其可能是社会归属的关键。我们研究了黑猩猩梳理毛发和玩耍这两种具有社会归属感的互动行为的传染性。我们在长峰市野生动物孤儿院对 N = 41 只生活在庇护所的黑猩猩进行了自然观察，在观察到黑猩猩梳理毛发或玩耍后对其进行了重点跟踪，并与匹配的对照组进行了比较。然后，我们测试了行为传染的存在和潜伏期是否受年龄、性别、等级和社会亲密度的影响。我们的研究结果为在庇护所生活的黑猩猩中存在梳理和玩耍传染提供了证据。梳理传染似乎受社会亲近度的影响，而游戏传染在年轻个体中更为明显。这些发现强调，传染并不局限于负价值或自我导向的行为，而且传染行为的预测因素与相关行为和物种密切相关。研究影响这一基本社会过程的因素有助于情感状态匹配理论的发展，也是理解社会联系和群体动力的关键。
{"title":"ChimpanSEE, ChimpanDO: Grooming and play contagion in chimpanzees","authors":"Georgia Sandars, Jake Stephen Brooker, Zanna Clay","doi":"10.1101/2024.08.29.610309","DOIUrl":"https://doi.org/10.1101/2024.08.29.610309","url":null,"abstract":"Behavioural contagion—the onset of a species-typical behaviour soon after witnessing it in a conspecific—forms the foundation of behavioural synchrony and cohesive group living in social animals. Although past research has mostly focused on negative emotions or neutral contexts, the sharing of positive emotions in particular may be key for social affiliation. We investigated the contagion of two socially affiliative interactive behaviours, grooming and play, in chimpanzees. We collected naturalistic observations of <em>N</em> = 41 sanctuary-living chimpanzees at Chimfunshi Wildlife Orphanage, conducting focal follows of individuals following observations of a grooming or play bout, compared with matched controls. We then tested whether the presence and latency of behavioural contagion was influenced by age, sex, rank, and social closeness. Our results offer evidence for the presence of grooming and play contagion in sanctuary-living chimpanzees. Grooming contagion appeared to be influenced by social closeness, whilst play contagion was more pronounced in younger individuals. These findings emphasise that contagion is not restricted to negatively valenced or self-directed behaviours, and that the predictors of contagious behaviour are highly specific to the behaviour and species in question. Examining the factors that influence this foundational social process contributes to theories of affective state matching and is key for understanding social bonding and group dynamics.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"23 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211770","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The Zebra finch is a well-studied animal for studying neural mechanisms of speech, and electrophysiology is the primary technique for understanding the song system in them. Most of the studies on zebra finches have focused on intracerebral recordings. However, these methods are only affordable for limited laboratories. Recently, different open-source hardware for acquiring EEG signals has been developed. It is unclear whether these solutions suit zebra finch studies as they have not been evaluated. Electrocorticography signals can provide a preliminary guide for more in-depth inquiries and also aid in understanding the global behavior of the bird's brain, as opposed to the more common localized approach. We provide a detailed protocol for acquiring iEEG data from zebra finches with an open-source device. We implemented stainless steel electrodes on the brain's surface and recorded the brain signals from two recording sites. To validate our method, we ran two different experiments. In the first experiment, we recorded neural activity under various concentrations of isoflurane and extracted the suppression duration to measure anesthesia depth. In the second experiment, we head-fixed the birds and presented them with different auditory stimuli to evaluate event-related potential (ERP). Results showed a significant increase in the suppression duration by increasing the anesthesia depth and evident ERP response to auditory stimuli. These findings indicate that by our methodology, we can successfully collect iEEG signals from awake and anesthetized birds. These findings pave the way for future studies to use iEEG to investigate bird cognition.
{"title":"An affordable solution for investigating zebra finch intracranial electroencephalography (iEEG) signals","authors":"Mohammad-Mahdi Abolghasemi, Shahriar Rezghi Shirsavar, Milad Yekani","doi":"10.1101/2024.08.29.610238","DOIUrl":"https://doi.org/10.1101/2024.08.29.610238","url":null,"abstract":"The Zebra finch is a well-studied animal for studying neural mechanisms of speech, and electrophysiology is the primary technique for understanding the song system in them. Most of the studies on zebra finches have focused on intracerebral recordings. However, these methods are only affordable for limited laboratories. Recently, different open-source hardware for acquiring EEG signals has been developed. It is unclear whether these solutions suit zebra finch studies as they have not been evaluated. Electrocorticography signals can provide a preliminary guide for more in-depth inquiries and also aid in understanding the global behavior of the bird's brain, as opposed to the more common localized approach. We provide a detailed protocol for acquiring iEEG data from zebra finches with an open-source device. We implemented stainless steel electrodes on the brain's surface and recorded the brain signals from two recording sites. To validate our method, we ran two different experiments. In the first experiment, we recorded neural activity under various concentrations of isoflurane and extracted the suppression duration to measure anesthesia depth. In the second experiment, we head-fixed the birds and presented them with different auditory stimuli to evaluate event-related potential (ERP). Results showed a significant increase in the suppression duration by increasing the anesthesia depth and evident ERP response to auditory stimuli. These findings indicate that by our methodology, we can successfully collect iEEG signals from awake and anesthetized birds. These findings pave the way for future studies to use iEEG to investigate bird cognition.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"11 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142226688","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-30DOI: 10.1101/2024.08.30.610458
Oceane La Loggia, Diogo F. Antunes, Nadia Aubin-Horth, Barbara Taborsky
In social species, early social experience shapes the development of appropriate social behaviours during conspecific interactions referred to as social competence. However, the underlying neuronal mechanisms responsible for the acquisition of social competence are largely unknown. One key candidate to influence social competence is neuroplasticity, which functions to restructure neural networks in response to novel experiences or alterations of the environment. One important mediator of this restructuring is the neurotrophin BDNF, which is well conserved among vertebrates. We studied the highly social fish Neolamprologus pulcher, in which the impact of early social experience on social competence has been previously shown. We investigated experimentally how variation of the early social environment impacts markers of neuroplasticity by analysing the relative expression of the bdnf gene and its receptors p75NTR and TrkB across nodes of the Social Decision-Making Network. In fish raised in larger groups, bdnf and TrkB were upregulated in the anterior tuberal nucleus, compared to fish raised in smaller groups, while TrkB was downregulated and bdnf was upregulated in the lateral part of the dorsal telencephalon. In the preoptic area (POA), all three genes were upregulated in fish raised in large groups, suggesting that early social experiences might lead to changes of the neuronal connectivity in the POA. Our results highlight the importance of the early social experience in programming the constitutive expression of neuroplasticity markers, suggesting that the effects of early social experience on social competence might be due to changes in neuroplasticity.
{"title":"Social complexity during early development has long-term effects on neuroplasticity in the social decision-making network","authors":"Oceane La Loggia, Diogo F. Antunes, Nadia Aubin-Horth, Barbara Taborsky","doi":"10.1101/2024.08.30.610458","DOIUrl":"https://doi.org/10.1101/2024.08.30.610458","url":null,"abstract":"In social species, early social experience shapes the development of appropriate social behaviours during conspecific interactions referred to as social competence. However, the underlying neuronal mechanisms responsible for the acquisition of social competence are largely unknown. One key candidate to influence social competence is neuroplasticity, which functions to restructure neural networks in response to novel experiences or alterations of the environment. One important mediator of this restructuring is the neurotrophin BDNF, which is well conserved among vertebrates. We studied the highly social fish Neolamprologus pulcher, in which the impact of early social experience on social competence has been previously shown. We investigated experimentally how variation of the early social environment impacts markers of neuroplasticity by analysing the relative expression of the bdnf gene and its receptors p75NTR and TrkB across nodes of the Social Decision-Making Network. In fish raised in larger groups, bdnf and TrkB were upregulated in the anterior tuberal nucleus, compared to fish raised in smaller groups, while TrkB was downregulated and bdnf was upregulated in the lateral part of the dorsal telencephalon. In the preoptic area (POA), all three genes were upregulated in fish raised in large groups, suggesting that early social experiences might lead to changes of the neuronal connectivity in the POA. Our results highlight the importance of the early social experience in programming the constitutive expression of neuroplasticity markers, suggesting that the effects of early social experience on social competence might be due to changes in neuroplasticity.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"20 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211769","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-30DOI: 10.1101/2024.08.29.610359
Carlos Alan Velazquez Vargas, Jordan A. Taylor
Many skills that humans acquire throughout their lives, such as playing video games or sports, require substantial motor learning and multi-step planning. While both processes are typically studied separately, they are likely to interact during the acquisition of complex motor skills. In this work, we studied this interaction by assessing human performance in a sequential decision-making task that requires the learning of a non-trivial motor mapping. Participants were tasked to move a cursor from start to target locations in a grid world, using a standard keyboard. Notably, the specific keys were arbitrarily mapped to a movement rule resembling the Knight chess piece. In Experiment 1, we showed the learning of this mapping in the absence of planning, led to significant improvements in the task when presented with sequential decisions at a later stage. Computational modeling analysis revealed that such improvements resulted from an increased learning rate about the state transitions of the motor mapping, which also resulted in more flexible planning from trial to trial (less perseveration or habitual responses). In Experiment 2, we showed that incorporating mapping learning into the planning process, allows us to capture (1) differential task improvements for distinct planning horizons and (2) overall lower performance for longer horizons. Additionally, model analysis suggested that participants may limit their search to three steps ahead. We hypothesize that this limitation in planning horizon arises from capacity constraints in working memory, and may be the reason complex skills are often broken down into individual subroutines or components during learning.
{"title":"Learning to Move and Plan like the Knight: Sequential Decision Making with a Novel Motor Mapping","authors":"Carlos Alan Velazquez Vargas, Jordan A. Taylor","doi":"10.1101/2024.08.29.610359","DOIUrl":"https://doi.org/10.1101/2024.08.29.610359","url":null,"abstract":"Many skills that humans acquire throughout their lives, such as playing video games or sports, require substantial motor learning and multi-step planning. While both processes are typically studied separately, they are likely to interact during the acquisition of complex motor skills. In this work, we studied this interaction by assessing human performance in a sequential decision-making task that requires the learning of a non-trivial motor mapping. Participants were tasked to move a cursor from start to target locations in a grid world, using a standard keyboard. Notably, the specific keys were arbitrarily mapped to a movement rule resembling the Knight chess piece. In Experiment 1, we showed the learning of this mapping in the absence of planning, led to significant improvements in the task when presented with sequential decisions at a later stage. Computational modeling analysis revealed that such improvements resulted from an increased learning rate about the state transitions of the motor mapping, which also resulted in more flexible planning from trial to trial (less perseveration or habitual responses). In Experiment 2, we showed that incorporating mapping learning into the planning process, allows us to capture (1) differential task improvements for distinct planning horizons and (2) overall lower performance for longer horizons. Additionally, model analysis suggested that participants may limit their search to three steps ahead. We hypothesize that this limitation in planning horizon arises from capacity constraints in working memory, and may be the reason complex skills are often broken down into individual subroutines or components during learning.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"62 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142227922","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-29DOI: 10.1101/2024.08.28.610140
Mohsen Parto-Dezfouli, M Isabel Vanegas, Mohammad Zarei, William H. Nesse, Kelsey L. Clark, Behrad Noudoost
In order to understand how prefrontal cortex provides the benefits of working memory (WM) for visual processing we examined the influence of WM on the representation of visual signals in V4 neurons in two macaque monkeys. We found that WM induces strong β oscillations in V4 and that the timing of action potentials relative to this oscillation reflects sensory information- i.e., a phase coding of visual information. Pharmacologically inactivating the Frontal Eye Field part of prefrontal cortex, we confirmed the necessity of prefrontal signals for the WM-driven boost in phase coding of visual information. Indeed, changes in the average firing rate of V4 neurons could be accounted for by WM-induced oscillatory changes. We present a network model to describe how WM signals can recruit sensory areas primarily by inducing oscillations within these areas and discuss the implications of these findings for a sensory recruitment theory of WM through coherence.
{"title":"Prefrontal working memory signal primarily controls phase-coded information within extrastriate cortex","authors":"Mohsen Parto-Dezfouli, M Isabel Vanegas, Mohammad Zarei, William H. Nesse, Kelsey L. Clark, Behrad Noudoost","doi":"10.1101/2024.08.28.610140","DOIUrl":"https://doi.org/10.1101/2024.08.28.610140","url":null,"abstract":"In order to understand how prefrontal cortex provides the benefits of working memory (WM) for visual processing we examined the influence of WM on the representation of visual signals in V4 neurons in two macaque monkeys. We found that WM induces strong β oscillations in V4 and that the timing of action potentials relative to this oscillation reflects sensory information- i.e., a phase coding of visual information. Pharmacologically inactivating the Frontal Eye Field part of prefrontal cortex, we confirmed the necessity of prefrontal signals for the WM-driven boost in phase coding of visual information. Indeed, changes in the average firing rate of V4 neurons could be accounted for by WM-induced oscillatory changes. We present a network model to describe how WM signals can recruit sensory areas primarily by inducing oscillations within these areas and discuss the implications of these findings for a sensory recruitment theory of WM through coherence.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"52 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211773","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-29DOI: 10.1101/2024.08.28.610197
Will Sowersby, Taiga Kobayahsi, Satoshi Awata, Shumpei Sogawa, Masanori Kohda
Sleep is ubiquitous across animal taxa. Strong evolutionary pressures have conserved sleep over the evolutionary history of animals, yet our understanding of the functions of sleep still largely derives from mammals and select laboratory models. Sleep is considered to play an important role in mental processes, including learning and memory consolidation, but how widespread this relationship occurs across taxa remains unclear. Here, we test the impact of sleep disruption on the ability of the cleaner fish (Labroides dimidiatus) to both learn and then remember a novel cognitive task. We found a significant negative relationship between sleep disruption and the ability to learn a food reward choice system. Specifically, we found that fish in a disturbed sleep treatment took significantly longer and made more incorrect decisions when finding the food reward, compared to individuals in a non-disturbed/normal sleep treatment. In contrast, the differences between the two treatment groups were non-significant when fish where tasked with remembering the food reward several days later. Our results demonstrate a negative impact of sleep disruption on performance in a cognitive challenging task and that the effects were strongest when fish were first exposed to the challenge. Importantly, we show that the association between sleep and mental processes, such as learning, may be widespread across vertebrate taxa and potentially have an early origin in the evolutionary history of animals.
{"title":"The influence of sleep disruption on learning and memory in fish","authors":"Will Sowersby, Taiga Kobayahsi, Satoshi Awata, Shumpei Sogawa, Masanori Kohda","doi":"10.1101/2024.08.28.610197","DOIUrl":"https://doi.org/10.1101/2024.08.28.610197","url":null,"abstract":"Sleep is ubiquitous across animal taxa. Strong evolutionary pressures have conserved sleep over the evolutionary history of animals, yet our understanding of the functions of sleep still largely derives from mammals and select laboratory models. Sleep is considered to play an important role in mental processes, including learning and memory consolidation, but how widespread this relationship occurs across taxa remains unclear. Here, we test the impact of sleep disruption on the ability of the cleaner fish (Labroides dimidiatus) to both learn and then remember a novel cognitive task. We found a significant negative relationship between sleep disruption and the ability to learn a food reward choice system. Specifically, we found that fish in a disturbed sleep treatment took significantly longer and made more incorrect decisions when finding the food reward, compared to individuals in a non-disturbed/normal sleep treatment. In contrast, the differences between the two treatment groups were non-significant when fish where tasked with remembering the food reward several days later. Our results demonstrate a negative impact of sleep disruption on performance in a cognitive challenging task and that the effects were strongest when fish were first exposed to the challenge. Importantly, we show that the association between sleep and mental processes, such as learning, may be widespread across vertebrate taxa and potentially have an early origin in the evolutionary history of animals.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"94 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211771","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-08-29DOI: 10.1101/2024.08.28.610088
Kota Yamada, Hiroshi Matsui, Koji Toda
Curiosity encourages agents to explore their environment, leading to learning opportunities. Although psychology and neurobiology have tackled how external rewards control behavior, how intrinsic factors control behavior remains unclear. An extinction burst is a behavioral phenomenon in which a sudden increase in the frequency of a behavior immediately follows the omission of a reward. Although the extinction burst is textbook knowledge in psychology, there is little empirical evidence of it in experimental situations. In this study, we show that the extinction burst can be explained by curiosity by combining computational modeling of behavior and empirical demonstrations in mice. First, we built a reinforcement learning model incorporating curiosity, defined as expected reward prediction errors, and the model additively controlled the agent's behavior to the primary reward. Simulations revealed that the curiosity-driven reinforcement learning model produced an extinction burst and burst intensity depended on the reward probability. Second, we established a behavioral procedure that captured extinction bursts in an experimental setup using mice. We conducted an operant conditioning task with head-fixed mice, in which the reward followed after pressing a lever at a given probability. After the training sessions, we occasionally withheld the reward delivery when the mice performed the task. We found that phasic bursts of responses occurred immediately after reward omission when responses were rewarded with a high probability, suggesting that the magnitude of reward prediction errors controlled the burst. These results provide theoretical and experimental evidence that intrinsic factors control behavior in adapting to an ever-changing environment.
{"title":"Extinction burst could be explained by curiosity-driven reinforcement learning","authors":"Kota Yamada, Hiroshi Matsui, Koji Toda","doi":"10.1101/2024.08.28.610088","DOIUrl":"https://doi.org/10.1101/2024.08.28.610088","url":null,"abstract":"Curiosity encourages agents to explore their environment, leading to learning opportunities. Although psychology and neurobiology have tackled how external rewards control behavior, how intrinsic factors control behavior remains unclear. An extinction burst is a behavioral phenomenon in which a sudden increase in the frequency of a behavior immediately follows the omission of a reward. Although the extinction burst is textbook knowledge in psychology, there is little empirical evidence of it in experimental situations. In this study, we show that the extinction burst can be explained by curiosity by combining computational modeling of behavior and empirical demonstrations in mice. First, we built a reinforcement learning model incorporating curiosity, defined as expected reward prediction errors, and the model additively controlled the agent's behavior to the primary reward. Simulations revealed that the curiosity-driven reinforcement learning model produced an extinction burst and burst intensity depended on the reward probability. Second, we established a behavioral procedure that captured extinction bursts in an experimental setup using mice. We conducted an operant conditioning task with head-fixed mice, in which the reward followed after pressing a lever at a given probability. After the training sessions, we occasionally withheld the reward delivery when the mice performed the task. We found that phasic bursts of responses occurred immediately after reward omission when responses were rewarded with a high probability, suggesting that the magnitude of reward prediction errors controlled the burst. These results provide theoretical and experimental evidence that intrinsic factors control behavior in adapting to an ever-changing environment.","PeriodicalId":501210,"journal":{"name":"bioRxiv - Animal Behavior and Cognition","volume":"10 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142211778","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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