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Neurobehavioural and molecular mechanisms of social learning in zebrafish
Dissertation presented to obtain the Ph.D. degree in
Behavioural Biology, presented at ISPA â Instituto UniversitĂĄrio in
the year of 2019Os animais utilizam informação social e não social para tomarem decisÔes adaptativas que
tem impacto no seu fitness. O uso de informação social traz vantagens como escapar a um predador,
encontrar fontes de comida ou evitar lutas com indivĂduos mais fortes, apenas por observação dos
seus conspecĂficos ou produtos relacionados com eles. A aprendizagem social ocorre quando os
indivĂduos observam o comportamento de outros ou as suas consequĂȘncias para modificar o seu
próprio comportamento. Esta estratégia comportamental é conservada entre espécies: os grilos,
Nemobius sylvestris, adaptam o seu comportamento para evitar um predador depois de observar o
comportamento de outros e mantem essas mudanças comportamentais, duradouramente, mesmo
apos os demonstradores nĂŁo estarem presentes; as abelhas operĂĄrias, Apis Mellifera, apresentam
uma série de comportamentos motores estereotipados que informam outras operårias da localização
precisa de uma fonte de comida.
Os mecanismos neuronais da aprendizagem social nĂŁo estĂŁo claramente compreendidos, e
são o centro de debate nesta årea de investigação. Alguns autores hipotetizam que os mecanismos
neurais da aprendizagem social sĂŁo partilhados, e outros autores defendem que a aprendizagem
social Ă© um domĂnio geral presente atĂ© em espĂ©cies solitĂĄrias.
O principal objetivo deste trabalho Ă© clarificar os mecanismos subjacentes a aprendizagem
social e nĂŁo social. Este trabalho subdivide-se em dois capĂtulos experimentais: o capĂtulo II, onde
procuramos os circuitos neurais do condicionamento observado com um estĂmulo social ou nĂŁo social;
e capitulo III, no qual a eficĂĄcia de estĂmulos sociais quĂmicos e visuais Ă© testada num paradigma de
condicionamento aversivo. Em ambos os capĂtulos, um gene de ativação imediata sĂŁo usados como
marcadores de atividade neuronal: no capĂtulo II utilizando a expressĂŁo de c-fos, por hibridação insitu,
para mapear as regiĂ”es do cĂ©rebro recrutadas em aprendizagem social e nĂŁo social; e no capĂtulo
III, a reação quantitativa em cadeia da polimerase foi utilizada numa abordagem com genes e regiÔes
do cérebro candidatas para perceber o envolvimento do sistema olfativo em aprendizagem social
olfativa.
No capĂtulo II, nĂłs demonstramos que a aprendizagem social (SL) recruta diferentes regiĂ”es
do cérebro quando comparada com a aprendizagem não social (AL): SL aumenta a expressão de c-fos
nos bulbos olfativos, na zona ventral da årea telencefålica ventral, na habénula ventral, no tålamo
ventromedial e a AL diminui a expressĂŁo de c-fos na habĂ©nula dorsal e no nĂșcleo tubercular anterior.
Alem disso, conjuntos diferenciais de regiÔes cerebrais aparecem associados a aprendizagem social e
não social depois de uma anålise funcional da conectividade entre as regiÔes do cérebro.
No capĂtulo III, nĂłs mostramos que pistas sociais visuais, como a observação de um
conspecĂfico a exibir uma resposta de alarme, nĂŁo Ă© eficaz como um estimulo nĂŁo condicionado (US),
mas pistas sociais olfativas, como substĂąncia de alarme, foi altamente eficiente como US em
aprendizagem aversiva. Além disso, identificamos os bulbos olfativos como uma årea do cérebro
essencial para condicionamento observado olfativo. Uma anĂĄlise funcional da coesĂŁo e conectividade
dos nĂșcleos do cĂ©rebro envolvidos em processamento olfativo mostraram uma rede apurada para
condicionamento observado olfativo.
Em resumo, a presente tese elucida o debate nesta årea de investigação sobre os mecanismos
da aprendizagem social. Este trabalho clarifica que ao nĂvel comportamental a aprendizagem social
requer um domĂnio geral e ao nĂvel neuronal Ă© necessĂĄria uma rede modular que permite a
computação em simultĂąneo de vĂĄrias informaçÔes com diferentes nĂveis de complexidade.Animals use social and asocial information to take adaptive decisions that impact their fitness.
The use of social information brings advantages as to escape a predator, to find a food source or to
avoid fights with strongest individuals, only by the observation of conspecifics or their related
products. Social learning occurs when individuals observe the behaviour of others, or its
consequences, to modify their own behaviour. This behavioural strategy is highly conserved across
taxa: the crickets, Nemobius sylvestris, adapt their predator-avoidance behaviour after having
observed the behaviour of knowledgeable others, and they maintain these behavioural changes
lastingly after demonstrators are gone; the foragers of honeybees, Apis mellifera, display a series of
stereotypical motor behaviours which inform other foragers of the precise location of floral food.
The neuronal mechanisms of social learning are not clearly understood, and they are in centre
of debate in the field. Some authors hypothesized that the neural mechanisms of social learning are
shared and others that social learning is a general domain present even in solitary species.
The main goal of the present work is to clarify the mechanisms underlying social and asocial
learning. This work subdivide in two experimental chapters: the chapter II, where we search for the
neuronal circuits of reward observational conditioning with social or asocial stimuli; and the chapter
III, in which the effectiveness of a chemical and a visual social stimulus are tested as unconditioned
stimulus (US) in an aversive learning paradigm. In both chapters, an immediate early gene is used as
a marker of neuronal activity: in chapter II using the expression of c-fos, by in-situ hybridization, to
map the brain regions recruited in social and asocial learning; and in chapter III, the quantitative
polymerase chain reaction (pPCR) was used in a candidate genes and brain regions approach.
In chapter II, we demonstrated that social learning (SL) recruit different brain regions than
asocial learning (AL): SL increased the expression of c-fos in olfactory bulbs, in ventral zone of ventral
telencephalic area, in ventral habenula, in ventromedial thalamus and AL decreased the expression of
c-fos in dorsal habenula and in anterior tubercular nucleus. Moreover, differential sets of brain regions
appear associated to social and asocial learning after a functional connectivity analysis.
In chapter III, we showed that the social visual cue, the sight of alarmed conspecifics, was not
effective as an US; but social olfactory cue, the alarm substance, was highly efficient in aversive
learning paradigm. Also, we identified the olfactory bulbs as an essential brain region to olfactory
observational conditioning. A functional analysis of the cohesion and connectivity of the brain nuclei
involved in olfactory processing were tuned to chemical observational conditioning.
In sum, the present thesis elucidated the debate in the field on the mechanisms of social
learning. This work clarified that at the behavioural level social learning proved to be a general domain,
and at the neuronal level a modular network is needed to allow the computation, at the same time,
of high amount information with different levels of complexity
Animal minds: from computation to evolution.
notes: PMCID: PMC3427558types: Introductory Journal Article; Research Support, Non-U.S. Gov'tCopyright © 2012 The Royal Society. Post print version deposited in accordance with SHERPA RoMEO guidelines. The definitive version is available at: http://rstb.royalsocietypublishing.org/content/367/1603/2670.longIn the great Darwinian struggle for existence, all animals must tackle the problems posed by variable environments, be it finding and processing food, recognizing and attracting potential mates, avoiding predators, outcompeting rivals or navigating back to nesting sites. Although the mental processes by which different species deal with such challenges are varied, all animals share the fundamental problem of having to cope with the sheer abundance of information in the environment, much of which is likely to be irrelevant to the task at hand.David Phillips Fellowship from the BBSRC (A.T.)The Human Frontiers Science Programme Organization (U.G.
What can vigilance tell us about fear?
Animal vigilance is concerned with the monitoring of potential threats caused by predators and conspecifics. Researchers have argued that threats are part of a landscape of fear tracking the level of risk posed by predators and conspecifics. Vigilance, which is expected to vary with the level of risk, could thus be used as a measure of fear. Here, I explore the relationship between vigilance and fear caused by predators and conspecifics. The joint occurrence of vigilance and other physiological responses to fear, such as increased heart rate and stress hormone release, would bolster the idea that vigilance can be a useful marker of fear. While there is some support for a positive relationship between vigilance and physiological correlates of fear, a common theme in much of the empirical research is that vigilance and physiological correlates of fear are often uncoupled. Uncoupling can arise for several reasons. In particular, vigilance is not always a sensitive or specific marker of the internal state of vigilance. Vigilance might occur in animals who do not appear overtly vigilant or conversely an animal might appear vigilant without necessarily maintaining a state of vigilance. Animals in a fearful state might also be unable to allocate time to vigilance if they are too hungry. Vigilant animals might not show physiological responses associated with fear if they become desensitized to threats. For all these reasons, inferring fear from vigilance is fraught with ambiguity
A sensory system for robots using evolutionary artificial neural networks.
The thesis presents the research involved with developing an Intelligent Vision System for an animat that can analyse a visual scene in uncontrolled environments. Inspiration was drawn both from Biological Visual Systems and Artificial Image Recognition Systems. Several Biological Systems including the Insect, Toad and Human Visual Systems were studied alongside popular Pattern Recognition Systems such as fully connected Feedforward Networks, Modular Neural Networks and the Neocognitron. The developed system, called the Distributed Neural Network (DNN) was based on the sensory-motor connections in the common toad, Bufo Bufo. The sparsely connected network architecture has features of modularity enhanced by the presence of lateral inhibitory connections. It was implemented using Evolutionary Artificial Neural Networks (EANN). A novel method called FUSION was used to train the DNN, which is an amalgamation of several concepts of learning in Artificial Neural Networks such as Unsupervised Learning, Supervised Learning, Reinforcement Learning, Competitive Learning, Self-organisation and Fuzzy Logic. The DNN has unique feature detecting capabilities. When the DNN was tested using images that comprised of combination of features used in the training set, the DNN was successful in recognising individual features. The combinations of features were never used in the training set. This is a unique feature of the DNN trained using Fusion that cannot be matched by any other popular ANN architecture or training method. The system proved to be robust in dealing with New and Noisy Images. The unique features of the DNN make the network suitable for applications in robotics such as obstacle avoidance and terrain recognition, where the environment is unpredictable. The network can also be used in the field of Medical Imaging, Biometrics (Face and Finger Print Recognition) and Quality Inspection in the Food Processing Industry and applications in other uncontrolled environments
Embodied Cognition and Representation in Domesticated Dogs
Embodied cognition is a relatively recent approach in the philosophy of mind. Similarly, the volume of research into dog cognition has increased in the last decade and is set to keep on growing as we learn more about the animals with which we have associated for so long. This thesis argues that the principles of embodied cognition can be productively applied to the study of dogs. Adoption of these principles can improve experimental design and inform the conclusions that we draw from empirical data regarding dogsâ cognitive capacities and behaviour. This dissertation advocates for ethologically appropriate studies, designed for dogs rather than humans, a greater emphasis on the dynamic interplay between the dog, environment and humans, and fresh interpretations of the behaviour and cognitive skills that dogs demonstrate. Moreover, the models of embodied representation expounded in this thesis aid our understanding of dog behaviour and cognition and can enhance our approach to dog training. The thesis closes with a case for embodied representations as facilitators of rational actions in the domesticated dog
Fatigue Detection for Ship OOWs Based on Input Data Features, from The Perspective of Comparison with Vehicle Drivers: A Review
Ninety percent of the worldâs cargo is transported by sea, and the fatigue of ship officers of the watch (OOWs) contributes significantly to maritime accidents. The fatigue detection of ship OOWs is more difficult than that of vehicles drivers owing to an increase in the automation degree. In this study, research progress pertaining to fatigue detection in OOWs is comprehensively analysed based on a comparison with that in vehicle drivers. Fatigue detection techniques for OOWs are organised based on input sources, which include the physiological/behavioural features of OOWs, vehicle/ship features, and their comprehensive features. Prerequisites for detecting fatigue in OOWs are summarised. Subsequently, various input features applicable and existing applications to the fatigue detection of OOWs are proposed, and their limitations are analysed. The results show that the reliability of the acquired feature data is insufficient for detecting fatigue in OOWs, as well as a non-negligible invasive effect on OOWs. Hence, low-invasive physiological information pertaining to the OOWs, behaviour videos, and multisource feature data of ship characteristics should be used as inputs in future studies to realise quantitative, accurate, and real-time fatigue detections in OOWs on actual ships
Genetic Factors Associated with Thermal Tolerance in Grow-finish Pigs as Measured by Feeding Behavior
The objectives of this study were: one, use electronic monitoring to determine feeding behavior patterns of grow-finish pigs throughout the year and to identify changes that occurred during heat stress events, and second, identify genetic markers associated with changes in feeding behavior due to heat stress. Pigs were placed in a grow-finish barn at approximately eight to ten weeks of age in 6 pens of 40 animals and monitored for 4-months. Gilts and barrows were from three different sire breeds, Duroc, Landrace, and Yorkshire. Each pen had one feeder, designed to feed 5 animals at a time. Feeders were fitted with an antenna and a multiplexer. Data were collected from antennas every 20 seconds. Outside temperature and humidity were obtained from a National Weather Station and used to calculate temperature humidity index (THI). Days in the study were partitioned into groups based on their maximum temperature humidity index (THI), where a THI less than 23.33°C was classified as âNormalâ, a THI between 23.33°C and 26.11°C was classified as âAlertâ, a THI between 26.11°C and 28.88°C was classified as âDangerâ, and a THI greater than 28.88°C was classified as âEmergencyâ. Feeding behavioral differences among breeds and sex were observed across all THI categories. Landrace-sired pigs had fewer feeder visits compared to Duroc- and Yorkshire-sired pigs. Gilts had fewer feeder visits than barrows in all THI categories. A genome-wide association study for an animalâs change in feeding behavior between different THI categories was also conducted. Heritabilities for the difference in a pigâs feeder visits between each of the THI categories were low to moderate (0.136 to 0.406). Greater than 71% of genetic variation was explained by regions within eight chromosomes in the comparison between Danger and Emergency THI. Biological processes related to sensory perception and detection of chemical stimuli were over-represented in the set of genes located in these regions. Differences in feeding behavior patterns between THI categories demonstrate that heat stress affects sire breeds and sexes differently. Also genetic markers identified in this study may facilitate genetic selection for improved grow-finish performance during elevated ambient temperatures
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Spatial-memory control of defensive actions
Adapting anti-predatory defensive strategies to the properties of the environment is critical for survival. Here, I investigated the dependence of mouse instinctive defensive behaviours on memory of the spatial environment, and the neural mechanisms responsible for accurate escape towards refuge.
First, using behavioural assays, I show that the choice and execution of defensive behaviours rely on rapidly acquired memory and are promptly updated following acute changes in the environment. In the presence of a known refuge mice escape directly to it, even if this requires approaching the source of threat. Escape is initiated by a memory- guided, accurate head-rotation movement towards the location of the refuge, indicating knowledge of the spatial goal prior to flight start.
Second, I demonstrate that the superior colliculus (SC) is essential to accurately orient to shelter during escape, in agreement with its known role in both sensory- and memory- guided head orientation. To identify which upstream areas provide information about refuge location to the SC, I retrogradely traced the SC afferents and performed loss-of- function experiments in candidate areas, which showed that the retrosplenial cortex (RSC) plays a critical role in escape accuracy. Furthermore, channelrhodopsin-2-assisted connectivity studies showed a functional connection between RSC and SC, and chemogenetic inactivation of this projection impaired accurate orientation to refuge during escape.
To understand how the RSC and SC control orientation to shelter during escape, I performed simultaneous single-unit recordings from the RSC and SC with Neuropixels probes. Both RSC and SC were found to encode the angular offset between the mouseâs heading and the shelter, at the single-neuron and population levels. Chemogenetic inactivation of SC-projecting RSC neurons disrupts encoding of head-shelter offset in both regions, but it does not compromise the SC motor function during a sensory- orientation task.
In summary, I show that escape is a flexible behaviour and its accuracy critically depends on a monosynaptic projection from the RSC to SC. In addition, I show RSC-dependent egocentric encoding of goal direction at SC, an area critical for orientation during escape, providing a possible mechanism for controlling ethologically relevant goal-directed navigation.Boehringer Ingelheim Fellowshi
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