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Frighetto, Giovanni (2019) Selection for action in Drosophila melanogaster. [Ph.D. thesis]

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Abstract (italian or english)

The present work focuses on the mechanisms of selection for the control of action in Drosophila melanogaster (D. melanogaster), also known as fruit fly. D. melanogaster has a rich repertoire of innate and learned behaviours and a quite simple brain, composed by roughly 100,000 neurons, which can be studied by means of sophisticated techniques. Therefore, it offers the possibility to study complex behaviour in a brain structure simpler than that of higher organisms. As a consequence the neurobiological underpinning of its behaviour can be understood in an easier manner. The comparison of its behaviour with similar behaviours shown by different and evolutively distant animals can provide important insights about their relationship with different or conserved underlying neural circuits.
This thesis was conceptualized to sketch out whether selection for action processes underlying the behaviour of mammals might be shared with lower organisms such as D. melanogaster. Selection for action entails a close interaction between visual and motor systems allowing to select a specific stimulus in the environment to which act upon. This process allows to filter out irrelevant information for action.
The first experiment was aimed at investigating whether flies have an action-based attention. Are flies able to inhibit via attentional mechanisms the response to an upcoming stimulus in order to successfully end an ongoing action? In particular, I observed whether flies are prone to interference effects caused by the upcoming appearance of a competitive stimulus (i.e., a distractor). I expected this inhibitory mechanism to be played out on spatial trajectories. In this study, flies were engaged in a walking task aimed at reaching a visual target (i.e., a bright stripe) while an abrupt identical distractor was laterally presented.
The second experiment pointed at extending the finding of the first experiment. In particular, angular distances between target and distractor were considered. The aim of this study was to test the hypothesis that the shorter the distance between target and distractor the greater is the level of inhibition.
Then, in the third experiment I targeted the hypothetical neural circuit underlying the behavioural effects observed in the previous experiments. Based on the increasing evidence for an intriguing homology between a specific neuropil of flies (Central Complex; CX) and the mammals’ neural structure involved in action selection, the idea was to test flies with a lesioned CX during the behavioural task used in the previous experiments. To do this, I used a technique based on the GAL4-UAS binary system in order to downregulate specific dopamine receptors in a very selected neural circuit, the so-called E-PG neurons. Moreover, I adopted an optogenetic technique for in vivo neural manipulation. I employed flies bearing light-sensitive ion channels in the same selected neural circuit of CX to briefly activate such neurons during the task. This neural circuit forms a donut-shape structure which it has been proposed to be an integrative circuit between visual and motor systems and to perform an attention-like function.
Finally, in the fourth experiment I characterized a series of neural circuits of CX from a neurochemical perspective. The hypothesis was that the dopaminergic system, involved in the action selection process of mammals, could also modulate the neurophysiological response within the CX of flies. Specifically, I recorded in vivo the neural response to dopamine application in CX of flies by using a bioluminescence technique based on a genetically encoded calcium indicator.
All in all, this work represents an attempt to tackle the mechanisms of selection for the control of action in flies. The interference paradigm I developed establishes a powerful platform to further explore the problem of selection for action in flies which might be useful for clarifying similar processes in higher organisms.

Abstract (a different language)

Il presente lavoro si focalizza sui meccanismi di selezione per il controllo dell’azione utilizzati da Drosophila melanogaster (D. melanogaster), anche nota come moscerino della frutta. D. melanogaster ha un ricco repertorio di comportamenti e un cervello semplice, composto di circa 100,000 neuroni, che può essere studiato con tecniche raffinate. Perciò, offre la possibilità di studiare un comportamento in una struttura cerebrale semplice rispetto a quella di organismi più complessi. Le basi neurobiologiche del suo comportamento possono essere così più facilmente comprese. Il confronto con comportamenti simili mostrarti da animali evolutivamente più lontani può fornire importanti intuizioni sui circuiti neurali sottesi.
Questa tesi è stata concettualizzata per verificare se i processi di selezione per l’azione dei mammiferi potessero essere condivisi con organismi più bassi come D. melanogaster. La selezione per l’azione implica una stretta interazione tra sistema visivo e motorio che consente di scegliere uno stimolo nell’ambiente per agire su di esso. Questo processo permette di filtrare le informazioni irrilevanti per l’azione.
Il primo esperimento era finalizzato a indagare se i moscerini mostrano un’attenzione basata sull’azione. Sono capaci di inibire la risposta a uno stimolo grazie a meccanismi attentivi per terminare un’azione? In particolare ho indagato se i moscerini sono inclini all’effetto d’interferenza causato dalla comparsa di uno stimolo competitivo (cioè, un distrattore). Mi aspettavo che questo meccanismo inibitorio fosse evidente nelle traiettorie spaziali. In questo studio i moscerini erano impegnati a raggiungere un target visivo (cioè, una striscia luminosa) mentre un distrattore compariva lateralmente.
Il secondo esperimento mirava a estendere le conclusioni del primo esperimento. In particolare sono state considerate le distanze tra target e distrattore. L’obiettivo di questo studio era di verificare l’ipotesi che più corta è la distanza tra target e distrattore, più elevato è il livello d’inibizione.
Nel terzo esperimento ho individuato l’ipotetico circuito neurale responsabile degli effetti comportamentali osservati negli esperimenti precedenti. Basandomi su crescenti evidenze in favore di un’affascinante omologia tra un neuropilo dei moscerini (il Complesso Centrale, CC) e la struttura neurale dei mammiferi implicata nella selezione dell’azione, ho testato il comportamento in moscerini con CC danneggiato. A questo scopo ho usato una tecnica basata sul sistema binario GAL4-UAS per ridurre l’espressione di specifici recettori dopaminergici in un circuito neurale molto selettivo, i cosiddetti neuroni E-PG. Inoltre, ho adottato una tecnica optogenetica per la manipolazione neurale in vivo. Ho utilizzato moscerini che esprimevano canali ionici foto-attivabili nello stesso circuito del CC per eccitare tali neuroni durante il compito. Questo circuito neurale forma una struttura a ciambella che è stata considerata un centro d’integrazione tra il sistema visivo e motorio deputato all’attenzione.
Infine, nel quarto esperimento, ho caratterizzato da un punto di vista neurochimico una serie di circuiti neurali del CC. L’ipotesi era che il sistema dopaminergico implicato nel processo di selezione dell’azione nei mammiferi potesse modulare anche nei moscerini la risposta neurofisiologica all’interno del CC. Nello specifico, ho registrato in vivo la risposta neurale ad applicazioni di dopamina nel CC dei moscerini utilizzando una tecnica di bioluminescenza basata su indicatori del calcio geneticamente codificati.
Nel complesso questo lavoro rappresenta un tentativo di affrontare i meccanismi di selezione per il controllo dell’azione nei moscerini. Il paradigma d’interferenza che ho sviluppato costituisce una potente piattaforma per esplorare il problema della selezione per l’azione che potrebbe essere utile al fine di chiarire processi simili in organismi più complessi.

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EPrint type:Ph.D. thesis
Tutor:Castiello, Umberto
Supervisor:Megighian, Aram
Ph.D. course:Ciclo 32 > Corsi 32 > SCIENZE PSICOLOGICHE
Data di deposito della tesi:22 November 2019
Anno di Pubblicazione:22 November 2019
Key Words:invertebrates, action selection, selective attention, central complex, visuomotor control, dopamine, Drosophila melanogaster
Settori scientifico-disciplinari MIUR:Area 11 - Scienze storiche, filosofiche, pedagogiche e psicologiche > M-PSI/02 Psicobiologia e psicologia fisiologica
Struttura di riferimento:Dipartimenti > Dipartimento di Psicologia Generale
Codice ID:12081
Depositato il:26 Jan 2021 15:21
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