Novelty detection and context dependent processing of sky-compass cues in the brain of the desert locust Schistocerca gregaria

NERVOUS SYSTEMS facilitate purposeful interactions between animals and their environment, based on the perceptual powers, cognition and higher motor control. Through goal-directed behavior, the animal aims to increase its advantage and minimize risk. For instance, the migratory desert locust should profit from being fast in finding a fresh habitat, thus minimizing the investment of bodily resources in locomotion as well as the risk of starvation or capture by a predator en route. Efficient solutions to this and similar tasks – be it finding your way to work, the daily foraging of worker bees or the seasonal long-range migration of monarch butterflies - strongly depend on spatial orientation in local or global frames of reference. Local settings may include visual landmarks at stable positions that can be mapped onto egocentric space and learned for orientation, e.g. to remember a short route to a source of benefit (e.g. food) that is distant or visually less salient than the landmarks. Compass signals can mediate orientation to a global reference-frame (allothetic orienation), e.g. for locomotion in a particular compass direction or to merely ensure motion along a straight line. Whilst spatial orientation is a prerequisite of doing the planned in such tasks, animal survival in general depends on the ability to adequately respond to the unexpected, i.e. to unpredicted events such as the approach of a predator or mate. The process of identifying relevant events in the outside world that are not predictable from preceding events is termed novelty detection. Yet, the definition of ‘novelty’ is highly contextual: depending on the current situation and goal, some changes may be irrelevant and remain ´undetected´. The present thesis describes neuronal representations of a compass stimulus, correlates of novelty detection and interactions between the two in the minute brain of an insect, the migratory desert locust Schistocerca gregaria. Experiments were carried out in tethered locusts with legs and wings removed. More precisely, adult male subjects in the gregarious phase (see phase theory, Uvarov 1966) that migrates in swarms across territories in North Africa and the Middle East were used. The author performed electrophysiological recordings from single neurons in the locust brain, while either the compass stimulus (Chapter I) or events in the visual scenery (Chapter II) or combinations of both (Chapter III) were being presented to the animal. Injections of a tracer through the recording electrode, visualized by means of fluorescent-dye coupling, allowed the allocation of cellular morphologies to previously described types of neuron or the characterization of novel cell types, respectively. Recordings were focused on cells of the central complex, a higher integration area in the insect brain that was shown to be involved in the visually mediated control of goal-directed locomotion. Experiments delivered insights into how representations of the compass cue are modulated in a manner suited for their integration in the control of goal-directed locomotion. In particular, an interaction between compass-signaling and novelty detection was found, corresponding to a process in which input in one sensory domain (object vision) modulates the processing of concurrent input to a different exteroceptive sensory system (compass sense). In addition to deepening the understanding of the compass network in the locust brain, the results reveal fundamental parallels to higher context-dependent processing of sensory information by the vertebrate cortex, both with respect to spatial cues and novelty detection

Analysis and network simulations of honeybee interneurons responsive to waggle dance vibration signals

BACKGROUND: Honeybees have long fascinated neuroscientists with their highly evolved social structure and rich behavioral repertoire. They sense air vibrations with their antennae, which is vital for several activities during foraging, like waggle dance communication and flight. GOALS: This thesis presents the investigation of the function of an identified vibration-sensitive interneuron, DL-Int-1. Primary goals were the investigation of (i) adaptations during maturation and (ii) the role of DL-Int-1 in networks encoding distance information of waggle dance vibration signals. RESULTS: Visual inspection indicated that DL-Int-1 morphologies had similar gross structure, but were translated, rotated and scaled relative to each other. To enable detailed spatial comparison, an algorithm for the spatial co-registration of neuron morphologies, Reg-MaxS-N was developed and validated. Experimental data from DL-Int-1 was provided by our Japanese collaborators. Comparison of morphologies from newly emerged adult and forager DL-Int-1 revealed minor changes in gross dendritic features and consistent, region-dependent and spatially localized changes in dendritic density. Comparison of electrophysiological response properties showed an increase in firing rate differences between stimulus and non-stimulus periods during maturation. A putative disinhibitory network in the honeybee primary auditory center was proposed based on experimental evidence. Simulations showed that the network was consistent with experimental observations and clarified the central inhibitory role of DL-Int-1 in shaping the network output. RELEVANCE: Reg-MaxS-N presents a novel approach for the spatial co-registration of morphologies. Adaptations in DL-Int-1 morphology during maturation indicate improved connectivity and signal propagation. The central role of DL-Int-1 in a disinhibitory network in the honeybee primary auditory center combined with adaptions in its response properties during maturation could indicate better encoding of distance information from waggle dance vibration sig- nals

Kõrgete välistemperatuuride sensoorne kodeerimine putukate antennaalsete termo- ja hügroneuronite triaadi poolt

A Thesis submitted for the degree of Doctor of Philosophy in AgricultureDespite that environmental thermal conditions play a major role in all levels of biological organization very little information is available on noxious high temperature sensation crucial in behavioural thermoregulation and survival of small ectothermic animals such as insects. Scarcely anything is known about encoding of noxious high temperatures by peripheral thermoreceptor neurons. In this thesis, using a novel focused ion beam scanning electron microscopy combined technique, it was demonstrated that in economically important carabid and elaterid beetles, thermo- and hygroreceptor neurons are located in antennal dome-shape sensilla (DSS) morphologically distinct from all known types of sensilla of other insects. They are innervated by the classical sensory triad of a cold neuron and two antagonistically responding hygroreceptor neurons, the moist air and and the dry air neuron, respectively. Using extracellular single sensillum recording in the range of 20 to 45 °C it was shown that at temperatures above 25 (30) °C, firing mode of the DSSs neurons changes. They switch from regular spiking to spike bursting. Several parameters of the bursts of all the three neurons are temperature dependent and may hierarchically encode noxious heat up to lethal levels in a graded manner. According to their reaction type and response modality, the three DSS neurons were reclassified as the cold-hot neuron, the moist-hot neuron and the dry-hot neuron, respectively. The possible involvement of spike bursting in behavioural thermoregulation of the beetles is discussed. These findings consider spike bursting as general, fundamental quality of the classical sensory triad of insect antennal thermo- and hygro-thermoreceptor neurons being a flexible and reliable mode of coding unfavourably high temperatures.Vaatamata sellele, et temperatuur mõjutab kõiki eluslooduse tasandeid, on väga vähe andmeid selle kohta, kuidas tajuvad ohtlikult kõrgeid temperatuure ektotermid sh. putukad, mis on määrava tähtsusega nende käitumuslikus termoregulatsioonis ja ellujäämisel. Väga vähe on teada mil viisil kodeerivad ohtlikult kõrgeid temperatuure perifeersed temperatuuritundlikud neuronid. Käesolevas doktoritöös, kasutades uudset fokusseeritud ioonkiirte skanneeriva elektronmikroskoopia kombineeritud tehnikat, näidatakse, et põllumajanduslikult olulistel jooksiklastel ja naksurlastel paiknevad termo-ja hügroretseptorneuronid antennaalsetes kuppeljates sensillides (DSS), mis erinevad morfoloogiliselt putukate kõigist senituntud sensillitüüpidest. DSS innerveerib klassikaline neuronite triaad: külmaneuron ja kaks antagonistlikku hügroretseptorneuronit (niiske ja kuiva õhu neuron). Üksiku sensilli rakuväline registreerimine temperatuuri vahemikus 20 kuni 45 oC näitas, et temperatuuridel üle 25 (30 oC) lülituvad DSS neuronid regulaarsete närviimpulsside genereerimiselt impulssvalangute genereerimisele. Kõigi kolme neuroni mitmed valangulised parameetrid on temperatuurisõltuvuslikud ja võivad hierarhiliselt kodeerida ohtlikult kõrgeid temperatuure. Vastavalt sensoorsele modaalsusele ja reaktsiooni tüübile nimetati DSS paiknevad neuronid ümber külma-kuumaneuroniks ja õhuniiskuse-kuumaneuroniks ning õhukuivuse-kuumaneuroniks. Töö tulemused näitavad esmakordselt, et impulss-valangute genereerimise võime on putukate klassikalise termo- ja hügroneuronite triaadi üldine ja fundamentaalne omadus võimaldades paindlikult ja usaldusväärselt kodeerida kõrgeid temperatuure, mis on kriitilise tähtsusega ektotermide käitumuslikus termoregulatsioonis.Publication of this thesis is supported by the Estonian University of Life Sciences

Short term plasticity. A neuromorphic perspective

Ramachandran H. Short term plasticity. A neuromorphic perspective. Bielefeld: Universität Bielefeld; 2018

A Flight Sensory-Motor to Olfactory Histamine Circuit Mediates Olfactory Processing of Ecologically and Behaviorally Natural Stimuli

Environmental pressures have conferred species specific behavioral and morphological traits to optimize reproductive success. To optimally interact with their environment, nervous systems have evolved motor-to-sensory circuits that mediate the processing of its own reafference. Moth flight behavioral patterns to odor sources are stereotyped, presumably to optimize the likelihood of interacting with the odor source. In the moth Manduca sexta wing beating causes oscillatory flow of air over the antenna; because of this, odorant-antennal interactions are oscillatory in nature. Electroantennogram recordings on antennae show that the biophysical properties of their spiking activity can effectively track odors presented at the wing beat frequency. Psychophysical experiments using Manduca show that when odors are pulsed, as opposed to presented as a continuous stream, detection and discrimination thresholds are lowered. In this study, we characterized histamine immunoreactivity in the thoracic ganglia and brain of Manduca. We generated antibodies for and characterized the distribution of the histamine B receptor, the first known antibody for this receptor protein. Our results show an elaborate pair of neurons projecting from the mesothoracic ganglion to the brain, including axon innervation of the antennal lobe and antennal mechanosensory and motor centers. Additionally, histamine B receptor labeling overlapped with a subset of GABAergic and peptidergic local interneurons. Next, we characterized the response properties of these cells within the context of fictive flight behavior and found a tonic increase in activity. Furthermore, disrupting this circuit, with surgical ablation and pharmacology, disrupts antennal lobe projection neurons from entraining to odors presented at a natural 20 Hz frequency, as well as behavioral measures of detection and discrimination thresholds. Finally, we characterized the relationship between motor patterns/behaviors, and circuit structure of this pair of histamine immunoreactive neurons. Specifically, presence of MDHn axon collaterals entering the antennal lobe is correlated with olfactory-guided target approach behaviors in crepuscular and nocturnal moths who require stereotyped zigzagging and wing beating behaviors for locating an olfactory target have axonal ramifications in the antennal lobe. This study is the first characterization of a motor to olfactory corollary discharge circuit in invertebrates and may represent the first characterization of a higher order corollary discharge circuit in an invertebrate model

Coding of sky-compass information in neurons of the anterior optic tubercle of the desert locust Schistocerca gregaria

The primary aim of my Doctoral thesis project was to test through intracellular recordings the hypothesis that the lower unit of the AOTu participates in polar- ization vision. Four types of interneurons with ramifications in the lower unit of the AOTu were characterized in multiple recordings. All of these neurons were sensitive to polarized light, sub- stantiating our hypothesis (Chapter I, -> page 19). Two types of neuron, called lobula tuber- cle neuron (LoTu1) and tubercle tubercle neuron (TuTu1), were especially amenable to intracel- lular recordings, due to their large axon diam- eters. In the first set of experiments, we found that all polarization-sensitive neurons were also responsive to unpolarized light (Chapter I, -> page 19). To investigate the significance of this finding, we extended the stimulation with un- polarized light in a second set of experiments. The responses of both LoTu1 and TuTu1 to UV and green light spots from different directions suggest that these neurons signal the horizontal direction of the sun (solar azimuth), by exploit- ing both intensity- and color-gradients as well as the sky-polarization pattern (Chapter II, -> page 35). The use of both unpolarized and po- larized light information to detect the solar az- imuth can result in conflicting information pro- vided by the different cues. One way to reduce this conflict of information is to exclude certain areas of polarized skylight from being analyzed by the polarization-vision system. By stimulat- ing with different degrees of polarization (d), we showed that the threshold for E-vector detec- tion lies around d-values of 0.3. This means that an area of around 100 degrees around the sun con- tains no visible E-vector information for these neurons (Chapter III, -> page 51). Recent be- havioral experiments further confirmed that the pathway described above is vital for polarotaxis in locusts. Tethered locusts that are flown under a slowly rotating polarizer show periodic changes in yaw torque with a period of 180 degrees (Mappes & Homberg, 2004). When the anterior optic tract is unilaterally transected, the locusts are still able to respond to the rotating E-vector in the same manner as intact animals. However, when the DRA that is contralateral to the transection site is occluded, the animals become disoriented (Mappes and Homberg, in revison)

Population-level neural coding for higher cognition

Higher cognition encompasses advanced mental processes that enable complex thinking, decision-making, problem-solving, and abstract reasoning. These functions involve integrating information from multiple sensory modalities and organizing action plans based on the abstraction of past information. The neural activity underlying these functions is often complex, and the contribution of single neurons in supporting population-level representations of cognitive variables is not yet clear. In this thesis, I investigated the neural mechanisms underlying higher cognition in higher-order brain regions with single-neuron resolution in human and non-human primates performing working memory tasks. I aimed to understand how representations are arranged and how neurons contribute to the population code. In the first manuscript, I investigated the population-level neural coding for the maintenance of numbers in working memory within the parietal association cortex. By analyzing intra-operative intracranial micro-electrode array recording data, I uncovered distinct representations for numbers in both symbolic and nonsymbolic formats. In the second manuscript, I delved deeper into the neuronal organizing principles of population coding to address the ongoing debate surrounding memory maintenance mechanisms. I unveiled sparse structures in the neuronal implementation of representations and identified biologically meaningful components that can be directly communicated to downstream neurons. These components were linked to subpopulations of neurons with distinct physiological properties and temporal dynamics, enabling the active maintenance of working memory while resisting distraction. Lastly, using an artificial neural network model, I demonstrated that the sparse implementation of temporally modulated working memory representations is preferred in recurrently connected neural populations such as the prefrontal cortex. In summary, this thesis provides a comprehensive investigation of higher cognition in higher-order brain regions, focusing on working memory tasks involving numerical stimuli. By examining neural population coding and unveiling sparse structures in the neuronal implementation of representations, our findings contribute to a deeper understanding of the mechanisms underlying working memory and higher cognitive functions

Developmental and interspecies comparison of morphology and plasticity in neuronal circuits involved in olfactory information processing

The anterior piriform cortex (aPCx) is a three layered paleocortex receiving afferent inputs from the olfactory bulb as well as local and long-range associational inputs. Neurons in layer 2 are segregated into layer 2A and layer 2B according to their position, morphology and implementation in the sensory and associative circuits. The dendritic architecture of these neurons is determined during postnatal development and plays an important role for the functionality and circuit integration of the two cell types. Here, confocal imaging, electrophysiology, morphometry and Ca2+ imaging, were combined in order to study the development of the dendritic arborizations for both subtypes of layer 2 neurons. Three different growth phases were identified: branch complexity determination, branch elongation and pruning, occurring at different time windows during development. Layer 2A and layer 2B neurons showed morphological differences between their apical and basal dendrites from the very first postnatal days; as well as phase-specific differences during development associated to differences in circuit implementation. During the first postnatal week, early spontaneous network activity in layer 2 of the aPCx displayed differences between layer 2A and layer 2B neurons in their functional connectivity, reflected in the morphological dissimilarities between their basal dendritic trees during the period of branch complexity determination. Additionally, strong differences in growth phase three were observed. Pruning was exclusive for layer 2B neurons and selective for apical dendrites receiving layer 1A sensory inputs. These differences between layer 2A and layer 2B cells in their morphological and functional development exhibit the close association between circuit specificity and neuronal development. Finally, synaptic plasticity in the mossy fiber (MF) pathway of the hippocampus in shrews was investigated and compared to mice. Although hippocampal structure in shrews is preserved, short and long-term plasticity at the MF synapsis was lower compared to mice, suggesting different involvement of these synapses in the behavioral outcome of different species.Der Cortex piriformis anterior (aPCx auf Englisch) ist ein dreischichtiger Paläokortex, der sensorische afferente Eingänge aus dem Riechkolben sowie intracerebrale assoziative Eingänge empfängt. Die Neuronen in Schicht 2 werden nach ihrer Position, Morphologie und Einbindung in die sensorischen und rekurrenten Netzwerke in die Schichten 2A und 2B unterteilt. Die dendritische Architektur dieser Neurone wird während der postnatalen Entwicklung festgelegt und spielt eine wichtige Rolle für die Funktionalität und Netzwerkintegration der beiden Zelltypen. Hier wurden konfokales Imaging, Elektrophysiologie, Morphometrie und Kalzium-Imaging kombiniert, um die Entwicklung der Dendritenbäume für beide Subtypen von Schicht-2-Neuronen zu untersuchen. Es wurden drei verschiedene Wachstumsphasen identifiziert: Bestimmung der Komplexität der Verzweigung, Verlängerung der Verzweigung und strukturelle Vereinfachung, die in verschiedenen Zeitfenstern während der Entwicklung auftreten. Neurone der Schicht 2A und der Schicht 2B zeigten bereits in den ersten postnatalen Tagen morphologische Unterschiede zwischen ihren apikalen und basalen Dendriten sowie phasenspezifische Unterschiede während der Entwicklung, die mit Unterschieden in der Netzwerkimplementierung verbunden sind. Während der ersten postnatalen Woche zeigte die frühe spontane Netzwerkaktivität in Schicht 2 des aPCx Unterschiede in der funktionellen Konnektivität zwischen Neuronen der Schicht 2A und Schicht 2B, die sich in den morphologischen Unterschieden zwischen ihren basalen Dendritenbäumen während der Bestimmung der Verzweigungskomplexität widerspiegelten. Außerdem wurden starke Unterschiede in der dritten Wachstumsphase beobachtet. Die strukturelle Vereinfachung fand ausschließlich bei Neuronen der Schicht 2B statt und war selektiv für apikale Dendriten, die sensorische Inputs der Schicht 1A erhielten. Diese Unterschiede zwischen Zellen der Schicht 2A und der Schicht 2B in ihrer morphologischen und funktionellen Entwicklung zeigen den engen Zusammenhang zwischen Netzwerkspezifität und neuronaler Entwicklung. Schließlich wurde die synaptische Plastizität des Moosfaser (MF)-Trakts des Hippocampus bei Spitzmäusen untersucht und mit der von Mäusen verglichen. Obwohl die Struktur des Hippocampus bei Spitzmäusen erhalten ist, war die Kurz- und Langzeitplastizität an den MF-Synapsen im Vergleich zu Mäusen geringer, was auf eine unterschiedliche Beteiligung dieser Synapsen an spezifisch adaptierte Verhaltensweisen der beiden Spezies hindeutet

Descending premotor target tracking systems in flying insects

The control of behaviour in all animals requires efficient transformation of sensory signals into the task-specific activation of muscles. Predation offers an advantageous model behaviour to study the computational organisation underlying sensorimotor control. Predators are optimised through diverse evolutionary arms races to outperform their prey in terms of sensorimotor coordination, leading to highly specialised anatomical adaptations and hunting behaviours, which are often innate and highly stereotyped. Predatory flying insects present an extreme example, performing complex visually-guided pursuits of small, often fast flying prey over extremely small timescales. Furthermore, this behaviour is controlled by a tiny nervous system, leading to pressure on neuronal organisation to be optimised for coding efficiency. In dragonflies, a population of eight pairs of bilaterally symmetric Target Selective Descending Neurons (TSDNs) relay visual information about small moving objects from the brain to the thoracic motor centres. These neurons encode the movement of small moving objects across the dorsal fovea region of the eye which is fixated on prey during predatory pursuit, and are thought to constitute the commands necessary for actuating an interception flight path. TSDNs are characterised by their receptive fields, with responses of each TSDN type spatially confined to a specific portion of the dorsal fovea visual field and tuned to a specific direction of object motion. To date, little is known about the descending representations mediating target tracking in other insects. This dissertation presents a comparative report of descending neurons in a variety of flying insects. The results are organised into three chapters: Chapter 3 identifies TSDNs in demoiselle damselflies and compares their response properties to those previously described in dragonflies. Demoiselle TSDNs are also found to integrate binocular information, which is further elaborated with prism and eyepatch experiments. Chapter 4 describes TSDNs in two dipteran species, the robberfly Holcocephala fusca and the killerfly Coenosia attenuata. Chapter 5 describes an interaction between small- and wide-field visual features in TSDNs of both predatory and nonpredatory dipterans, finding functional similarity of these neurons for prey capture and conspecific pursuit. Dipteran TSDN responses are repressed by background motion in a direction dependent manner, suggesting a control architecture in which target tracking and optomotor stabilization pathways operate in parallel during pursuit.echnology and Biological Sciences ResearchCouncil (BB/M011194/1