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Simple Summary: Serotonin is ubiquitously expressed in vertebrates and invertebrates, where it regulates specific behavioural patterns. Though the specific effects of serotonin release in the optic lobe are not entirely known, increasing evidence associates the serotonergic system with optic lobe-mediated behaviours. In this study, the localization of serotonin transporter (SERT) was immunohistochemically analysed in the optic lobes of moderate, docile and aggressive worker honeybees. SERT-immunoreactive fibres were stratified in the optic lobe and distributed in the three visual neuropils: lamina, medulla and lobula. Interestingly, SERT immunoreactivity was inversely related to aggressive behaviour. The present study indicates that low levels of serotonin in the optic lobe are associated with aggressive behaviour. Visual information is processed in the optic lobes, which consist of three retinotopic neuropils. These are the lamina, the medulla and the lobula. Biogenic amines play a crucial role in the control of insect responsiveness, and serotonin is clearly related to aggressiveness in invertebrates. Previous studies suggest that serotonin modulates aggression-related behaviours, possibly via alterations in optic lobe activity. The aim of this investigation was to immunohistochemically localize the distribution of serotonin transporter (SERT) in the optic lobe of moderate, docile and aggressive worker honeybees. SERT-immunoreactive fibres showed a wide distribution in the lamina, medulla and lobula; interestingly, the highest percentage of SERT immunoreactivity was observed across all the visual neuropils of the docile group. Although future research is needed to determine the relationship between the distribution of serotonin fibres in the honeybee brain and aggressive behaviours, our immunohistochemical study provides an anatomical basis supporting the role of serotonin in aggressive behaviour in the honeybee. [ABSTRACT FROM AUTHOR]

Dragonflies are highly skilled and successful aerial predators that are even capable of selectively attending to one target within a swarm. Detection and tracking of prey is likely to be driven by small target motion detector (STMD) neurons identified from several insect groups. Prior work has shown that dragonfly STMD responses are facilitated by targets moving on a continuous path, enhancing the response gain at the present and predicted future location of targets. In this study, we combined detailed morphological data with computational modeling to test whether a combination of dendritic morphology and nonlinear properties of NMDA receptors could explain these observations. We developed a hybrid computational model of neurons within the dragonfly optic lobe, which integrates numerical and morphological components. The model was able to generate potent facilitation for targets moving on continuous trajectories, including a localized spotlight of maximal sensitivity close to the last seen target location, as also measured during in vivo recordings. The model did not, however, include a mechanism capable of producing a traveling or spreading wave of facilitation. Our data support a strong role for the high dendritic density seen in the dragonfly neuron in enhancing non-linear facilitation. An alternative model based on the morphology of an unrelated type of motion processing neuron from a dipteran fly required more than three times higher synaptic gain in order to elicit similar levels of facilitation, despite having only 20% fewer synapses. Our data support a potential role for NMDA receptors in target tracking and also demonstrate the feasibility of combining biologically plausible dendritic computations with more abstract computational models for basic processing as used in earlier studies. [ABSTRACT FROM AUTHOR]

Visual information is processed in the optic lobes, which consist of three retinotopic neuropils. These are the lamina, the medulla and the lobula. Biogenic amines play a crucial role in the control of insect responsiveness, and serotonin is clearly related to aggressiveness in invertebrates. Previous studies suggest that serotonin modulates aggression-related behaviours, possibly via alterations in optic lobe activity. The aim of this investigation was to immunohistochemically localize the distribution of serotonin transporter (SERT) in the optic lobe of moderate, docile and aggressive worker honeybees. SERT-immunoreactive fibres showed a wide distribution in the lamina, medulla and lobula; interestingly, the highest percentage of SERT immunoreactivity was observed across all the visual neuropils of the docile group. Although future research is needed to determine the relationship between the distribution of serotonin fibres in the honeybee brain and aggressive behaviours, our immunohistochemical study provides an anatomical basis supporting the role of serotonin in aggressive behaviour in the honeybee.

Visual pathways from the compound eye of an insect relay to four neuropils, successively the lamina, medulla, lobula, and lobula plate in the underlying optic lobe. Among these neuropils, the medulla, lobula, and lobula plate are interconnected by the complex second optic chiasm, through which the anteroposterior axis undergoes an inversion between the medulla and lobula. Given their complex structure, the projection patterns through the second optic chiasm have so far lacked critical analysis. By densely reconstructing axon trajectories using a volumetric scanning electron microscopy (SEM) technique, we reveal the three-dimensional structure of the second optic chiasm of Drosophila melanogaster , which comprises interleaving bundles and sheets of axons insulated from each other by glial sheaths. These axon bundles invert their horizontal sequence in passing between the medulla and lobula. Axons connecting the medulla and lobula plate are also bundled together with them but do not decussate the sequence of their horizontal positions. They interleave with sheets of projection neuron axons between the lobula and lobula plate, which also lack decussations. We estimate that approximately 19,500 cells per hemisphere, about two thirds of the optic lobe neurons, contribute to the second chiasm, most being Tm cells, with an estimated additional 2,780 T4 and T5 cells each. The chiasm mostly comprises axons and cell body fibers, but also a few synaptic elements. Based on our anatomical findings, we propose that a chiasmal structure between the neuropils is potentially advantageous for processing complex visual information in parallel. The EM reconstruction shows not only the structure of the chiasm in the adult brain, the previously unreported main topic of our study, but also suggest that the projection patterns of the neurons comprising the chiasm may be determined by the proliferation centers from which the neurons develop. Such a complex wiring pattern could, we suggest, only have arisen in several evolutionary steps. [ABSTRACT FROM AUTHOR]

Sex pheromones orient male moths toward conspecific female moths; the presence of visual information modulates this behavior. In the current study, we explore candidate neuronal pathways for the interaction between vision and the locomotor signal for pheromone orientation. We describe the connectivity between visual neuropils and brain premotor centers, the posterior slope (PS) and the lateral accessory lobe (LAL), in the silkmoth Bombyx mori. Using a single-cell labeling technique, we analyze visual projection neurons supplying these areas. Neurons from both the medulla and lobula complex projected to the PS but only the neurons originating in the lobula complex had additional processes to the LAL. Further, we identified populations of putative feedback neurons from the premotor centers to the optic lobe. Neurons originating in the PS were likely to project to the medulla, whereas those originating in the LAL were likely to project to the lobula complex. The anatomical study contributes to further understanding of integration of visual information on the locomotor control in the insect brain. [ABSTRACT FROM AUTHOR]

Molecular genetic experiments are revealing how the fly brain generates behavioral responses to visual stimuli.

Visual projection neurons (VPNs) provide an anatomical connection between early visual processing and higher brain regions. Here we characterize lobula columnar (LC) cells, a class of Drosophila VPNs that project to distinct central brain structures called optic glomeruli. We anatomically describe 22 different LC types and show that, for several types, optogenetic activation in freely moving flies evokes specific behaviors. The activation phenotypes of two LC types closely resemble natural avoidance behaviors triggered by a visual loom. In vivo two-photon calcium imaging reveals that these LC types respond to looming stimuli, while another type does not, but instead responds to the motion of a small object. Activation of LC neurons on only one side of the brain can result in attractive or aversive turning behaviors depending on the cell type. Our results indicate that LC neurons convey information on the presence and location of visual features relevant for specific behaviors.

Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate, that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the lobula plate. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: 1) the morphology of their dendritic arbors; 2) their four morphological and functional subtypes; 3) their cholinergic profile in Drosophila; 4) their input from the pathways of L3 cells in the first neuropil, or lamina, and by one of a pair of lamina cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and 5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla, and T5 in the third neuropil or lobula. Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate medulla and lobula neuropils, and that a fiber crossing – the internal chiasma – arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the lobula as a new neuropil that formed when it separated from its ancestral neuropil to leave the medulla, suggesting additionally that medulla input neurons to T4 and T5 may also have had a common origin.

ABSTRACT In Drosophila, color vision and wavelength-selective behaviors are mediated by the compound eye's narrow-spectrum photoreceptors R7 and R8 and their downstream medulla projection (Tm) neurons Tm5a, Tm5b, Tm5c, and Tm20 in the second optic neuropil or medulla. These chromatic Tm neurons project axons to a deeper optic neuropil, the lobula, which in insects has been implicated in processing and relaying color information to the central brain. The synaptic targets of the chromatic Tm neurons in the lobula are not known, however. Using a modified GFP reconstitution across synaptic partners (GRASP) method to probe connections between the chromatic Tm neurons and 28 known and novel types of lobula neurons, we identify anatomically the visual projection neurons LT11 and LC14 and the lobula intrinsic neurons Li3 and Li4 as synaptic targets of the chromatic Tm neurons. Single-cell GRASP analyses reveal that Li4 receives synaptic contacts from over 90% of all four types of chromatic Tm neurons, whereas LT11 is postsynaptic to the chromatic Tm neurons, with only modest selectivity and at a lower frequency and density. To visualize synaptic contacts at the ultrastructural level, we develop and apply a 'two-tag' double-labeling method to label LT11's dendrites and the mitochondria in Tm5c's presynaptic terminals. Serial electron microscopic reconstruction confirms that LT11 receives direct contacts from Tm5c. This method would be generally applicable to map the connections of large complex neurons in Drosophila and other animals. J. Comp. Neurol. 524:213-227, 2016. © 2015 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

In Drosophila, the paired giant descending neurons (GDNs), also known as giant fibers, and the paired giant antennal mechanosensory descending neurons (GAMDNs), are supplied by visual and mechanosensory inputs. Both neurons have the largest cell bodies in the brain and both supply slender axons to the neck connective. The GDN axon thereafter widens to become the largest axon in the thoracic ganglia, supplying information to leg extensor and wing depressor muscles. The GAMDN axon remains slender, interacting with other descending neuron axons medially. GDN and GAMDN dendrites are partitioned to receive inputs from antennal mechanosensory afferents and inputs from the optic lobes. Although GDN anatomy has been well studied in Musca domestica, less is known about the Drosophila homolog, including electrophysiological responses to sensory stimuli. Here we provide detailed anatomical comparisons of the GDN and the GAMDN, characterizing their sensory inputs. The GDN showed responses to light-on and light-off stimuli, expanding stimuli that result in luminance decrease, mechanical stimulation of the antennae, and combined mechanical and visual stimulation. We show that ensembles of lobula columnar neurons (type Col A) and mechanosensory antennal afferents are likely responsible for these responses. The reluctance of the GDN to spike in response to stimulation confirms observations of the Musca GDN. That this reluctance may be a unique property of the GDN is suggested by comparisons with the GAMDN, in which action potentials are readily elicited by mechanical and visual stimuli. The results are discussed in the context of descending pathways involved in multimodal integration and escape responses. [ABSTRACT FROM AUTHOR]

Topographic maps, the systematic spatial ordering of neurons by response tuning, are common across species. In Drosophila , the lobula columnar (LC) neuron types project from the optic lobe to the central brain, where each forms a glomerulus in a distinct position. However, the advantages of this glomerular arrangement are unclear. Here, we examine the functional and spatial relationships of 10 glomeruli using single-neuron calcium imaging. We discover novel detectors for objects smaller than the lens resolution (LC18) and for complex line motion (LC25). We find that glomeruli are spatially clustered by selectivity for looming versus drifting object motion and ordered by size tuning to form a topographic visual feature map. Furthermore, connectome analysis shows that downstream neurons integrate from sparse subsets of possible glomeruli combinations, which are biased for glomeruli encoding similar features. LC neurons are thus an explicit example of distinct feature detectors topographically organized to facilitate downstream circuit integration. • Lobula columnar (LC) neurons are tuned to distinct features of object motion • LC18 detects motion of very small objects by comparing contrast changes in time • LCs project to optic glomeruli that are spatially ordered by visual feature tuning • Downstream neurons integrate from sparse subsets of neighboring glomeruli By combining calcium imaging and synaptic connectivity analysis, Klapoetke et al. reveal that optic glomeruli in the fly central brain form a topographic visual map, with glomeruli anatomically ordered by visual feature selectivity. Downstream circuits appear to exploit this map by integrating primarily from nearby glomeruli encoding similar features. [ABSTRACT FROM AUTHOR]

A wide variety of animal species including humans and fruit flies see second-order motion although they lack coherent spatiotemporal correlations in luminance. Recent electrophysiological recordings, together with intensive psychophysical studies, are bringing to light the neural underpinnings of second-order motion perception in mammals. However, where and how the higher-order motion signals are processed in the fly brain is poorly understood. Using the rich genetic tools available in Drosophila and examining optomotor responses in fruit flies to several stimuli, we revealed that two lobula-specific visual projection neurons, specifically connecting the lobula and the central brain, are involved in the perception of motion-defined second-order motion, independent of whether the second-order feature is moving perpendicular or opposite to the local first-order motion. By contrast, blocking these neurons has no effect on first-order and flicker-defined second-order stimuli in terms of response delay. Our results suggest that visual neuropils deep in the optic lobe and the central brain, whose functional roles in motion processing were previously unclear, may be specifically required for motion-defined motion processing. [ABSTRACT FROM AUTHOR]

Animals use vision to perform such diverse behaviors as finding food, interacting socially with other animals, choosing a mate, and avoiding predators. These behaviors are complex and the visual system must process color, motion, and pattern cues efficiently so that animals can respond to relevant stimuli. The visual system achieves this by dividing visual information into separate pathways, but to what extent are these parallel streams separated in the brain? To answer this question, we recorded intracellularly in vivo from 105 morphologically identified neurons in the lobula, a major visual processing structure of bumblebees (Bombus impatiens). We found that these cells have anatomically segregated dendritic inputs confined to one or two of six lobula layers. Lobula neurons exhibit physiological characteristics common to their respective input layer. Cells with arborizations in layers 1- 4 are generally indifferent to color but sensitive to motion, whereas layer 5- 6 neurons often respond to both color and motion cues. Furthermore, the temporal characteristics of these responses differ systematically with dendritic branching pattern. Some layers are more temporally precise, whereas others are less precise but more reliable across trials. Because different layers send projections to different regions of the central brain, we hypothesize that the anatomical layers of the lobula are the structural basis for the segregation of visual information into color, motion, and stimulus timing. [ABSTRACT FROM AUTHOR]

Electron microscopy (EM)-based connectomes provide important insights into how visual circuitry of fruit fly Drosophila computes various visual features, guiding and complementing behavioral and physiological studies. However, connectomic analyses of the lobula, a neuropil putatively dedicated to detecting object-like features, remains underdeveloped, largely because of incomplete data on the inputs to the brain region. Here, we attempted to map the columnar inputs into the Drosophila lobula neuropil by performing connectivity-based and morphology-based clustering on a densely reconstructed connectome dataset. While the dataset mostly lacked visual neuropils other than lobula, which would normally help identify inputs to lobula, our clustering analysis successfully extracted clusters of cells with homogeneous connectivity and morphology, likely representing genuine cell types. We were able to draw a correspondence between the resulting clusters and previously identified cell types, revealing previously undocumented connectivity between lobula input and output neurons. While future, more complete connectomic reconstructions are necessary to verify the results presented here, they can serve as a useful basis for formulating hypotheses on mechanisms of visual feature detection in lobula., (Copyright © 2022 Tanaka and Clark.)

Summary Many animals rely on vision to detect, locate, and track moving objects. In Drosophila courtship, males primarily use visual cues to orient toward and follow females and to select the ipsilateral wing for courtship song. Here, we show that the LC10 visual projection neurons convey essential visual information during courtship. Males with LC10 neurons silenced are unable to orient toward or maintain proximity to the female and do not predominantly use the ipsilateral wing when singing. LC10 neurons preferentially respond to small moving objects using an antagonistic motion-based center-surround mechanism. Unilateral activation of LC10 neurons recapitulates the orienting and ipsilateral wing extension normally elicited by females, and the potency with which LC10 induces wing extension is enhanced in a state of courtship arousal controlled by male-specific P1 neurons. These data suggest that LC10 is a major pathway relaying visual input to the courtship circuits in the male brain. [ABSTRACT FROM AUTHOR]

Molecular genetic experiments are revealing how the fly brain generates behavioral responses to visual stimuli., Competing Interests: The authors declare that no competing interests exist.

Visual projection neurons (VPNs) provide an anatomical connection between early visual processing and higher brain regions. Here we characterize lobula columnar (LC) cells, a class of Drosophila VPNs that project to distinct central brain structures called optic glomeruli. We anatomically describe 22 different LC types and show that, for several types, optogenetic activation in freely moving flies evokes specific behaviors. The activation phenotypes of two LC types closely resemble natural avoidance behaviors triggered by a visual loom. In vivo two-photon calcium imaging reveals that these LC types respond to looming stimuli, while another type does not, but instead responds to the motion of a small object. Activation of LC neurons on only one side of the brain can result in attractive or aversive turning behaviors depending on the cell type. Our results indicate that LC neurons convey information on the presence and location of visual features relevant for specific behaviors., Competing Interests: The authors declare that no competing interests exist.

Synaptic circuits for identified behaviors in the Drosophila brain have typically been considered from either a developmental or functional perspective without reference to how the circuits might have been inherited from ancestral forms. For example, two candidate pathways for ON- and OFF-edge motion detection in the visual system act via circuits that use respectively either T4 or T5, two cell types of the fourth neuropil, or lobula plate (LOP), that exhibit narrow-field direction-selective responses and provide input to wide-field tangential neurons. T4 or T5 both have four subtypes that terminate one each in the four strata of the LOP. Representatives are reported in a wide range of Diptera, and both cell types exhibit various similarities in: (1) the morphology of their dendritic arbors; (2) their four morphological and functional subtypes; (3) their cholinergic profile in Drosophila; (4) their input from the pathways of L3 cells in the first neuropil, or lamina (LA), and by one of a pair of LA cells, L1 (to the T4 pathway) and L2 (to the T5 pathway); and (5) their innervation by a single, wide-field contralateral tangential neuron from the central brain. Progenitors of both also express the gene atonal early in their proliferation from the inner anlage of the developing optic lobe, being alone among many other cell type progeny to do so. Yet T4 receives input in the second neuropil, or medulla (ME), and T5 in the third neuropil or lobula (LO). Here we suggest that these two cell types were originally one, that their ancestral cell population duplicated and split to innervate separate ME and LO neuropils, and that a fiber crossing-the internal chiasma-arose between the two neuropils. The split most plausibly occurred, we suggest, with the formation of the LO as a new neuropil that formed when it separated from its ancestral neuropil to leave the ME, suggesting additionally that ME input neurons to T4 and T5 may also have had a common origin.

Motion information provides essential cues for a wide variety of animal behaviors such as mate, prey, or predator detection. In decapod crustaceans and pterygote insects, visual codification of object motion is associated with visual processing in the third optic neuropile, the lobula. In this neuropile, tangential neurons collect motion information from small field columnar neurons and relay it to the midbrain where behavioral responses would be finally shaped. In highly ordered structures, detailed knowledge of the neuroanatomy can give insight into their function. In spite of the relevance of the lobula in processing motion information, studies on the neuroarchitecture of this neuropile are scant. Here, by applying dextran-conjugated dyes in the second optic neuropile (the medulla) of the crab Neohelice, we mass stained the columnar neurons that convey visual information into the lobula. We found that the arborizations of these afferent columnar neurons lie at four main lobula depths. A detailed examination of serial optical sections of the lobula revealed that these input strata are composed of different number of substrata and that the strata are thicker in the centre of the neuropile. Finally, by staining the different lobula layers composed of tangential processes we combined the present characterization of lobula input strata with the previous characterization of the neuroarchitecture of the crab's lobula based on reduced-silver preparations. We found that the third lobula input stratum overlaps with the dendrites of lobula giant tangential neurons. This suggests that columnar neurons projecting from the medulla can directly provide visual input to the crab's lobula giant neurons., (Copyright © 2014 Elsevier Ltd. All rights reserved.)