Neural Organization and Visual Processing in the Anterior Optic Tubercle of the Honeybee Brain (original) (raw)
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Visual Processing in the Central Bee Brain
Journal of Neuroscience, 2009
Visual scenes comprise enormous amounts of information from which nervous systems extract behaviorally relevant cues. In most model systems, little is known about the transformation of visual information as it occurs along visual pathways. We examined how visual information is transformed physiologically as it is communicated from the eye to higher-order brain centers using bumblebees, which are known for their visual capabilities. We recorded intracellularly in vivo from 30 neurons in the central bumblebee brain (the lateral protocerebrum) and compared these neurons to 132 neurons from more distal areas along the visual pathway, namely the medulla and the lobula. In these three brain regions (medulla, lobula, and central brain), we examined correlations between the neurons' branching patterns and their responses primarily to color, but also to motion stimuli. Visual neurons projecting to the anterior central brain were generally color sensitive, while neurons projecting to the posterior central brain were predominantly motion sensitive. The temporal response properties differed significantly between these areas, with an increase in spike time precision across trials and a decrease in average reliable spiking as visual information processing progressed from the periphery to the central brain. These data suggest that neurons along the visual pathway to the central brain not only are segregated with regard to the physical features of the stimuli (e.g., color and motion), but also differ in the way they encode stimuli, possibly to allow for efficient parallel processing to occur.
Chromatic Processing in the Anterior Optic Tubercle of the Honey Bee Brain
Journal of Neuroscience, 2013
Color vision in honey bees (Apis mellifera) has been extensively studied at the behavioral level and, to a lesser degree, at the physiological level by means of electrophysiological intracellular recordings of single neurons. Few visual neurons have been so far characterized in the lateral protocerebrum of bees. Therefore, the possible implication of this region in chromatic processing remains unknown. We performed in vivo calcium imaging of interneurons in the anterior optic tubercle (AOTu) of honey bees upon visual stimulation of the compound eye to analyze chromatic response properties. Stimulation with distinct monochromatic lights (ultraviolet [UV], blue, and green) matching the sensitivity of the three photoreceptor types of the bee retina induced different signal amplitudes, temporal dynamics, and spatial activity patterns in the AOTu intertubercle network, thus revealing intricate chromatic processing properties. Green light strongly activated both the dorsal and ventral lobes of the AOTu's major unit; blue light activated the dorsal lobe more while UV light activated the ventral lobe more. Eye stimulation with mixtures of blue and green light induced suppression phenomena in which responses to the mixture were lower than those to the color components, thus concurring with color-opponent processing. These data provide evidence for a spatial segregation of color processing in the AOTu, which may serve for navigation purposes.
Frontiers in Behavioral Neuroscience, 2016
While the ability of honeybees to navigate relying on sky-compass information has been investigated in a large number of behavioral studies, the underlying neuronal system has so far received less attention. The sky-compass pathway has recently been described from its input region, the dorsal rim area (DRA) of the compound eye, to the anterior optic tubercle (AOTU). The aim of this study is to reveal the connection from the AOTU to the central complex (CX). For this purpose, we investigated the anatomy of large microglomerular synaptic complexes in the medial and lateral bulbs (MBUs/LBUs) of the lateral complex (LX). The synaptic complexes are formed by tubercle-lateral accessory lobe neuron 1 (TuLAL1) neurons of the AOTU and GABAergic tangential neurons of the central body's (CB) lower division (TL neurons). Both TuLAL1 and TL neurons strongly resemble neurons forming these complexes in other insect species. We further investigated the ultrastructure of these synaptic complexes using transmission electron microscopy. We found that single large presynaptic terminals of TuLAL1 neurons enclose many small profiles (SPs) of TL neurons. The synaptic connections between these neurons are established by two types of synapses: divergent dyads and divergent tetrads. Our data support the assumption that these complexes are a highly conserved feature in the insect brain and play an important role in reliable signal transmission within the sky-compass pathway.
Ocellar interneurons in the honeybee
Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology, 1984
Intracellular recording and staining techniques revealed new aspects of the anatomy and physiology of ocellar L-neurons in the honeybee (Apis mellifera). Structural comparisons of homologous identified L-neurons showed that their axon pathways and projection areas in the brain were similar, whereas somata location and terminal branching patterns differed. L-neuron responses to light ranged from graded reponses with fast on-and off-transients to inhibition of spontaneous discharge. Since the same morphological type of L-neuron responded differently in different animals, response types could not be correlated systematically with morphology. However, purely graded responses were not found in extrinsic LD-neurons , and lateral ocellar L-neurons never exhibited an inhibition of the tonic spike discharge without a graded component. L-neuron graded responses could be elicited only by light stimulation of the ocelli, but not by moving striped patterns, polarised white light, light stimuli to the compound eyes, airpuffs, or odor stimuli. Various parameters of the graded response code light intensity differently. Response/intensity functions rise over an intensity range of 5 log units to saturate at higher intensities. The spectral sensitivity has two peaks close to 340 nm and 500 nm.
Neuroarchitecture of the central complex in the brain of the honeybee: Neuronal cell types
Journal of comparative neurology, 2020
The central complex (CX) in the insect brain is a higher order integration center that controls a number of behaviors, most prominently goal directed locomotion. The CX comprises the protocerebral bridge (PB), the upper division of the central body (CBU), the lower division of the central body (CBL), and the paired noduli (NO). Although spatial orientation has been extensively studied in honeybees at the behavioral level, most electrophysiological and anatomical analyses have been carried out in other insect species, leaving the morphology and physiology of neurons that constitute the CX in the honeybee mostly enigmatic. The goal of this study was to morphologically identify neuronal cell types of the CX in the honeybee Apis mellifera. By performing iontophoretic dye injections into the CX, we traced 16 subtypes of neuron that connect a subdivision of the CX with other regions in the bee's central brain, and eight subtypes that mainly interconnect different subdivisions of the CX. They establish extensive connections between the CX and the lateral complex, the superior protocerebrum and the posterior protocerebrum. Characterized neuron classes and subtypes are morphologically similar to those described in other insects, suggesting considerable conservation in the neural network relevant for orientation.
New vistas on honey bee vision
Apidologie, 2012
The honey bee is a traditional animal model for the study of visual perception, learning, and memory. Extensive behavioral studies have shown that honey bees perceive, learn, and memorize colors, shapes, and patterns when these visual cues are paired with sucrose reward. Bee color vision is trichromatic, based on three photoreceptor types (S, M, L), which peak in the UV, blue, and green region of the spectrum. Perceptual color spaces have been proposed to account for bee color vision, and the anatomy of the visual neuropils in the bee brain was described to a large extent. In the last decade, conceptual and technical advances improved significantly our comprehension of visual processing in bees. At the behavioral level, unexpected cognitive visual capacities were discovered such as categorical and conceptual categorization. At the neurobiological level, molecular analyses of the compound eye revealed an intricate heterogeneity in the distribution of photoreceptors in the retina. Spatial segregation and integration of visual information in the bee brain has been analyzed at functional levels so far unexploited. These recent discoveries associated with the perspective of accessing the bee brain of harnessed bees while they perceive and learn visual cues open new avenues toward a comprehension of the neural substrates of visual perception and learning in bees. Understanding how the miniature brain of bees achieves sophisticated visual performances is a fundamental goal for the comparative study of vision and cognition.
Interneurones of the central complex in the bee brain (Apis mellifera, L.)
Journal of Insect Physiology, 1985
The response characteristics of 46 interneurones of the central complex in the bee brain to visual, various antenna1 and mechanical stimuli were studied. Different types of neurones can be distinguished anatomically. Intrinsic cells arborize only in the central complex. Segmental neurones innervate a segment of the protocerebral bridge and the central body and project to the lateral accessory lobes. Fan-shaped neurones have arborizations throughout the whole upper or lower division of the central body. Intrinsic neurones of the protocerebral bridge process visual information, the other cells display different and often multimodal response characteristics, which cannot be correlated with the neuroanatomical groups. Seventeen per cent of the cells did not respond at all to the stimuli presented. The role of the central complex in the processing of sensory information is discussed and compared with the mushroom bodies and the diffuse protocerebral lobes.
The Circuitry of Olfactory Projection Neurons in the Brain of the Honeybee, Apis mellifera
Frontiers in neuroanatomy, 2016
In the honeybee brain, two prominent tracts - the medial and the lateral antennal lobe tract - project from the primary olfactory center, the antennal lobes (ALs), to the central brain, the mushroom bodies (MBs), and the protocerebral lobe (PL). Intracellularly stained uniglomerular projection neurons were reconstructed, registered to the 3D honeybee standard brain atlas, and then used to derive the spatial properties and quantitative morphology of the neurons of both tracts. We evaluated putative synaptic contacts of projection neurons (PNs) using confocal microscopy. Analysis of the patterns of axon terminals revealed a domain-like innervation within the MB lip neuropil. PNs of the lateral tract arborized more sparsely within the lips and exhibited fewer synaptic boutons, while medial tract neurons occupied broader regions in the MB calyces and the PL. Our data show that uPNs from the medial and lateral tract innervate both the core and the cortex of the ipsilateral MB lip but dif...
Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens )
The Journal of Comparative Neurology, 2009
The mechanisms of processing a visual scene involve segregating features (such as color) into separate information channels at different stages within the brain, processing these features, and then integrating this information at higher levels in the brain. To examine how this process takes place in the insect brain, we focused on the medulla, an area within the optic lobe through which all of the visual information from the retina must pass before it proceeds to central brain areas. We used histological and immunocytochemical techniques to examine the bumblebee medulla and found that the medulla is divided into eight layers. We then recorded and morphologically identified 27 neurons with processes in the medulla. During our recordings we presented color cues to determine whether response types correlated with locations of the neural branching patterns of the filled neurons among the medulla layers. Neurons in the outer medulla layers had less complex color responses compared to neurons in the inner medulla layers and there were differences in the temporal dynamics of the responses among the layers. Progressing from the outer to the inner medulla, neurons in the different layers appear to process increasingly complex aspects of the natural visual scene.
Possible functions of a population of descending neurons in the honeybee's visuo-motor pathway
Apidologie, 1993
— An identified population of honeybee descending neurons (DNs) responds to wide-field motion over the compound eyes. They give non-habituating, directionally selective responses which adapt to continued motion. Contrast sensitivity functions show the responses depend on luminance, contrast, spatial and temporal frequency. The distribution of the DNs' outputs in the thoracic ganglia is consistent with changes in muscular activity required for particular compensatory movements. These features suggest the DNs lie along the optomotor pathway. The DNs' responses have different time-courses. This might reflect distinctions in their putative inputs and between pathways implicated in different aspects of visually mediated flight control. The responses of horizontal DNs to contraction and expansion and to unidirectional motion were compared revealing differences in the way they integrate the monocular components of binocular flow-fields and how velocity and spatial structure effects this integration. It is possible the DNs are convergence site(s) for substrates underlying different behaviours each triggered by specific optical flow templates. descending neuron / vision / motion sensitivity / directional selectivity * Present address: