The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain

Paulk, Angelique C.; Phillips-Portillo, James; Dacks, Andrew M.; Fellous, Jean-Marc; Gronenberg, Wulfila

doi:10.1523/jneurosci.1196-08.2008

Cited by 121 publications

(168 citation statements)

References 76 publications

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“…1). They peak at 556, 436, and 344 nm, respectively (Menzel and Blakers 1976;Peitsch et al 1992). The green LED was capable of selectively stimulating the green channel because the blue photoreceptor channel has virtually no sensitivity above 500 nm.…”

Section: Discussionmentioning

confidence: 99%

Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee

Hung

Kleef

Stange

et al. 2013

Journal of Neurophysiology

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Hung YS, van Kleef JP, Stange G, Ibbotson MR. Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee. J Neurophysiol 109: 1202-1213, 2013. First published November 28, 2012 doi:10.1152/jn.00830.2012.-By measuring insect compensatory optomotor reflexes to visual motion, researchers have examined the computational mechanisms of the motion processing system. However, establishing the spectral sensitivity of the neural pathways that underlie this motion behavior has been difficult, and the contribution of the simple eyes (ocelli) has been rarely examined. In this study we investigate the spectral response properties and ocellar inputs of an anatomically identified descending neuron (DNII 2 ) in the honeybee optomotor pathway. Using a panoramic stimulus, we show that it responds selectively to optic flow associated with pitch rotations. The neuron is also stimulated with a custom-built light-emitting diode array that presented moving bars that were either all-green (spectrum 500 -600 nm, peak 530 nm) or all-short wavelength (spectrum 350 -430 nm, peak 380 nm). Although the optomotor response is thought to be dominated by green-sensitive inputs, we show that DNII 2 is equally responsive to, and direction selective to, both greenand short-wavelength stimuli. The color of the background image also influences the spontaneous spiking behavior of the cell: a green background produces significantly higher spontaneous spiking rates. Stimulating the ocelli produces strong modulatory effects on DNII 2 , significantly increasing the amplitude of its responses in the preferred motion direction and decreasing the response latency by adding a directional, short-latency response component. Our results suggest that the spectral sensitivity of the optomotor response in honeybees may be more complicated than previously thought and that ocelli play a significant role in shaping the timing of motion signals.

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Section: Discussionmentioning

confidence: 99%

Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee

Hung

Kleef

Stange

et al. 2013

Journal of Neurophysiology

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“…Recordings with each visual stimulus as well as control recordings were replicated three times per bee. The minimum interstimulus interval was 1 min, thus avoiding potential adaptation to light stimuli (Paulk et al, 2008).…”

Section: Methodsmentioning

confidence: 99%

“…Knowledge of AOTu function in bees was scarce, and the few previous recordings obtained from isolated neurons pointed to a possible involvement of the AOTu in the processing of chromatic information (Paulk et al, 2008(Paulk et al, , 2009). Here we provide the first functional data on AOTu neural populations.…”

Section: Aotu Function In a Physiological And Behavioral Contextmentioning

confidence: 99%

Neural Organization and Visual Processing in the Anterior Optic Tubercle of the Honeybee Brain

Mota¹,

Yamagata²,

Giurfa³

et al. 2011

J. Neurosci.

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The honeybee Apis mellifera represents a valuable model for studying the neural segregation and integration of visual information. Vision in honeybees has been extensively studied at the behavioral level and, to a lesser degree, at the physiological level using intracellular electrophysiological recordings of single neurons. However, our knowledge of visual processing in honeybees is still limited by the lack of functional studies of visual processing at the circuit level. Here we contribute to filling this gap by providing a neuroanatomical and neurophysiological characterization at the circuit level of a practically unstudied visual area of the bee brain, the anterior optic tubercle (AOTu). First, we analyzed the internal organization and neuronal connections of the AOTu. Second, we established a novel protocol for performing optophysiological recordings of visual circuit activity in the honeybee brain and studied the responses of AOTu interneurons during stimulation of distinct eye regions. Our neuroanatomical data show an intricate compartmentalization and connectivity of the AOTu, revealing a dorsoventral segregation of the visual input to the AOTu. Light stimuli presented in different parts of the visual field (dorsal, lateral, or ventral) induce distinct patterns of activation in AOTu output interneurons, retaining to some extent the dorsoventral input segregation revealed by our neuroanatomical data. In particular, activity patterns evoked by dorsal and ventral eye stimulation are clearly segregated into distinct AOTu subunits. Our results therefore suggest an involvement of the AOTu in the processing of dorsoventrally segregated visual information in the honeybee brain.

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“…LT11, a pair of bilateral hemivisual-field VPNs, have been shown to play a role in spectrum-specific phototaxis (Otsuna et al, 2014). In bees, electrophysiological studies have demonstrated that neurons innervating the deep lobula strata (Lo5-6) are color sensitive and in general have a larger receptive field than the corresponding medulla neurons (Hertel, 1980;Paulk et al, 2008). Given that the central brain targets of lobula output neurons (VPN) lack retinotopic organization, the lobula seems likely to transform images into feature-based information, such as associating color and motion visual attributes with objects.…”

Section: Introductionmentioning

confidence: 99%

Mapping chromatic pathways in the Drosophila visual system

Lin

Luo

Shinomiya

et al. 2015

J of Comparative Neurology

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In Drosophila, color vision and wavelength-selective behaviors are mediated by the compound eye's narrow-spectrum photoreceptors, R7 and R8, and their downstream neurons, Tm5a/b/c 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 GRASP (GFP reconstitution across synaptic partners) method to probe connections between the chromatic Tm neurons and 28 known and novel types of lobula neurons, we identified 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 revealed that Li4 receives synaptic contacts from over 90% of all four types of chromatic Tm neurons while 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 developed and applied a "two-tag" double labeling method to label LT11's dendrites and the mitochondria in Tm5c's presynaptic terminals. Serial electron microscopic reconstruction confirmed 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. Graphical Abstract CONFLICT OF INTERESTThe authors declare no conflicts of interest. ROLE OF AUTHORSAll authors had access to all data presented in this study. The authors accept responsibility for the integrity and accuracy of the data and data analysis. Study concept and design: TYL, CHL, IAM. Preparation and acquisition of data: TYL, JL, KS, CYT, ZL. Analysis and interpretation of data: TYL, CHL. Drafting of the manuscript: TYL, IAM, CHL. Using trans-synaptic tracing and ultrastructural "two-tag" double-labeling approaches for EM, the authors identify synaptic targets of first-order chromatic interneurons in the deep visual processing center, the lobula. Lobula intrinsic neuron Li4 and projection neuron LT11 receive parallel chromatic inputs but with differential synaptic densities. HHS Public Access

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The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain

Cited by 121 publications

References 76 publications

Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee

Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee

Neural Organization and Visual Processing in the Anterior Optic Tubercle of the Honeybee Brain

Mapping chromatic pathways in the Drosophila visual system

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