scholarly journals Neuronal circuits integrating visual motion information in Drosophila

2021 ◽  
Author(s):  
Kazunori Shinomiya ◽  
Aljoscha Nern ◽  
Ian Meinertzhagen ◽  
Stephen M Plaza ◽  
Michael B Reiser

The detection of visual motion enables sophisticated animal navigation, and studies in flies have provided profound insights into the cellular and circuit basis of this neural computation. The fly's directionally selective T4 and T5 neurons respectively encode ON and OFF motion. Their axons terminate in one of four retinotopic layers in the lobula plate, where each layer encodes one of four cardinal directions of motion. While the input circuitry of the directionally selective neurons has been studied in detail, the synaptic connectivity of circuits integrating T4/T5 motion signals is largely unknown. Here we report a 3D electron microscopy reconstruction, wherein we comprehensively identified T4/T5's synaptic partners in the lobula plate, revealing a diverse set of new cell types and attributing new connectivity patterns to known cell types. Our reconstruction explains how the ON and OFF motion pathways converge. T4 and T5 cells that project to the same layer, connect to common synaptic partners symmetrically, that is with similar weights, and also comprise a core motif together with bilayer interneurons, detailing the circuit basis for computing motion opponency. We discovered pathways that likely encode new directions of motion by integrating vertical and horizontal motion signals from upstream T4/T5 neurons. Finally, we identify substantial projections into the lobula, extending the known motion pathways and suggesting that directionally selective signals shape feature detection there. The circuits we describe enrich the anatomical basis for experimental and computations analyses of motion vision and bring us closer to understanding complete sensory-motor pathways.

2020 ◽  
Author(s):  
Maria-Bianca Leonte ◽  
Aljoscha Leonhardt ◽  
Alexander Borst ◽  
Alex S. Mauss

AbstractVisual motion detection is among the best understood neuronal computations. One assumed behavioural role is to detect self-motion and to counteract involuntary course deviations, extensively investigated in tethered walking or flying flies. In free flight, however, any deviation from a straight course is signalled by both the visual system as well as by proprioceptive mechanoreceptors called ‘halteres’, which are the equivalent of the vestibular system in vertebrates. Therefore, it is yet unclear to what extent motion vision contributes to course control, or whether straight flight is completely controlled by proprioceptive feedback from the halteres. To answer these questions, we genetically rendered flies motion-blind by blocking their primary motion-sensitive neurons and quantified their free-flight performance. We found that such flies have difficulties maintaining a straight flight trajectory, much like control flies in the dark. By unilateral wing clipping, we generated an asymmetry in propulsory force and tested the ability of flies to compensate for this perturbation. While wild-type flies showed a remarkable level of compensation, motion-blind animals exhibited pronounced circling behaviour. Our results therefore unequivocally demonstrate that motion vision is necessary to fly straight under realistic conditions.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Shigehiro Namiki ◽  
Michael H Dickinson ◽  
Allan M Wong ◽  
Wyatt Korff ◽  
Gwyneth M Card

In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in Drosophila melanogaster and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all Drosophila DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly’s capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.


2017 ◽  
Vol 115 (1) ◽  
pp. 186-191 ◽  
Author(s):  
Matthew Chalk ◽  
Olivier Marre ◽  
Gašper Tkačik

A central goal in theoretical neuroscience is to predict the response properties of sensory neurons from first principles. To this end, “efficient coding” posits that sensory neurons encode maximal information about their inputs given internal constraints. There exist, however, many variants of efficient coding (e.g., redundancy reduction, different formulations of predictive coding, robust coding, sparse coding, etc.), differing in their regimes of applicability, in the relevance of signals to be encoded, and in the choice of constraints. It is unclear how these types of efficient coding relate or what is expected when different coding objectives are combined. Here we present a unified framework that encompasses previously proposed efficient coding models and extends to unique regimes. We show that optimizing neural responses to encode predictive information can lead them to either correlate or decorrelate their inputs, depending on the stimulus statistics; in contrast, at low noise, efficiently encoding the past always predicts decorrelation. Later, we investigate coding of naturalistic movies and show that qualitatively different types of visual motion tuning and levels of response sparsity are predicted, depending on whether the objective is to recover the past or predict the future. Our approach promises a way to explain the observed diversity of sensory neural responses, as due to multiple functional goals and constraints fulfilled by different cell types and/or circuits.


2016 ◽  
Author(s):  
Kit D. Longden ◽  
Martina Wicklein ◽  
Benjamin J. Hardcastle ◽  
Stephen J. Huston ◽  
Holger G. Krapp

SummaryMany animals use the visual motion generated by travelling in a line, the translatory optic flow, to successfully navigate obstacles: near objects appear larger and to move more quickly than distant ones. Flies are experts at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. Here, we present novel cell types that have motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes forwards sideslip self-motion, and fires action potentials in clusters of spikes, spike bursts. We show that the spike burst coding is size and speed-tuned, and is selectively modulated by parallax motion, the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the single spike rate is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have the properties required for the fly to successfully navigate clutter and encode its movements along near cardinal axes of thrust, lift and forward sideslip.


2018 ◽  
Author(s):  
Daniel M. Cohen ◽  
Hee-Woong Lim ◽  
Kyoung-Jae Won ◽  
David J. Steger

ABSTRACTSequence-specific DNA binding recruits transcription factors (TFs) to the genome to regulate gene expression. Here, we perform high resolution mapping of CEBP proteins to determine how sequence dictates genomic occupancy. We demonstrate a fundamental difference between the sequence repertoire utilized by CEBPs in vivo versus the palindromic sequence preference reported by classical in vitro models, by identifying a palindromic motif at less than 1% of the genomic binding sites. On the native genome, CEBPs bind a diversity of related 10 bp sequences resulting from the fusion of degenerate and canonical half-sites. Altered DNA specificity of CEBPs in cells occurs through heterodimerization with other bZip TFs, and approximately 40% of CEBP-binding sites in primary human cells harbor motifs characteristic of CEBP heterodimers. In addition, we uncover an important role for sequence bias at core-motif-flanking bases for CEBPs and demonstrate that flanking bases regulate motif function across mammalian bZip TFs. Favorable flanking bases confer efficient TF occupancy and transcriptional activity, and DNA shape may explain how the flanks alter TF binding. Importantly, motif optimization within the 10-mer is strongly correlated with cell-type-independent recruitment of CEBPβ, providing key insight into how sequence sub-optimization affects genomic occupancy of widely expressed CEBPs across cell types.


Author(s):  
Maria-Bianca Leonte ◽  
Aljoscha Leonhardt ◽  
Alexander Borst ◽  
Alex S. Mauss

Visual motion detection is among the best understood neuronal computations. As extensively investigated in tethered flies, visual motion signals are assumed to be crucial to detect and counteract involuntary course deviations. During free flight, however, course changes are also signalled by other sensory systems. Therefore, it is yet unclear to what extent motion vision contributes to course control. To address this question, we genetically rendered flies motion-blind by blocking their primary motion-sensitive neurons and quantified their free-flight performance. We found that such flies have difficulties maintaining a straight flight trajectory, much like unimpaired flies in the dark. By unilateral wing clipping, we generated an asymmetry in propulsive force and tested the ability of flies to compensate for this perturbation. While wild-type flies showed a remarkable level of compensation, motion-blind animals exhibited pronounced circling behaviour. Our results therefore directly confirm that motion vision is necessary to fly straight under realistic conditions.


2007 ◽  
Vol 97 (3) ◽  
pp. 2032-2041 ◽  
Author(s):  
Ulrich Beckers ◽  
Martin Egelhaaf ◽  
Rafael Kurtz

Synapses are generally considered to operate efficiently only when their signaling range matches the spectrum of prevailing presynaptic signals in terms of both amplitudes and dynamics. However, the prerequisites for optimally matching the signaling ranges may differ between spike-mediated and graded synaptic transmission. This poses a problem for synapses that convey both graded and spike signals at the same time. We addressed this issue by tracing transmission systematically in vivo in the blowfly's visual-motion pathway by recording from single neurons that receive mixed potential signals consisting of rather slow graded fluctuations superimposed with highly variable spikes from a small number of presynaptic elements. Both pre- and postsynaptic neurons were previously shown to represent preferred-direction motion velocity reliably and linearly at low fluctuation frequencies. To selectively assess the performance of individual synapses and to precisely control presynaptic signals, we voltage clamped one of the presynaptic neurons. Results showed that synapses can effectively convey signals over a much larger amplitude and frequency range than is normally used during graded transmission of visual signals. An explanation for this unexpected finding might lie in the transmission of the spike component that reaches larger amplitudes and contains higher frequencies than graded signals.


2015 ◽  
Vol 11 (10) ◽  
pp. 20150687 ◽  
Author(s):  
Finlay J. Stewart ◽  
Michiyo Kinoshita ◽  
Kentaro Arikawa

Many insects’ motion vision is achromatic and thus dependent on brightness rather than on colour contrast. We investigate whether this is true of the butterfly Papilio xuthus , an animal noted for its complex retinal organization, by measuring head movements of restrained animals in response to moving two-colour patterns. Responses were never eliminated across a range of relative colour intensities, indicating that motion can be detected through chromatic contrast in the absence of luminance contrast. Furthermore, we identify an interaction between colour and contrast polarity in sensitivity to achromatic patterns, suggesting that ON and OFF contrasts are processed by two channels with different spectral sensitivities. We propose a model of the motion detection process in the retina/lamina based on these observations.


2019 ◽  
Vol 121 (2) ◽  
pp. 371-395 ◽  
Author(s):  
Max L. Mehlman ◽  
Shawn S. Winter ◽  
Jeffrey S. Taube

An animal’s directional heading within its environment is encoded by the activity of head direction (HD) cells. In rodents, these neurons are found primarily within the limbic system in the interconnected structures that form the limbic HD circuit. In our accompanying report in this issue, we describe two HD cell populations located outside of this circuit in the medial precentral cortex (PrCM) and dorsal striatum (DS). These extralimbic areas receive their HD signals from the limbic system but do not provide critical input or feedback to limbic HD cells (Mehlman ML, Winter SS, Valerio S, Taube JS. J Neurophysiol 121: 350–370, 2019.). In this report, we complement our previous lesion and recording experiments with a series of neuroanatomical tracing studies in rats designed to examine patterns of connectivity between the PrCM, DS, limbic HD circuit, and related spatial processing circuitry. Retrograde tracing revealed that the DS receives direct input from numerous structures known to contain HD cells and/or other spatially tuned cell types. Importantly, these projections preferentially target and converge within the most medial portion of the DS, the same area in which we previously recorded HD cells. The PrCM receives direct input from a subset of these spatial processing structures. Anterograde tracing identified indirect pathways that could permit the PrCM and DS to convey self-motion information to the limbic HD circuit. These tracing studies reveal the anatomical basis for the functional relationships observed in our lesion and recording experiments. Collectively, these findings expand our understanding of how spatial processing circuitry functionally and anatomically extends beyond the limbic system into the PrCM and DS. NEW & NOTEWORTHY Head direction (HD) cells are located primarily within the limbic system, but small populations of extralimbic HD cells are found in the medial precentral cortex (PrCM) and dorsal striatum (DS). The neuroanatomical tracing experiments reported here explored the pathways capable of transmitting the HD signal to these extralimbic areas. We found that projections arising from numerous spatial processing structures converge within portions of the PrCM and DS that contain HD cells.


2005 ◽  
Vol 94 (3) ◽  
pp. 1761-1769 ◽  
Author(s):  
J. Heitwerth ◽  
R. Kern ◽  
J. H. van Hateren ◽  
M. Egelhaaf

Neurons sensitive to visual motion change their response properties during prolonged motion stimulation. These changes have been interpreted as adaptive and were concluded, for instance, to adjust the sensitivity of the visual motion pathway to velocity changes or to increase the reliability of encoding of motion information. These conclusions are based on experiments with experimenter-designed motion stimuli that differ substantially with respect to their dynamical properties from the optic flow an animal experiences during normal behavior. We analyze for the first time motion adaptation under natural stimulus conditions. The experiments are done on the H1-cell, an identified neuron in the blowfly visual motion pathway that has served in many previous studies as a model system for visual motion computation. We reconstructed optic flow perceived by a blowfly in free flight and used this behaviorally generated optic flow to study motion adaptation. A variety of measures (variability in spike count, response latency, jitter of spike timing) suggests that the coding quality does not improve with prolonged stimulation. However, although the number of spikes decreases considerably during stimulation with natural optic flow, the amount of information that is conveyed stays nearly constant. Thus the information per spike increases, and motion adaptation leads to parsimonious coding without sacrificing the reliability with which behaviorally relevant information is encoded.


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