Photo-ablation of single neurons in the fly visual system reveals neural circuit for the detection of small moving objects

Three motion-sensitive key elements of a neural circuit, presumably involved in processing object and distance information, were analyzed with optic flow sequences as experienced by blowflies in a three-dimensional environment. This optic flow is largely shaped by the blowfly's saccadic flight and gaze strategy, which separates translational flight segments from fast saccadic rotations. By modifying this naturalistic optic flow, all three analyzed neurons could be shown to respond during the intersaccadic intervals not only to nearby objects but also to changes in the distance to background structures. In the presence of strong background motion, the three types of neuron differ in their sensitivity for object motion. Object-induced response increments are largest in FD1, a neuron long known to respond better to moving objects than to spatially extended motion patterns, but weakest in VCH, a neuron that integrates wide-field motion from both eyes and, by inhibiting the FD1 cell, is responsible for its object preference. Small but significant object-induced response increments are present in HS cells, which serve both as a major input neuron of VCH and as output neurons of the visual system. In both HS and FD1, intersaccadic background responses decrease with increasing distance to the animal, although much more prominently in FD1. This strong dependence of FD1 on background distance is concluded to be the consequence of the activity of VCH that dramatically increases its activity and, thus, its inhibitory strength with increasing distance.

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THE VISUAL SYSTEM: A "CHICKEN AND EGG" PROBLEM SOLVED

New Mathematics and Natural Computation ◽

10.1142/s1793005709001337 ◽

2009 ◽

Vol 05 (01) ◽

pp. 115-121

Author(s):

ANDREW R. PARKER ◽

H. JOHN CAULFIELD

Keyword(s):

Visual System ◽

Neural Plasticity ◽

Neural Circuit ◽

Process Data ◽

System A ◽

New Information ◽

The Brain

"What comes first: the chicken or the egg?" Eyes and vision were a great concern for Darwin. Recently, religious fundamentalists have started to attack evolution on the grounds that this is a chicken and egg problem. How could eyes improve without the brain module to use the new information that eye provides? But how could the brain evolve a neural circuit to process data not available to it until a new eye capability emerges? We argue that neural plasticity in the brain allows it to make use of essentially any useful information the eye can produce. And it does so easily within the animal's lifetime. Richard Gregory suggested something like this 40 years ago. Our work resolves a problem with his otherwise-insightful work.

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Optimal Smoothing in Visual Motion Perception

Neural Computation ◽

10.1162/08997660152002843 ◽

2001 ◽

Vol 13 (6) ◽

pp. 1243-1253 ◽

Cited By ~ 38

Author(s):

Rajesh P. N. Rao ◽

David M. Eagleman ◽

Terrence J. Sejnowski

Keyword(s):

Visual System ◽

Moving Objects ◽

Visual Motion ◽

Moving Object ◽

Motion Direction ◽

Visual Motion Perception ◽

Statistical Framework ◽

Lag Effect ◽

Propagation Delays ◽

Optimal Smoothing

When a flash is aligned with a moving object, subjects perceive the flash to lag behind the moving object. Two different models have been proposed to explain this “flash-lag” effect. In the motion extrapolation model, the visual system extrapolates the location of the moving object to counteract neural propagation delays, whereas in the latency difference model, it is hypothesized that moving objects are processed and perceived more quickly than flashed objects. However, recent psychophysical experiments suggest that neither of these interpretations is feasible (Eagleman & Sejnowski, 2000a, 2000b, 2000c), hypothesizing instead that the visual system uses data from the future of an event before committing to an interpretation. We formalize this idea in terms of the statistical framework of optimal smoothing and show that a model based on smoothing accounts for the shape of psychometric curves from a flash-lag experiment involving random reversals of motion direction. The smoothing model demonstrates how the visual system may enhance perceptual accuracy by relying not only on data from the past but also on data collected from the immediate future of an event.

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Cell-type specific patterned stimulus-independent neuronal activity in the Drosophila visual system during synapse formation

10.1101/376871 ◽

2018 ◽

Author(s):

Orkun Akin ◽

Bryce T. Bajar ◽

Mehmet F. Keles ◽

Mark A. Frye ◽

S. Lawrence Zipursky

Keyword(s):

Visual System ◽

Synapse Formation ◽

Neural Circuit ◽

Specific Activity ◽

System Development ◽

Nervous System Development ◽

Adult Brain ◽

Cell Type ◽

Cell Type Specific

SummaryStereotyped synaptic connections define the neural circuits of the brain. In vertebrates, stimulus-independent activity contributes to neural circuit formation. It is unknown whether this type of activity is a general feature of nervous system development. Here, we report patterned, stimulus-independent neural activity in the Drosophila visual system during synaptogenesis. Using in vivo calcium, voltage, and glutamate imaging, we found that all neurons participate in this spontaneous activity, which is characterized by brain-wide periodic active and silent phases. Glia are active in a complementary pattern. Each of the 15 examined of the over 100 specific neuron types in the fly visual system exhibited a unique activity signature. The activity of neurons that are synaptic partners in the adult was highly correlated during development. We propose that this cell type-specific activity coordinates the development of the functional circuitry of the adult brain.

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CUB and Sushi Multiple Domains 1 (CSMD1) opposes the complement cascade in neural tissues

10.1101/2020.09.11.291427 ◽

2020 ◽

Author(s):

Matthew L. Baum ◽

Daniel K. Wilton ◽

Allie Muthukumar ◽

Rachel G. Fox ◽

Alanna Carey ◽

...

Keyword(s):

Visual System ◽

Cortical Neurons ◽

Neural Circuit ◽

Ex Vivo ◽

Embryonic Stem ◽

Gene Copy Number ◽

Gene Copy ◽

Complement Cascade ◽

Neural Tissues ◽

Complement Component 4

AbstractSchizophrenia risk is associated with increased gene copy number and brain expression of complement component 4 (C4). Because the complement system facilitates synaptic pruning, the C4 association has renewed interest in a hypothesis that excessive pruning contributes to schizophrenia pathogenesis. However, little is known about complement regulation in neural tissues or whether such regulation could be relevant to psychiatric illness. Intriguingly, common variation within CSMD1, which encodes a putative complement inhibitor, has consistently associated with schizophrenia at genome-wide significance. We found that Csmd1 is predominantly expressed in the brain by neurons, and is enriched at synapses; that human stem cell-derived neurons lacking CSMD1 are more vulnerable to complement deposition; and that mice lacking Csmd1 have increased brain complement activity, fewer synapses, aberrant complement-dependent development of a neural circuit, and synaptic elements that are preferentially engulfed by cultured microglia. These data suggest that CSMD1 opposes the complement cascade in neural tissues.Graphic Abstract.Our findings support a model in which CSMD1 opposes actions of the complement cascade in neural tissues (top left). We investigated two models in which Csmd1 was genetically ablated: human cortical neurons derived from embryonic stem cells, and a back-crossed C57bl6-Tac mouse line (top right). Csmd1 is normally expressed by neurons and present at synapses where it can protect them from complement (bottom left); in the absence of Csmd1 (bottom right), we find more deposition of complement (on cultured human cortical neurons and in the mouse visual system), reduced numbers of synapses (in the mouse visual system), and synaptic fractions that are more readily engulfed by microglia (ex vivo). Created with BioRender.com.

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Compensating time delays with neural predictions: are predictions sensory or motor?

Philosophical Transactions of The Royal Society A Mathematical Physical and Engineering Sciences ◽

10.1098/rsta.2008.0270 ◽

2009 ◽

Vol 367 (1891) ◽

pp. 1063-1078 ◽

Cited By ~ 33

Author(s):

Romi Nijhawan ◽

Si Wu

Keyword(s):

Visual System ◽

Visual Information ◽

Moving Objects ◽

Early Stage ◽

Adaptive Behaviour ◽

Neural Pathways ◽

Neural Signals ◽

Multiple Resources ◽

Compensation Mechanisms ◽

The Future

Neural delays are a general property of computations carried out by neural circuits. Delays are a natural consequence of temporal summation and coding used by the nervous system to integrate information from multiple resources. For adaptive behaviour, however, these delays must be compensated. In order to sense and interact with moving objects, for example, the visual system must predict the future position of the object to compensate for delays. In this paper, we address two critical questions concerning the implementation of the compensation mechanisms in the brain, namely, where does compensation occur and how is it realized. We present evidence showing that compensation can happen in both the motor and sensory systems, and that compensation using ‘diagonal neural pathways’ is a suitable strategy for implementing compensation in the visual system. In this strategy, neural signals in the early stage of information processing are sent to the future cortical positions that correspond to the distance the object will travel in the period of transmission delay. We propose a computational model to elucidate this using the retinal visual information pathway.

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Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques

Journal of Neurophysiology ◽

10.1152/jn.1993.69.2.329 ◽

1993 ◽

Vol 69 (2) ◽

pp. 329-339 ◽

Cited By ~ 65

Author(s):

A. K. Warzecha ◽

M. Egelhaaf ◽

A. Borst

Keyword(s):

Visual Field ◽

Moving Objects ◽

Neural Circuit ◽

Response Characteristic ◽

Large Field ◽

Small Field ◽

Gamma Aminobutyric Acid ◽

Ventral Part ◽

Specific Selectivity

1. Visual interneurons tuned to the motion of small objects are found in many animal species and are assumed to be the neuronal basis of figure-ground discrimination by relative motion. A well-examined example is the FD1-cell in the third visual neuropil of blowflies. This cell type responds best to motion of small objects. Motion of extended patterns elicits only small responses. As a neuronal mechanism that leads to such a response characteristic, it was proposed that the FD1-cell is inhibited by the two presumably GABAergic and, thus, inhibitory CH-cells, the VCH- and the DCH-cell. The CH-cells respond best to exactly that type of motion by which the activity of the FD1-cell is reduced. The hypothesis that the CH-cells inhibit the FD1-cell and, thus, mediate its selectivity to small moving objects was tested by ablating the CH-cells either pharmacologically or by photoinactivation. 2. After application of the gamma-aminobutyric acid (GABA) antagonist picrotoxinin, the FD1-cell responds more strongly to large-field than to small-field motion, i.e., it has lost its small-field selectivity. This suggests that the tuning of the FD1-cell to small moving objects relies on a GABAergic mechanism and, thus, most likely on the CH-cells. 3. The role of each CH-cell for small-field tuning was determined by inactivating them individually. They were injected with a fluorescent dye and then ablated by laser illumination. Only photoinactivation of the VCH-cell eliminated the specific selectivity of the FD1-cell for small-field motion. Ablation of the DCH-cell did not significantly change the response characteristic of the FD1-cell. This reveals the important role of the VCH-cells in mediating the characteristic sensitivity of the FD1-cell to motion of small objects. 4. The FD1-cell is most sensitive to motion of small objects in the ventral part of the ipsilateral visual field, whereas motion in the dorsal part influences the cell only weakly. This specific feature fits well to the sensitivity of the VCH-cell to ipsilateral motion that is most pronounced in the ventral part of the visual field. The spatial sensitivity distribution of the FD1-cell matches also the characteristics of figure-ground discrimination and fixation behavior.

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Feature Fusion Reveals Slow and Fast Visual Memories

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2007.19.4.632 ◽

2007 ◽

Vol 19 (4) ◽

pp. 632-641 ◽

Cited By ~ 18

Author(s):

Frank Scharnowski ◽

Frouke Hermens ◽

Thomas Kammer ◽

Haluk Öğmen ◽

Michael H. Herzog

Keyword(s):

Visual System ◽

Moving Objects ◽

Short Term Memory ◽

Feature Fusion ◽

Temporal Integration ◽

Substantial Part ◽

Short Term ◽

Visual Short Term Memory ◽

Short Time

Although the visual system can achieve a coarse classification of its inputs in a relatively short time, the synthesis of qualia-rich and detailed percepts can take substantially more time. If these prolonged computations were to take place in a retinotopic space, moving objects would generate extensive smear. However, under normal viewing conditions, moving objects appear relatively sharp and clear, suggesting that a substantial part of visual short-term memory takes place at a nonretinotopic locus. By using a retinotopic feature fusion and a nonretinotopic feature attribution paradigm, we provide evidence for a relatively fast retinotopic buffer and a substantially slower nonretinotopic memory. We present a simple model that can account for the dynamics of these complementary memory processes. Taken together, our results indicate that the visual system can accomplish temporal integration of information while avoiding smear by breaking off sensory memory into fast and slow components that are implemented in retinotopic and nonretinotopic loci, respectively.

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Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system

PLoS Genetics ◽

10.1371/journal.pgen.1009857 ◽

2021 ◽

Vol 17 (11) ◽

pp. e1009857

Author(s):

Weiyue Ji ◽

Lani F. Wu ◽

Steven J. Altschuler

Keyword(s):

Visual System ◽

Neural Circuit ◽

Growth Cones ◽

Local Regularity ◽

Tissue Organization ◽

Cellular Behaviors ◽

Neural Superposition ◽

The Right ◽

Circuit Formation

A fascinating question in neuroscience is how ensembles of neurons, originating from different locations, extend to the proper place and by the right time to create precise circuits. Here, we investigate this question in the Drosophila visual system, where photoreceptors re-sort in the lamina to form the crystalline-like neural superposition circuit. The repeated nature of this circuit allowed us to establish a data-driven, standardized coordinate system for quantitative comparison of sparsely perturbed growth cones within and across specimens. Using this common frame of reference, we investigated the extension of the R3 and R4 photoreceptors, which is the only pair of symmetrically arranged photoreceptors with asymmetric target choices. Specifically, we found that extension speeds of the R3 and R4 growth cones are inherent to their cell identities. The ability to parameterize local regularity in tissue organization facilitated the characterization of ensemble cellular behaviors and dissection of mechanisms governing neural circuit formation.

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Birth order dependent growth cone segregation determines synaptic layer identity in the Drosophila visual system

eLife ◽

10.7554/elife.13715 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 33

Author(s):

Abhishek Kulkarni ◽

Deniz Ertekin ◽

Chi-Hon Lee ◽

Thomas Hummel

Keyword(s):

Visual System ◽

Birth Order ◽

Growth Cone ◽

Neural Circuit ◽

Growth Cones ◽

Initial Growth ◽

Developmental Context ◽

Differential Positioning ◽

Dependent Growth ◽

Relative Differences

The precise recognition of appropriate synaptic partner neurons is a critical step during neural circuit assembly. However, little is known about the developmental context in which recognition specificity is important to establish synaptic contacts. We show that in the Drosophila visual system, sequential segregation of photoreceptor afferents, reflecting their birth order, lead to differential positioning of their growth cones in the early target region. By combining loss- and gain-of-function analyses we demonstrate that relative differences in the expression of the transcription factor Sequoia regulate R cell growth cone segregation. This initial growth cone positioning is consolidated via cell-adhesion molecule Capricious in R8 axons. Further, we show that the initial growth cone positioning determines synaptic layer selection through proximity-based axon-target interactions. Taken together, we demonstrate that birth order dependent pre-patterning of afferent growth cones is an essential pre-requisite for the identification of synaptic partner neurons during visual map formation in Drosophila.

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