scholarly journals How fly neurons compute the direction of visual motion

2019 ◽  
Vol 206 (2) ◽  
pp. 109-124 ◽  
Author(s):  
Alexander Borst ◽  
Jürgen Haag ◽  
Alex S. Mauss

Abstract Detecting the direction of image motion is a fundamental component of visual computation, essential for survival of the animal. However, at the level of individual photoreceptors, the direction in which the image is shifting is not explicitly represented. Rather, directional motion information needs to be extracted from the photoreceptor array by comparing the signals of neighboring units over time. The exact nature of this process as implemented in the visual system of the fruit fly Drosophila melanogaster has been studied in great detail, and much progress has recently been made in determining the neural circuits giving rise to directional motion information. The results reveal the following: (1) motion information is computed in parallel ON and OFF pathways. (2) Within each pathway, T4 (ON) and T5 (OFF) cells are the first neurons to represent the direction of motion. Four subtypes of T4 and T5 cells exist, each sensitive to one of the four cardinal directions. (3) The core process of direction selectivity as implemented on the dendrites of T4 and T5 cells comprises both an enhancement of signals for motion along their preferred direction as well as a suppression of signals for motion along the opposite direction. This combined strategy ensures a high degree of direction selectivity right at the first stage where the direction of motion is computed. (4) At the subsequent processing stage, tangential cells spatially integrate direct excitation from ON and OFF-selective T4 and T5 cells and indirect inhibition from bi-stratified LPi cells activated by neighboring T4/T5 terminals, thus generating flow-field-selective responses.

2020 ◽  
Vol 114 (4-5) ◽  
pp. 443-460
Author(s):  
Qinbing Fu ◽  
Shigang Yue

Abstract Decoding the direction of translating objects in front of cluttered moving backgrounds, accurately and efficiently, is still a challenging problem. In nature, lightweight and low-powered flying insects apply motion vision to detect a moving target in highly variable environments during flight, which are excellent paradigms to learn motion perception strategies. This paper investigates the fruit fly Drosophila motion vision pathways and presents computational modelling based on cutting-edge physiological researches. The proposed visual system model features bio-plausible ON and OFF pathways, wide-field horizontal-sensitive (HS) and vertical-sensitive (VS) systems. The main contributions of this research are on two aspects: (1) the proposed model articulates the forming of both direction-selective and direction-opponent responses, revealed as principal features of motion perception neural circuits, in a feed-forward manner; (2) it also shows robust direction selectivity to translating objects in front of cluttered moving backgrounds, via the modelling of spatiotemporal dynamics including combination of motion pre-filtering mechanisms and ensembles of local correlators inside both the ON and OFF pathways, which works effectively to suppress irrelevant background motion or distractors, and to improve the dynamic response. Accordingly, the direction of translating objects is decoded as global responses of both the HS and VS systems with positive or negative output indicating preferred-direction or null-direction translation. The experiments have verified the effectiveness of the proposed neural system model, and demonstrated its responsive preference to faster-moving, higher-contrast and larger-size targets embedded in cluttered moving backgrounds.


2020 ◽  
Vol 6 (1) ◽  
pp. 335-362
Author(s):  
Tatiana Pasternak ◽  
Duje Tadin

Psychophysical and neurophysiological studies of responses to visual motion have converged on a consistent set of general principles that characterize visual processing of motion information. Both types of approaches have shown that the direction and speed of target motion are among the most important encoded stimulus properties, revealing many parallels between psychophysical and physiological responses to motion. Motivated by these parallels, this review focuses largely on more direct links between the key feature of the neuronal response to motion, direction selectivity, and its utilization in memory-guided perceptual decisions. These links were established during neuronal recordings in monkeys performing direction discriminations, but also by examining perceptual effects of widespread elimination of cortical direction selectivity produced by motion deprivation during development. Other approaches, such as microstimulation and lesions, have documented the importance of direction-selective activity in the areas that are active during memory-guided direction comparisons, area MT and the prefrontal cortex, revealing their likely interactions during behavioral tasks.


2001 ◽  
Vol 86 (2) ◽  
pp. 997-1005 ◽  
Author(s):  
M. R. Ibbotson ◽  
C.W.G. Clifford

An apparent motion stimulus is used to probe the interactions between signals representing brightness increments (on stimuli) and decrements (off stimuli) in the directional motion detectors forming the input to the nucleus of the optic tract (NOT) of the wallaby, Macropus eugenii. Direction-selective NOT neurons increase their firing rates during image motion from temporal-to-nasal over the contralateral eye (preferred direction) and their spontaneous activities are inhibited by motion in the opposite, anti-preferred direction. An apparent motion stimulus, consisting of neighboring vertical bars, where the brightness can be manipulated independently, also produces directional responses. Preferred direction sequences of brightness changes of like polarities (on-onor off-off) produce increased firing rates while sequences of opposite polarities (on-offor off-on) in the same direction produce relatively small excitatory responses or inhibit the spontaneous rate. For apparent motion in the anti-preferred direction, these directional properties are reversed, showing that signals for brightness increments and decrements provide inputs to the same motion detectors. There is no evidence for segregation of motion detectors into those receiving only half-wave rectified inputs. Interactions between on andoff signals utilize the sign of the incoming signals. An array of Reichardt-type motion detectors receiving inputs represented as positive and negative values for on and offstimuli, respectively, are used to simulate the NOT responses. The brightness signals enter band-pass temporal filters prior to motion detection. By altering the time constants of these prefilters, it was possible to accurately simulate the time courses of each cell's responses.


2000 ◽  
Vol 84 (4) ◽  
pp. 1914-1923 ◽  
Author(s):  
Rafael Kurtz ◽  
Volker Dürr ◽  
Martin Egelhaaf

Motion adaptation in directionally selective tangential cells (TC) of the fly visual system has previously been explained as a presynaptic mechanism. Based on the observation that adaptation is in part direction selective, which is not accounted for by the former models of motion adaptation, we investigated whether physiological changes located in the TC dendrite can contribute to motion adaptation. Visual motion in the neuron's preferred direction (PD) induced stronger adaptation than motion in the opposite direction and was followed by an afterhyperpolarization (AHP). The AHP subsides in the same time as adaptation recovers. By combining in vivo calcium fluorescence imaging with intracellular recording, we show that dendritic calcium accumulation following motion in the PD is correlated with the AHP. These results are consistent with a calcium-dependent physiological change in TCs underlying adaptation during continuous stimulation with PD motion, expressing itself as an AHP after the stimulus stops. However, direction selectivity of adaptation is probably not solely related to a calcium-dependent mechanism because direction-selective effects can also be observed for fast moving stimuli, which do not induce sizeable calcium accumulation. In addition, a comparison of two classes of TCs revealed differences in the relationship of calcium accumulation and AHP when the stimulus velocity was varied. Thus the potential role of calcium in motion adaptation depends on stimulation parameters and cell class.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Juergen Haag ◽  
Alexander Arenz ◽  
Etienne Serbe ◽  
Fabrizio Gabbiani ◽  
Alexander Borst

How neurons become sensitive to the direction of visual motion represents a classic example of neural computation. Two alternative mechanisms have been discussed in the literature so far: preferred direction enhancement, by which responses are amplified when stimuli move along the preferred direction of the cell, and null direction suppression, where one signal inhibits the response to the subsequent one when stimuli move along the opposite, i.e. null direction. Along the processing chain in the Drosophila optic lobe, directional responses first appear in T4 and T5 cells. Visually stimulating sequences of individual columns in the optic lobe with a telescope while recording from single T4 neurons, we find both mechanisms at work implemented in different sub-regions of the receptive field. This finding explains the high degree of directional selectivity found already in the fly’s primary motion-sensing neurons and marks an important step in our understanding of elementary motion detection.


e-Neuroforum ◽  
2012 ◽  
Vol 18 (3) ◽  
Author(s):  
T. Euler ◽  
S.E. Hausselt

AbstractHow direction of image motion is detected as early as at the level of the vertebrate eye has been intensively studied in retina research. Although the first direction-selective (DS) ret­inal ganglion cells were already described in the 1960s and have since then been in the fo­cus of many studies, scientists are still puz­zled by the intricacy of the neuronal circuits and computational mechanisms underlying retinal direction selectivity. The fact that the retina can be easily isolated and studied in a Petri dish-by presenting light stimuli while recording from the various cell types in the retinal circuits-in combination with the ex­tensive anatomical, molecular and physiolog­ical knowledge about this part of the brain presents a unique opportunity for studying this intriguing visual circuit in detail. This ar­ticle provides a brief overview of the histo­ry of research on retinal direction selectivi­ty, but then focuses on the past decade and the progress achieved, in particular driven by methodological advances in optical record­ing techniques, molecular genetics approach­es and large-scale ultrastructural reconstruc­tions. As it turns out, retinal direction selec­tivity is a complex, multi-tiered computation, involving dendrite-intrinsic mechanisms as well as several types of network interactions on the basis of highly selective, likely genet­ically predetermined synaptic connectivi­ty. Moreover, DS ganglion cell types appear to be more diverse than previously thought, differing not only in their preferred direction and response polarity, but also in physiology, DS mechanism, dendritic morphology and, importantly, the target area of their projec­tions in the brain.


1983 ◽  
Vol 49 (5) ◽  
pp. 1127-1147 ◽  
Author(s):  
J. H. Maunsell ◽  
D. C. Van Essen

1. Recordings were made from single units in the middle temporal visual area (MT) of anesthetized, paralyzed macaque monkeys. A computer-driven stimulator was used to make quantitative tests of selectivity for stimulus direction, speed, and orientation. The data were taken from 168 units that were histologically identified as being in MT. 2. The results confirm previous reports of a high degree of direction selectivity in MT. The response above background to stimuli moving in a unit's preferred direction was, an average, 10.9 times that to stimuli moving in the opposite direction. There was a marked tendency for nearby units to have similar preferred directions. 3. Most units were also sharply tuned for the speed of stimulus motion. For some cells the response fell to less than half-maximal at speeds only a factor of two from the optimum; on average, responses were greater than half-maximal only over a 7.7-fold range of speed. The distribution of preferred speeds for different units was unimodal, with a peak near 32 degrees/s; the total range of preferred speeds extended from 2 to 256 degrees/s. Nearby units generally responded best to similar speeds of motion. 4. Most units in MT showed selectivity for stimulus orientation when tested with stationary, flashed bars. However, stationary stimuli generally elicited only brief responses; when averaged over the duration of the stimulus, the responses were much less than those to moving stimuli. The preferred orientation was usually, but not always, perpendicular to the preferred direction of movement. 5. A comparison of the results of the present study with a previous quantitative investigation in the owl monkey shows a striking similarity in response properties in MT of the two species. 6. The presence of both direction and speed selectivity in MT of the macaque suggests that this area is more specialized for the analysis of visual motion than has been previously recognized.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Juergen Haag ◽  
Abhishek Mishra ◽  
Alexander Borst

In the fruit fly optic lobe, T4 and T5 cells represent the first direction-selective neurons, with T4 cells responding selectively to moving brightness increments (ON) and T5 cells to brightness decrements (OFF). Both T4 and T5 cells comprise four subtypes with directional tuning to one of the four cardinal directions. We had previously found that upward-sensitive T4 cells implement both preferred direction enhancement and null direction suppression (Haag et al., 2016). Here, we asked whether this mechanism generalizes to OFF-selective T5 cells and to all four subtypes of both cell classes. We found that all four subtypes of both T4 and T5 cells implement both mechanisms, that is preferred direction enhancement and null direction inhibition, on opposing sides of their receptive fields. This gives rise to the high degree of direction selectivity observed in both T4 and T5 cells within each subpopulation.


1996 ◽  
Vol 76 (3) ◽  
pp. 1786-1799 ◽  
Author(s):  
T. M. Brotz ◽  
A. Borst

1. To identify some of the neurotransmitters involved in the processing of visual motion information the pharmacology of transmitter receptors on motion-sensitive visual interneurons (VS and HS cells) was investigated in an in vitro preparation of the blowfly (Calliphora erythrocephala) brain. Cholinergic and GABAergic drugs were applied in the bath and iontophoretically while recording intracellularly from HS and VS cells. 2. Bath-applied carbachol (10 and 100 microM) leads to a depolarization in HS and VS cells. One micromolar nicotine also has a depolarizing effect. Both agonists are effective in 0 Ca2+/high Mg(2+)-saline, too, which isolates the cells synaptically. The muscarinic agonists pilocarpine and oxotremorine have no effects on the membrane potential. 3. Iontophoretic application of acetylcholine, carbachol, and nicotine depolarizes VS and HS cells. The iontophoretic carbachol response is antagonized by alpha-bungarotoxin (EC50 = 0.19 microM), mecamylamine (EC50 = 0.32 microM), d-tubocurarine (EC50 = 9.5 microM), and bicuculline but not by decamethonium and scopolamine. 4. Bath application of muscimol strongly hyperpolarizes VS cells in normal fly saline. The gamma-aminobutyric acid-C (GABAC)-receptor agonist cis-4-aminocrotonic acid (CACA) has no effects. The hyperpolarizing response to iontophoretic applied muscimol is present in 0 Ca2+/high Mg2+ saline as well as in Co(2+)-containing saline. The muscimol response is reduced in low chloride saline and thus chloride sensitive. The muscimol response is blocked by picrotoxinin (EC50 = 3.4 microM) but not by the GABAA receptor antagonist bicuculline. 5. Taken together the primary responses of the lobula plate tangential cells appear to be nicotinic cholinergic and GABAergic. 6. The pharmacology of natural synaptic input to VS cells was investigated by extracellular electrical stimulation of the medulla. Such evoked excitatory postsynaptic potentials (EPSPs) are blocked reversibly in 0 Ca2+/high Mg2+ saline. The nicotinic antagonists mecamylamine (1 microM) and d-tubocurarine (50-100 microM) abolish or diminish the EPSPs, respectively. 7. The pharmacological data are incorporated into a semicellular model of a visual motion detector favoring a role of lobula plate tangential cells in certain steps of visual motion processing. Cholinergic and GABAergic inputs are an ideal cellular implementation of a linear subtraction of the signals arising from local motion-sensitive elements with opposite preferred direction. Such a mechanism enhances direction-selectivity and, together with dendritic integration, increases the sensitivity of the tangential cells for wide-field motion.


2005 ◽  
Vol 94 (6) ◽  
pp. 4156-4167 ◽  
Author(s):  
Daniel Zaksas ◽  
Tatiana Pasternak

Neurons in cortical area MT have localized receptive fields (RF) representing the contralateral hemifield and play an important role in processing visual motion. We recorded the activity of these neurons during a behavioral task in which two monkeys were required to discriminate and remember visual motion presented in the ipsilateral hemifield. During the task, the monkeys viewed two stimuli, sample and test, separated by a brief delay and reported whether they contained motion in the same or in opposite directions. Fifty to 70% of MT neurons were activated by the motion stimuli presented in the ipsilateral hemifield at locations far removed from their classical receptive fields. These responses were in the form of excitation or suppression and were delayed relative to conventional MT responses. Both excitatory and suppressive responses were direction selective, but the nature and the time course of their directionality differed from the conventional excitatory responses recorded with stimuli in the RF. Direction selectivity of the excitatory remote response was transient and early, whereas the suppressive response developed later and persisted after stimulus offset. The presence or absence of these unusual responses on error trials, as well as their magnitude, was affected by the behavioral significance of stimuli used in the task. We hypothesize that these responses represent top-down signals from brain region(s) accessing information about stimuli in the entire visual field and about the behavioral state of the animal. The recruitment of neurons in the opposite hemisphere during processing of behaviorally relevant visual signals reveals a mechanism by which sensory processing can be affected by cognitive task demands.


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