scholarly journals A common directional tuning mechanism of Drosophila motion-sensing neurons in the ON and in the OFF pathway

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.

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.


2003 ◽  
Vol 89 (5) ◽  
pp. 2743-2759 ◽  
Author(s):  
Margaret S. Livingstone ◽  
Bevil R. Conway

We used two-dimensional (2-D) sparse noise to map simultaneous and sequential two-spot interactions in simple and complex direction-selective cells in macaque V1. Sequential-interaction maps for both simple and complex cells showed preferred-direction facilitation and null-direction suppression for same-contrast stimulus sequences and the reverse for inverting-contrast sequences, although the magnitudes of the interactions were weaker for the simple cells. Contrast-sign selectivity in complex cells indicates that direction-selective interactions in these cells must occur in antecedent simple cells or in simple-cell-like dendritic compartments. Our maps suggest that direction selectivity, and on andoff segregation perpendicular to the orientation axis, can occur prior to receptive-field elongation along the orientation axis. 2-D interaction maps for some complex cells showed elongated alternating facilitatory and suppressive interactions as predicted if their inputs were orientation-selective simple cells. The negative interactions, however, were less elongated than the positive interactions, and there was an inflection at the origin in the positive interactions, so the interactions were chevron-shaped rather than band-like. Other complex cells showed only two round interaction regions, one negative and one positive. Several explanations for the map shapes are considered, including the possibility that directional interactions are generated directly from unoriented inputs.


2019 ◽  
Author(s):  
Arunava Banerjee

AbstractWe present a general optimization procedure that given a parameterized network of nonspiking conductance based compartmentally modeled neurons, tunes the parameters to elicit a desired network behavior. Armed with this tool, we address the elementary motion detector problem. Central to established theoretical models, the Hassenstein-Reichardt and Barlow-Levick detectors, are delay lines whose outputs from spatially separated locations are prescribed to be nonlinearly integrated with the direct outputs to engender direction selectivity. The neural implementation of the delays—which are substantial as stipulated by interomatidial angles—has remained elusive although there is consensus regarding the neurons that constitute the network. Assisted by the optimization procedure, we identify parameter settings consistent with the connectivity architecture and physiology of the Drosophila optic lobe, that demonstrates that the requisite delay and the concomitant direction selectivity can emerge from the nonlinear dynamics of small recurrent networks of neurons with simple tonically active synapses. Additionally, although the temporally extended responses of the neurons permit simple synaptic integration of their signals to be sufficient to induce direction selectivity, both preferred direction enhancement and null direction suppression is necessary to abridge the overall response. Finally, the characteristics of the response to drifting sinusoidal gratings are readily explained by the charging-up of the recurrent networks and their low-pass nature.


1991 ◽  
Vol 66 (2) ◽  
pp. 505-529 ◽  
Author(s):  
R. C. Reid ◽  
R. E. Soodak ◽  
R. M. Shapley

1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


2002 ◽  
Vol 88 (2) ◽  
pp. 1026-1039 ◽  
Author(s):  
Steven F. Stasheff ◽  
Richard H. Masland

We recorded from on-off direction-selective ganglion cells (DS cells) in the rabbit retina to investigate in detail the inhibition that contributes to direction selectivity in these cells. Using paired stimuli moving sequentially across the cells' receptive fields in the preferred direction, we directly confirmed the prediction of Wyatt and Daw (1975) that a wave of inhibition accompanies any moving excitatory stimulus on its null side, at a fixed spatial offset. Varying the interstimulus distance, stimulus size, luminance, and speed yielded a spatiotemporal map of the strength of inhibition within this region. This “null” inhibition was maximal at an intermediate distance behind a moving stimulus: ½ to 1½ times the width of the receptive field. The strength of inhibition depended more on the distance behind the stimulus than on stimulus speed, and the inhibition often lasted 1–2 s. These spatial and temporal parameters appear to account for the known spatial frequency and velocity tuning of on-off DS cells to drifting contrast gratings. Stimuli that elicit distinct onand off responses to leading and trailing edges revealed that an excitatory response of either polarity could inhibit a subsequent response of either polarity. For example, an offresponse inhibited either an on or off response of a subsequent stimulus. This inhibition apparently is conferred by a neural element or network spanning the on andoff sublayers of the inner plexiform layer, such as a multistratified amacrine cell. Trials using a stationary flashing spot as a probe demonstrated that the total amount of inhibition conferred on the DS cell was equivalent for stimuli moving in either the null or preferred direction. Apparently the cell does not act as a classic “integrate and fire” neuron, summing all inputs at the soma. Rather, computation of stimulus direction likely involves interactions between excitatory and inhibitory inputs in local regions of the dendrites.


1998 ◽  
Vol 80 (6) ◽  
pp. 2991-3004 ◽  
Author(s):  
Allen L. Humphrey ◽  
Alan B. Saul

Humphrey, Allen L. and Alan B. Saul. Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. J. Neurophysiol. 80: 2991–3004, 1998. Direction selectivity in simple cells of cat area 17 is linked to spatiotemporal (S-T) receptive-field structure. S-T inseparable receptive fields display gradients of response timing across the receptive field that confer a preferred direction of motion. Receptive fields that are not direction selective lack gradients; they are S-T separable, displaying uniform timing across the field. Here we further examine this link using a developmental paradigm that disrupts direction selectivity. Cats were reared from birth to 8 mo of age in 8-Hz stroboscopic illumination. Direction selectivity in simple cells was then measured using gratings drifting at different temporal frequencies (0.25–16 Hz). S-T structure was assessed using stationary bars presented at different receptive-field positions, with bar luminance being modulated sinusoidally at different temporal frequencies. For each cell, plots of response phase versus bar position were fit by lines to characterize S-T inseparability at each temporal frequency. Strobe rearing produced a profound loss of direction selectivity at all temporal frequencies; only 10% of cells were selective compared with 80% in normal cats. The few remaining directional cells were selective over a narrower than normal range of temporal frequencies and exhibited weaker than normal direction selectivity. Importantly, the directional loss was accompanied by a virtual elimination of S-T inseparability. Nearly all cells were S-T separable, like nondirectional cells in normal cats. The loss was clearest in layer 4. Normally, inseparability is greatest there, and it correlates well ( r = 0.77) with direction selectivity; strobe rearing reduced inseparability and direction selectivity to very low values. The few remaining directional cells were inseparable. In layer 6 of normal cats, most direction-selective cells are only weakly inseparable, and there is no consistent relationship between the two measures. However, after strobe rearing, even the weak inseparability was eliminated along with direction selectivity. The correlated changes in S-T structure and direction selectivity were confirmed using conventional linear predictions of directional tuning based on responses to counterphasing bars and white noise stimuli. The developmental changes were permanent, being observed up to 12 yr after strobe rearing. The deficits were remarkably specific; strobe rearing did not affect spatial receptive-field structure, orientation selectivity, spatial or temporal frequency tuning, or general responsiveness to visual stimuli. These results provide further support for a critical role of S-T structure in determining direction selectivity in simple cells. Strobe rearing eliminates directional tuning by altering the timing of responses within the receptive field.


1993 ◽  
Vol 70 (6) ◽  
pp. 2632-2646 ◽  
Author(s):  
D. R. Wylie ◽  
T. Kripalani ◽  
B. J. Frost

1. Extracellular recordings were made from 235 neurons in the vestibulocerebellum (VbC), including the flocculus (lateral VbC), nodulus (folium X), and ventral uvula (ventral folium IXc,d), of the anesthetized pigeon, in response to an optokinetic stimulus. 2. The optokinetic stimuli consisted of two black and white random-dot patterns that were back-projected onto two large tangent screens. The screens were oriented parallel to each other and placed on either side of the bird's head. The resultant stimulus covered the central 100 degrees x 100 degrees of each hemifield. The directional tuning characteristics of each unit were assessed by moving the largefield stimulus in 12 different directions, 30 degrees apart. The directional tuning curves were performed monocularly or binocularly. The binocular directional tuning curves were performed with the direction of motion the same in both eyes (in-phase; e.g., ipsi = upward, contra = upward) or with the direction of motion opposite in either eye (antiphase; e.g., ipsi = upward, contra = downward). 3. Mossy fiber units (n = 17) found throughout folia IXa,b and IXc,d had monocular receptive fields and exhibited direction selectivity in response to stimulation of either the ipsilateral (n = 12) or contralateral (n = 5) eye. None had binocular receptive fields. 4. The complex spike (CS) activity of 218 Purkinje cells in folia IXc,d and X exhibited direction selectivity in response to the large-field visual stimulus moving in one or both visual fields. Ninety-one percent of the cells had binocular receptive fields that could be classified into four groups: descent neurons (n = 112) preferred upward motion in both eyes; ascent neurons (n = 14) preferred downward motion in both eyes; roll neurons (n = 33) preferred upward and downward motion in the ipsilateral and contralateral eyes, respectively; and yaw neurons (n = 40) preferred forward and backward motion in the ipsilateral and contralateral eyes, respectively. Within all groups, most neurons (70%) showed an ipsilateral dominance. 5. For most binocular neurons (91%), the maximum depth of modulation occurred with simultaneous stimulation of both eyes, compared with monocular stimulation of the dominant eye alone. For the translation neurons (descent and ascent), binocular inphase stimulation produced the maximum depth of modulation, whereas for the rotation neurons (roll and yaw), binocular antiphase stimulation produced the maximum depth of modulation. 6. There was a clear functional segregation of the translation and rotation neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


2014 ◽  
Vol 112 (2) ◽  
pp. 362-373 ◽  
Author(s):  
Xiaojuan Hei (黑晓娟) ◽  
Carl R. Stoelzel ◽  
Jun Zhuang (庄骏) ◽  
Yulia Bereshpolova ◽  
Joseph M. Huff ◽  
...  

Directionally selective (DS) neurons are found in the retina and lateral geniculate nucleus (LGN) of rabbits and rodents, and in rabbits, LGN DS cells project to primary visual cortex. Here, we compare visual response properties of LGN DS neurons with those of layer 4 simple cells, most of which show strong direction/orientation selectivity. These populations differed dramatically, suggesting that DS cells may not contribute significantly to the synthesis of simple receptive fields: 1) whereas the first harmonic component (F1)-to-mean firing rate (F0) ratios of LGN DS cells are strongly nonlinear, those of simple cells are strongly linear; 2) whereas LGN DS cells have overlapped ON/OFF subfields, simple cells have either a single ON or OFF subfield or two spatially separate subfields; and 3) whereas the preferred directions of LGN DS cells are closely tied to the four cardinal directions, the directional preferences of simple cells are more evenly distributed. We further show that directional selectivity in LGN DS neurons is strongly enhanced by alertness via two mechanisms, 1) an increase in responses to stimulation in the preferred direction, and 2) an enhanced suppression of responses to stimuli moving in the null direction. Finally, our simulations show that these two consequences of alertness could each serve, in a vector-based population code, to hasten the computation of stimulus direction when rabbits become alert.


Sign in / Sign up

Export Citation Format

Share Document