Direction Selectivity in Drosophila Emerges from Preferred-Direction Enhancement and Null-Direction Suppression

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.

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An Optimization framework for Nonspiking Neuronal Networks and Aided Discovery of a Model for the Elementary Motion Detector

10.1101/666149 ◽

2019 ◽

Author(s):

Arunava Banerjee

Keyword(s):

Optic Lobe ◽

Optimization Procedure ◽

Theoretical Models ◽

Direction Selectivity ◽

Recurrent Networks ◽

Motion Detector ◽

Null Direction ◽

Optimization Framework ◽

Preferred Direction ◽

Low Pass

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.

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Complementary mechanisms create direction selectivity in the fly

eLife ◽

10.7554/elife.17421 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 54

Author(s):

Juergen Haag ◽

Alexander Arenz ◽

Etienne Serbe ◽

Fabrizio Gabbiani ◽

Alexander Borst

Keyword(s):

Motion Detection ◽

Visual Motion ◽

Optic Lobe ◽

Direction Selectivity ◽

Neural Computation ◽

Directional Selectivity ◽

Motion Sensing ◽

Null Direction ◽

Preferred Direction ◽

High Degree

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.

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Spatially displaced excitation contributes to the encoding of interrupted motion by the retinal direction-selective circuit

10.1101/2020.05.29.124461 ◽

2020 ◽

Author(s):

Jennifer Ding ◽

Albert Chen ◽

Janet Chung ◽

Hector Acaron Ledesma ◽

David M. Berson ◽

...

Keyword(s):

Ganglion Cells ◽

Spatial Location ◽

Direction Selectivity ◽

Natural Scenes ◽

Visual Response ◽

Null Direction ◽

Motion Trajectories ◽

Preferred Direction ◽

Synchronous Firing ◽

Spatially Distributed

AbstractSpatially distributed excitation and inhibition collectively shape a visual neuron’s receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the effects of strong null-direction inhibition of On-Off direction-selective ganglion cells (ON-OFF DSGCs) on their direction selectivity are well-studied. However, how excitatory inputs influence the On-Off DSGC’s visual response is underexplored. Here, we report that the glutamatergic excitation of On-Off DSGCs shows a spatial displacement to the side where preferred-direction motion stimuli approach the soma (the ‘preferred side’). Underlying this displacement is a non-uniform distribution of excitatory conductance across the dendritic span of the DSGC on the preferred-null motion axis. The skewed excitatory RF contributes to robust null-direction spiking during RF activation limited to the preferred side, a potential ethologically relevant signal to encode interrupted or discontinuous motion trajectories abundant in natural scenes. Theoretical analysis indicates that such differential firing patterns of On-Off DSGCs to continuous and interrupted motion stimuli may help leverage synchronous firing to signal the spatial location of a moving object in complex, naturalistic visual environments. Our study highlights that visual circuitry, even the well-defined direction-selective circuit, exploits different sets of neural mechanisms under different stimulus conditions to generate context-dependent neural representations of visual features.

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

eLife ◽

10.7554/elife.29044 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 22

Author(s):

Juergen Haag ◽

Abhishek Mishra ◽

Alexander Borst

Keyword(s):

Optic Lobe ◽

Receptive Fields ◽

Fruit Fly ◽

Direction Selectivity ◽

Motion Sensing ◽

Null Direction ◽

Directional Tuning ◽

Tuning Mechanism ◽

Preferred Direction ◽

High Degree

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.

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Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT

Journal of Neurophysiology ◽

10.1152/jn.1986.55.6.1308 ◽

1986 ◽

Vol 55 (6) ◽

pp. 1308-1327 ◽

Cited By ~ 222

Author(s):

A. Mikami ◽

W. T. Newsome ◽

R. H. Wurtz

Keyword(s):

Discharge Rate ◽

Direction Selectivity ◽

Peak Discharge ◽

Spontaneous Discharge ◽

Null Direction ◽

Area Mt ◽

Mt Neurons ◽

Preferred Direction ◽

Single Flash ◽

Temporal Intervals

Mechanisms of direction selectivity and speed selectivity were studied in single neurons of the middle temporal visual area (MT) of behaving macaque monkeys. Visual stimuli were presented in both smooth and stroboscopic motion within a neuron's receptive field as the monkey fixated a stationary point of light. Direction selectivity, speed selectivity, and the spontaneous discharge characteristics of MT neurons in behaving monkeys were similar to those reported in previous studies in anesthetized monkeys. Stroboscopic motion stimuli were sequences of flashes characterized by the spatial and temporal intervals between each flash. The spatial and temporal intervals were systematically varied so that suppressive and facilitatory interactions could be studied in both the preferred and null directions. Suppression and facilitation were measured by subtracting the peak discharge rate elicited by a single flash from the peak discharge rate elicited by a stroboscopic train of flashes. The dominant mechanism of direction selectivity in MT was a pronounced suppression of discharge for motion in the null direction which we interpreted as inhibition. The inhibition was sufficiently potent to abolish the responses to single flashed stimuli when they were embedded in a series of flashes in the null direction, and it frequently reduced the neuronal discharge to a level below the spontaneous firing rate. Facilitation in the preferred direction was a prominent feature of the responses of some, but not all, MT neurons. The peak discharge rate for stroboscopic motion in the preferred direction was more than twice the peak rate to a single flash for approximately 50% of the neurons in our sample. The direction selectivity of most MT neurons showed the effects of both inhibitory and facilitatory mechanisms, and it was not possible to segregate MT neurons into distinct groups on the basis of these measures. Suppressive mechanisms contributed to speed tuning as well as direction tuning. The low-speed cutoff for motion in the preferred direction resulted from suppression in 82% of the neurons tested. The high-speed cutoff resulted from suppression in 32% of the neurons tested. The latter mechanism appeared to be distinct from the inhibitory mechanism which acted in the null direction in that large spatial intervals were required for its activation.

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Modeling simple-cell direction selectivity with normalized, half-squared, linear operators

Journal of Neurophysiology ◽

10.1152/jn.1993.70.5.1885 ◽

1993 ◽

Vol 70 (5) ◽

pp. 1885-1898 ◽

Cited By ~ 125

Author(s):

D. J. Heeger

Keyword(s):

Linear Prediction ◽

Direction Selectivity ◽

Linear Operators ◽

Simple Cell ◽

Physiological Data ◽

Simple Cells ◽

Cell Responses ◽

Preferred Direction ◽

Model Cell ◽

Actual Response

1. A longstanding view of simple cells is that they sum their inputs linearly. However, the linear model falls short of a complete account of simple-cell direction selectivity. We have developed a nonlinear model of simple-cell responses (hereafter referred to as the normalization model) to explain a larger body of physiological data. 2. The normalization model consists of an underlying linear stage along with two additional nonlinear stages. The first is a half-squaring nonlinearity; half-squaring is half-wave rectification followed by squaring. The second is a divisive normalization non-linearity in which each model cell is suppressed by the pooled activity of a large number of cells. 3. By comparing responses with counterphase (flickering) gratings and drifting gratings, researchers have demonstrated that there is a nonlinear contribution to simple-cell responses. Specifically they found 1) that the linear prediction from counterphase grating responses underestimates a direction index computed from drifting grating responses, 2) that the linear prediction correctly estimates responses to gratings drifting in the preferred direction, and 3) that the linear prediction overestimates responses to gratings drifting in the nonpreferred direction. 4. We have simulated model cell responses and derived mathematical expressions to demonstrate that the normalization model accounts for this empirical data. Specifically the model behaves as follows. 1) The linear prediction from counterphase data underestimates the direction index computed from drifting grating responses. 2) The linear prediction from counterphase data overestimates the response to gratings drifting in the nonpreferred direction. The discrepancy between the linear prediction and the actual response is greater when using higher contrast stimuli. 3) For an appropriate choice of contrast, the linear prediction from counterphase data correctly estimates the response to gratings drifting in the preferred direction. For higher contrasts the linear prediction overestimates the actual response, and for lower contrasts the linear prediction underestimates the actual response. 5. In addition, the normalization model is qualitatively consistent with data on the dynamics of simple-cell responses. Tolhurst et al. found that simple cells respond with an initial transient burst of activity when a stimulus first appears. The normalization model behaves similarly; it takes some time after a stimulus first appears before the model cells are fully normalized. We derived the dynamics of the model and found that the transient burst of activity in model cells depends in a particular way on stimulus contrast. The burst is short for high-contrast stimuli and longer for low-contrast stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

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Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex

Journal of Neurophysiology ◽

10.1152/jn.1991.66.2.505 ◽

1991 ◽

Vol 66 (2) ◽

pp. 505-529 ◽

Cited By ~ 149

Author(s):

R. C. Reid ◽

R. E. Soodak ◽

R. M. Shapley

Keyword(s):

Time Course ◽

Linear Prediction ◽

Striate Cortex ◽

Receptive Fields ◽

Quantitative Measure ◽

Direction Selectivity ◽

Simple Cells ◽

Preferred Direction ◽

Orientation Contrast ◽

Cat Striate Cortex

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)

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Weighting neurons by selectivity produces near-optimal population codes

Journal of Neurophysiology ◽

10.1152/jn.00504.2018 ◽

2019 ◽

Vol 121 (5) ◽

pp. 1924-1937

Author(s):

Elizabeth Zavitz ◽

Nicholas S. C. Price

Keyword(s):

A Priori ◽

Maximum Level ◽

Optimization Methods ◽

Neuronal Population ◽

Direction Selectivity ◽

Motion Direction ◽

Temporal Area ◽

Linear Discriminant ◽

Preferred Direction

Perception is produced by “reading out” the representation of a sensory stimulus contained in the activity of a population of neurons. To examine experimentally how populations code information, a common approach is to decode a linearly weighted sum of the neurons’ spike counts. This approach is popular because of the biological plausibility of weighted, nonlinear integration. For neurons recorded in vivo, weights are highly variable when derived through optimization methods, but it is unclear how the variability affects decoding performance in practice. To address this, we recorded from neurons in the middle temporal area (MT) of anesthetized marmosets ( Callithrix jacchus) viewing stimuli comprising a sheet of dots that moved coherently in 1 of 12 different directions. We found that high peak response and direction selectivity both predicted that a neuron would be weighted more highly in an optimized decoding model. Although learned weights differed markedly from weights chosen according to a priori rules based on a neuron’s tuning profile, decoding performance was only marginally better for the learned weights. In the models with a priori rules, selectivity is the best predictor of weighting, and defining weights according to a neuron’s preferred direction and selectivity improves decoding performance to very near the maximum level possible, as defined by the learned weights. NEW & NOTEWORTHY We examined which aspects of a neuron’s tuning account for its contribution to sensory coding. Strongly direction-selective neurons are weighted most highly by optimal decoders trained to discriminate motion direction. Models with predefined decoding weights demonstrate that this weighting scheme causally improved direction representation by a neuronal population. Optimizing decoders (using a generalized linear model or Fisher’s linear discriminant) led to only marginally better performance than decoders based purely on a neuron’s preferred direction and selectivity.

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Comparison of the Spatial Limits on Direction Selectivity in Visual Areas MT and V1

Journal of Neurophysiology ◽

10.1152/jn.00767.2004 ◽

2005 ◽

Vol 93 (3) ◽

pp. 1235-1245 ◽

Cited By ~ 25

Author(s):

Mark M. Churchland ◽

Nicholas J. Priebe ◽

Stephen G. Lisberger

Keyword(s):

Apparent Motion ◽

Great Majority ◽

Spatial Separation ◽

Direction Selectivity ◽

Temporal Separation ◽

Temporal Area ◽

Mean Values ◽

V1 Neurons ◽

Preferred Direction ◽

The Difference

We recorded responses to apparent motion from directionally selective neurons in primary visual cortex (V1) of anesthetized monkeys and middle temporal area (MT) of awake monkeys. Apparent motion consisted of multiple stationary stimulus flashes presented in sequence, characterized by their temporal separation (Δ t) and spatial separation (Δ x). Stimuli were 8° square patterns of 100% correlated random dots that moved at apparent speeds of 16 or 32°/s. For both V1 and MT, the difference between the response to the preferred and null directions declined with increasing flash separation. For each neuron, we estimated the maximum flash separation for which directionally selective responses were observed. For the range of speeds we used, Δ x provided a better description of the limitation on directional responses than did Δ t. When comparing MT and V1 neurons of similar preferred speed, there was no difference in the maximum Δ x between our samples from the two areas. In both V1 and MT, the great majority of neurons had maximal values of Δ x in the 0.25–1° range. Mean values were almost identical between the two areas. For most neurons, larger flash separations led to both weaker responses to the preferred direction and increased responses to the opposite direction. The former mechanism was slightly more dominant in MT and the latter slightly more dominant in V1. We conclude that V1 and MT neurons lose direction selectivity for similar values of Δ x, supporting the hypothesis that basic direction selectivity in MT is inherited from V1, at least over the range of stimulus speeds represented by both areas.

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