Central complex neurons exhibit behaviorally gated responses to visual motion in Drosophila

2014 ◽  
Vol 111 (1) ◽  
pp. 62-71 ◽  
Author(s):  
Peter T. Weir ◽  
Bettina Schnell ◽  
Michael H. Dickinson

Sensory systems provide abundant information about the environment surrounding an animal, but only a small fraction of that information is relevant for any given task. One example of this requirement for context-dependent filtering of a sensory stream is the role that optic flow plays in guiding locomotion. Flying animals, which do not have access to a direct measure of ground speed, rely on optic flow to regulate their forward velocity. This observation suggests that progressive optic flow, the pattern of front-to-back motion on the retina created by forward motion, should be especially salient to an animal while it is in flight, but less important while it is standing still. We recorded the activity of cells in the central complex of Drosophila melanogaster during quiescence and tethered flight using both calcium imaging and whole cell patch-clamp techniques. We observed a genetically identified set of neurons in the fan-shaped body that are unresponsive to visual motion while the animal is quiescent. During flight their baseline activity increases, and they respond to front-to-back motion with changes relative to this baseline. The results provide an example of how nervous systems selectively respond to complex sensory stimuli depending on the current behavioral state of the animal.

2021 ◽  
Vol 57 (11) ◽  
pp. 1810-1821
Author(s):  
Yiming Qian ◽  
Andrea R. Seisler ◽  
Rick O. Gilmore

1997 ◽  
Vol 77 (2) ◽  
pp. 554-561 ◽  
Author(s):  
Jong-Nam Kim ◽  
Kathleen Mulligan ◽  
Helen Sherk

Kim, Jong-Nam, Kathleen Mulligan, and Helen Sherk. Simulated optic flow and extrastriate cortex. I. Optic flow versus texture. J. Neurophysiol. 77: 554–561, 1997. A locomoting observer sees a very different visual scene than an observer at rest: images throughout the visual field accelerate and expand, and they follow approximately radial outward paths from a single origin. This so-called optic flow field is presumably used for visual guidance, and it has been suggested that particular areas of visual cortex are specialized for the analysis of optic flow. In the cat, the lateral suprasylvian visual area (LS) is a likely candidate. To test the hypothesis that LS is specialized for analysis of optic flow fields, we recorded cell responses to optic flow displays. Stimulus movies simulated the experience of a cat trotting slowly across an endless plain covered with small balls. In different simulations we varied the size of balls, their organization (randomly or regularly dispersed), and their color (all one gray level, or multiple shades of gray). For each optic flow movie, a “texture” movie composed of the same elements but lacking optic flow cues was tested. In anesthetized cats, >500 neurons in LS were studied with a variety of movies. Most (70%) of 454 visually responsive cells responded to optic flow movies. Visually responsive cells generally preferred optic flow to texture movies (69% of those responsive to any movie). The direction in which a movie was shown (forward or reverse) was also an important factor. Most cells (68%) strongly preferred forward motion, which corresponded to visual experience during locomotion.


2020 ◽  
Author(s):  
Nardin Nakhla ◽  
Yavar Korkian ◽  
Matthew R. Krause ◽  
Christopher C. Pack

AbstractThe processing of visual motion is carried out by dedicated pathways in the primate brain. These pathways originate with populations of direction-selective neurons in the primary visual cortex, which project to dorsal structures like the middle temporal (MT) and medial superior temporal (MST) areas. Anatomical and imaging studies have suggested that area V3A might also be specialized for motion processing, but there have been very few studies of single-neuron direction selectivity in this area. We have therefore performed electrophysiological recordings from V3A neurons in two macaque monkeys (one male and one female) and measured responses to a large battery of motion stimuli that includes translation motion, as well as more complex optic flow patterns. For comparison, we simultaneously recorded the responses of MT neurons to the same stimuli. Surprisingly, we find that overall levels of direction selectivity are similar in V3A and MT and moreover that the population of V3A neurons exhibits somewhat greater selectivity for optic flow patterns. These results suggest that V3A should be considered as part of the motion processing machinery of the visual cortex, in both human and non-human primates.Significance statementAlthough area V3A is frequently the target of anatomy and imaging studies, little is known about its functional role in processing visual stimuli. Its contribution to motion processing has been particularly unclear, with different studies yielding different conclusions. We report a detailed study of direction selectivity in V3A. Our results show that single V3A neurons are, on average, as capable of representing motion direction as are neurons in well-known structures like MT. Moreover, we identify a possible specialization for V3A neurons in representing complex optic flow, which has previously been thought to emerge in higher-order brain regions. Thus it appears that V3A is well-suited to a functional role in motion processing.


i-Perception ◽  
2021 ◽  
Vol 12 (6) ◽  
pp. 204166952110557
Author(s):  
Diederick C. Niehorster

The concept of optic flow, a global pattern of visual motion that is both caused by and signals self-motion, is canonically ascribed to James Gibson's 1950 book “ The Perception of the Visual World.” There have, however, been several other developments of this concept, chiefly by Gwilym Grindley and Edward Calvert. Based on rarely referenced scientific literature and archival research, this article describes the development of the concept of optic flow by the aforementioned authors and several others. The article furthermore presents the available evidence for interactions between these authors, focusing on whether parts of Gibson's proposal were derived from the work of Grindley or Calvert. While Grindley's work may have made Gibson aware of the geometrical facts of optic flow, Gibson's work is not derivative of Grindley's. It is furthermore shown that Gibson only learned of Calvert's work in 1956, almost a decade after Gibson first published his proposal. In conclusion, the development of the concept of optic flow presents an intriguing example of convergent thought in the progress of science.


2017 ◽  
Vol 117 (2) ◽  
pp. 738-755 ◽  
Author(s):  
Nareg Berberian ◽  
Amanda MacPherson ◽  
Eloïse Giraud ◽  
Lydia Richardson ◽  
J.-P. Thivierge

In various regions of the brain, neurons discriminate sensory stimuli by decreasing the similarity between ambiguous input patterns. Here, we examine whether this process of pattern separation may drive the rapid discrimination of visual motion stimuli in the lateral intraparietal area (LIP). Starting with a simple mean-rate population model that captures neuronal activity in LIP, we show that overlapping input patterns can be reformatted dynamically to give rise to separated patterns of neuronal activity. The population model predicts that a key ingredient of pattern separation is the presence of heterogeneity in the response of individual units. Furthermore, the model proposes that pattern separation relies on heterogeneity in the temporal dynamics of neural activity and not merely in the mean firing rates of individual neurons over time. We confirm these predictions in recordings of macaque LIP neurons and show that the accuracy of pattern separation is a strong predictor of behavioral performance. Overall, results propose that LIP relies on neuronal pattern separation to facilitate decision-relevant discrimination of sensory stimuli. NEW & NOTEWORTHY A new hypothesis is proposed on the role of the lateral intraparietal (LIP) region of cortex during rapid decision making. This hypothesis suggests that LIP alters the representation of ambiguous inputs to reduce their overlap, thus improving sensory discrimination. A combination of computational modeling, theoretical analysis, and electrophysiological data shows that the pattern separation hypothesis links neural activity to behavior and offers novel predictions on the role of LIP during sensory discrimination.


2014 ◽  
Vol 18 (3) ◽  
pp. 436-451 ◽  
Author(s):  
Seth B. Agyei ◽  
Magnus Holth ◽  
F.R. Ruud van der Weel ◽  
Audrey L.H. van der Meer

1993 ◽  
Vol 5 (3) ◽  
pp. 374-391 ◽  
Author(s):  
Markus Lappe ◽  
Josef P. Rauschecker

Interest in the processing of optic flow has increased recently in both the neurophysiological and the psychophysical communities. We have designed a neural network model of the visual motion pathway in higher mammals that detects the direction of heading from optic flow. The model is a neural implementation of the subspace algorithm introduced by Heeger and Jepson (1990). We have tested the network in simulations that are closely related to psychophysical and neurophysiological experiments and show that our results are consistent with recent data from both fields. The network reproduces some key properties of human ego-motion perception. At the same time, it produces neurons that are selective for different components of ego-motion flow fields, such as expansions and rotations. These properties are reminiscent of a subclass of neurons in cortical area MSTd, the triple-component neurons. We propose that the output of such neurons could be used to generate a computational map of heading directions in or beyond MST.


2009 ◽  
Vol 102 (6) ◽  
pp. 3606-3618 ◽  
Author(s):  
Kit D. Longden ◽  
Holger G. Krapp

Active locomotive states are metabolically expensive and require efficient sensory processing both to avoid wasteful movements and to cope with an extended bandwidth of sensory stimuli. This is particularly true for flying animals because flight, as opposed to walking or resting, imposes a steplike increase in metabolism for the precise execution and control of movements. Sensory processing itself carries a significant metabolic cost, but the principles governing the adjustment of sensory processing to different locomotor states are not well understood. We use the blowfly as a model system to study the impact on visual processing of a neuromodulator, octopamine, which is known to be involved in the regulation of flight physiology. We applied an octopamine agonist and recorded the directional motion responses of identified visual interneurons known to process self-motion–induced optic flow to directional motion stimuli. The neural response range of these neurons is increased and the response latency is reduced. We also found that, due to an elevated spontaneous spike rate, the cells' negative signaling range is increased. Meanwhile, the preferred self-motion parameters the cells encode were state independent. Our results indicate that in the blowfly energetically expensive sensory coding strategies, such as rapid, large responses, and high spontaneous spike activity could be adjusted by the neuromodulator octopamine, likely to save energy during quiet locomotor states.


Perception ◽  
1997 ◽  
Vol 26 (7) ◽  
pp. 823-830 ◽  
Author(s):  
Lothar Spillmann ◽  
Stuart Anstis ◽  
Anne Kurtenbach ◽  
Ian Howard

A random-dot field undergoing counterphase flicker paradoxically appears to move in the same direction as head and eye movements, ie opposite to the optic-flow field. The effect is robust and occurs over a wide range of flicker rates and pixel sizes. The phenomenon can be explained by reversed phi motion caused by apparent pixel movement between successive retinal images. The reversed motion provides a positive feedback control of the display, whereas under normal conditions retinal signals provide a negative feedback. This altered polarity invokes self-sustaining eye movements akin to involuntary optokinetic nystagmus.


Perception ◽  
1994 ◽  
Vol 23 (6) ◽  
pp. 681-690 ◽  
Author(s):  
Jos Monen ◽  
Eli Brenner

Experiments were designed to establish whether we can use the optic flow to detect changes in our own velocity. Subjects were presented with simulations of forward motion across a flat surface. They were asked to respond as quickly as possible to a step increase in simulated ego-velocity. The smallest change for which subjects could respond within 500 ms was determined. At realistic simulated speeds of locomotion, the simulated ego-velocity had to increase by about 50%. The threshold for detecting changes in simulated ego-velocity was hardly better than the threshold for detecting other changes in the acceleration of the dots on the screen. It made little difference whether the surface across which the subject appeared to move was built up of dots, lines, or triangles; neither did it matter whether subjects saw the same image with both eyes, or whether the simulation was presented in stereoscopic depth. The results show that we are very poor at detecting changes in our own velocity on the basis of visual input alone.


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