Flies see second-order motion

Theobald, Jamie C.; Duistermars, Brian J.; Ringach, Dario L.; Frye, Mark A.

doi:10.1016/j.cub.2008.03.050

Cited by 96 publications

(74 citation statements)

References 8 publications

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“…While it could be argued that the response to higher harmonics that we observed is an artefact of the rectification displayed by some electroreceptors and might not carry any behavioral relevance, a growing amount of evidence suggests that this is not the case. Indeed, some species take into account the higher harmonics contained in a call when choosing their mate (Bodnar, 1996;Hennig, 2009) while insects can reliably track contrast-based motion patterns (Theobald et al, 2008). Further studies are needed to elucidate these important questions in the electrosensory system.…”

Section: Nonlinear Coding In the Peripheral Electrosensory Systemmentioning

confidence: 99%

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Savard¹,

Krahe²,

Chacron³

2011

Neuroscience

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Peripheral sensory neurons respond to stimuli containing a wide range of spatio-temporal frequencies. We investigated electroreceptor neuron coding in the gymnotiform wave-type weakly electric fish Apteronotus leptorhynchus. Previous studies used low to mid temporal frequencies (<256 Hz) and showed that electroreceptor neuron responses to sensory stimuli could be almost exclusively accounted for by linear models, thereby implying a rate code. We instead used temporal frequencies up to 425 Hz, which is in the upper behaviorally relevant range for this species. We show that electroreceptors can: (A) respond up to the highest frequencies tested and (B) display strong nonlinearities in their responses to such stimuli. These nonlinearities were manifested by the fact that the responses to repeated presentations of the same stimulus were coherent at temporal frequencies outside of those contained in the stimulus waveform. Specifically, these consisted of low frequencies corresponding to the time varying contrast or envelope of the stimulus as well as higher harmonics of the frequencies contained in the stimulus. Heterogeneities in the afferent population influenced nonlinear coding as afferents with the lowest baseline firing rates tended to display the strongest nonlinear responses. To understand the link between afferent heterogeneity and nonlinear responsiveness, we used a phenomenological mathematical model of electrosensory afferents. Varying a single parameter in the model was sufficient to account for the variability seen in our experimental data and yielded a prediction: nonlinear responses to the envelope and at higher harmonics are both due to afferents with lower baseline firing rates displaying greater degrees of rectification in their responses. This prediction was verified experimentally as we found that the coherence between the half-wave rectified stimulus and the response resembled the coherence between the responses to repeated presentations of the stimulus in our dataset. This result shows that rectification cannot only give rise to responses to low frequency envelopes but also at frequencies that are higher than those contained in the stimulus. The latter result implies that information is contained in the fine temporal structure of electroreceptor afferent spike trains. Our results show that heterogeneities in peripheral neuronal populations can have dramatic consequences on the nature of the neural code.

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Section: Nonlinear Coding In the Peripheral Electrosensory Systemmentioning

confidence: 99%

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Savard¹,

Krahe²,

Chacron³

2011

Neuroscience

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“…Even if a driftbalanced bar is not encoded by a standard EMD (Fig. 1B, iii) (3,5,16), HSN mostly depolarizes to preferred-direction FM and hyperpolarizes in the anti-preferred direction (Fig. 1B, ii).…”

Section: Resultsmentioning

confidence: 99%

“…When viewing theta motion stimuli, the EM cues tended to dominate the response, as expected by a system depending on EMD-type input. However, in behavior fruit flies robustly track not only Fourier bars, but also drift-balanced and theta bars (16)(17)(18).Because flies compute motion in a similar way to vertebrates (1), respond to higher-order motion cues (5, 16-18), and are amenable to quantitative electrophysiological investigations, they become an attractive model system for investigating the mechanisms underlying higher-order motion detection. Here we quantify sensitivity to higher-order motion stimuli and discuss how this sensitivity critically depends on both the stimulus time course and the neuron's underlying receptive field.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

“…Because flies compute motion in a similar way to vertebrates (1), respond to higher-order motion cues (5,(16)(17)(18), and are amenable to quantitative electrophysiological investigations, they become an attractive model system for investigating the mechanisms underlying higher-order motion detection. Here we quantify sensitivity to higher-order motion stimuli and discuss how this sensitivity critically depends on both the stimulus time course and the neuron's underlying receptive field.…”

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confidence: 99%

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Higher-order motion sensitivity in fly visual circuits

Lee

Nordström

2012

Proc. Natl. Acad. Sci. U.S.A.

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In higher-order motion stimuli, the direction of object motion does not follow the direction of luminance change. Such stimuli could be generated by the wing movements of a flying butterfly and further complicated by its motion in and out of shadows. Human subjects readily perceive the direction of higher-order motion, although this stands in stark contrast to prevailing motion vision models. Flies and humans compute motion in similar ways, and because flies behaviorally track bars containing higher-order motion cues, they become an attractive model system for investigating the neurophysiology underlying higher-order motion sensitivity. We here use intracellular electrophysiology of motionvision-sensitive neurons in the hoverfly lobula plate to quantify responses to stimuli containing higher-order motion. We show that motion sensitivity can be broken down into two separate streams, directionally coding for elementary motion and figure motion, respectively, and that responses to Fourier and theta motion can be predicted from these. The sensitivity is affected both by the stimulus' time course and by the neuron's underlying receptive field. Responses to preferred-direction theta motion are sexually dimorphic and particularly robust along the visual midline.T here is broad evidence that essentially all animals with imageforming eyes compute visual motion by correlating the luminance from two neighboring photo-inputs, after delaying the signal from one of these inputs (1). The detection of such firstorder motion, or Fourier motion, therefore depends on the coherent correlation of luminance across space and time and forms the theoretical basis for the elementary motion detector (EMD) (2). However, motion signals in nature may not form exact spacetime correlations, but may also be composed of higher-order signals related to changes in contrast or texture.The term "higher-order motion" refers to movement of visual objects that have no net motion energy (3) or that contain paradoxical motion cues (4). A "drift-balanced" stimulus can be described as a moving object that contains an internal pattern that varies from and replaces the background as the object itself moves, but which itself is nonmoving. Drift-balanced bars generate no response from standard EMDs, but sensitivity can be generated by adding front-end nonlinearities to the inputs (5). "Theta motion stimuli" (4) consist of a moving object that contains an internal pattern that moves coherently in the direction opposite to the object itself. In this case, an EMD would encode the motion of the internal pattern (i.e., the elementary motion, or EM) instead of the motion of the object itself (i.e., the figure motion, or FM). Sensitivity to theta motion can be generated by, for example, layering two EMD networks (6) or by recurrent motion processing (7).Vertebrates, including human observers, readily perceive higher-order motion, including drift-balanced and theta motion, even though these contain no net EM cues in the direction of FM (for recent review, see ref. 8)....

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