Adaptation changes directional sensitivity in a visual motion-sensitive neuron of the fly

Kalb, Julia; Egelhaaf, Martin; Kurtz, Rafael

doi:10.1016/j.visres.2008.05.004

Cited by 9 publications

(16 citation statements)

References 33 publications

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“…Within the expected coherences the lowest values were found after epinastine administration (Figures 7A,B, right). The low expected coherence after epinastine application indicates an increase in noise, which is likely to result from the overall decrease in spike rate (Kalb et al, 2008). However, comparing the mean coherence values with the expected coherences forming the respective upper bounds reveals significant drug effects, which cannot be attributed to an increase in noise alone.…”

Section: Resultsmentioning

confidence: 99%

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow

Rien

Kern

Kurtz

2013

Front. Behav. Neurosci.

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In a variety of species locomotor activity, like walking or flying, has been demonstrated to alter visual information processing. The neuromodulator octopamine was shown to change the response characteristics of optic flow processing neurons in the fly's visual system in a similar way as locomotor activity. This modulation resulted in enhanced neuronal responses, in particular during sustained stimulation with high temporal frequencies, and in shorter latencies of responses to abrupt onsets of pattern motion. These state-dependent changes were interpreted to adjust neuronal tuning to the range of high velocities encountered during locomotion. Here we assess the significance of these changes for the processing of optic flow as experienced during flight. Naturalistic image sequences were reconstructed based on measurements of the head position and gaze direction of Calliphora vicina flying in an arena. We recorded the responses of the V1 neuron during presentation of these image sequences on a panoramic stimulus device (“FliMax”). Consistent with previous accounts, we found that spontaneous as well as stimulus-induced spike rates were increased by an octopamine agonist and decreased by an antagonist. Moreover, a small but consistent decrease in response latency upon octopaminergic activation was present, which might support fast responses to optic flow cues and limit instabilities during closed-loop optomotor regulation. However, apart from these effects the similarities between the dynamic response properties in the different pharmacologically induced states were surprisingly high, indicating that the processing of naturalistic optic flow is not fundamentally altered by octopaminergic modulation.

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Section: Resultsmentioning

confidence: 99%

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow

Rien

Kern

Kurtz

2013

Front. Behav. Neurosci.

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“…This window has been used in several previous publications (e.g., Harris et al, 2000; Kalb et al, 2008; Nordström et al, 2011), but some of the earliest effects of motion adaptation may not be visible this far into the response. For example, we showed that CDM has a clear effect on the initial response delay, only 30 ms after stimulus onset (Figure 5).…”

Section: Discussionmentioning

confidence: 99%

“…During rest, the only type of motion that may carry physiologically relevant information is found in transient motion impulses. Signaling levels to prolonged visual motion are indeed reduced in immobilized animals (see e.g., Maddess and Laughlin, 1985; Clifford and Langley, 1996; Harris et al, 2000; Kurtz et al, 2000; Kalb et al, 2008), whereas transient pulses remain reliably encoded (Maddess and Laughlin, 1985; Kurtz et al, 2009a). …”

Section: Discussionmentioning

confidence: 99%

“…To be able to code these broad inputs, and to enable signaling of even small deviations, each neuron adapts to the currently prevailing stimulus conditions (Maddess and Laughlin, 1985; Ulanovsky et al, 2003; Kurtz et al, 2009a). The process of such neural adaptation is well studied in a number of systems, ranging from primate cortical MT neurons (Kohn and Movshon, 2003), through the cat visual (Hu et al, 2011) and auditory cortex (Ulanovsky et al, 2003), and the visual inter-neurons of the fly lobula plate (Maddess and Laughlin, 1985; Harris et al, 2000; Fairhall et al, 2001; Neri and Laughlin, 2005; Kalb et al, 2008; Kurtz et al, 2009a). These studies show that adaptation changes the neural coding range to code the distribution of stimuli that is being encountered, not only by shifting the sensitivity range to the current mean stimulus and reducing the output to a continuous stimulus (Maddess and Laughlin, 1985; Kurtz et al, 2009a), but also by adjusting the coding sensitivity to the spread of the stimulus (Fairhall et al, 2001; Ulanovsky et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Octopaminergic modulation of contrast sensitivity

Haan¹,

Lee²,

Nordström³

2012

Front. Integr. Neurosci.

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Sensory systems adapt to prolonged stimulation by decreasing their response to continuous stimuli. Whereas visual motion adaptation has traditionally been studied in immobilized animals, recent work indicates that the animal's behavioral state influences the response properties of higher-order motion vision-sensitive neurons. During insect flight octopamine is released, and pharmacological octopaminergic activation can induce a fictive locomotor state. In the insect optic ganglia, lobula plate tangential cells (LPTCs) spatially pool input from local elementary motion detectors (EMDs) that correlate luminosity changes from two spatially discrete inputs after delaying the signal from one. The LPTC velocity optimum thereby depends on the spatial separation of the inputs and on the EMD's delay properties. Recently it was shown that behavioral activity increases the LPTC velocity optimum, with modeling suggesting this to originate in the EMD's temporal delay filters. However, behavior induces an additional post-EMD effect: the LPTC membrane conductance increases in flying flies. To physiologically investigate the degree to which activity causes presynaptic and postsynaptic effects, we conducted intracellular recordings of Eristalis horizontal system (HS) neurons. We constructed contrast response functions before and after adaptation at different temporal frequencies, with and without the octopamine receptor agonist chlordimeform (CDM). We extracted three motion adaptation components, where two are likely to be generated presynaptically of the LPTCs, and one within them. We found that CDM affected the early, EMD-associated contrast gain reduction, temporal frequency dependently. However, a CDM-induced change of the HS membrane conductance disappeared during and after visual stimulation. This suggests that physical activity mainly affects motion adaptation presynaptically of LPTCs, whereas post-EMD effects have a minimal effect.

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“…In particular, to optimize the encoding of the fluctuations of environmental image features during the intersaccadic intervals, adaptation in the visual system should essentially take place on a timescale shorter than the duration of these intervals (i.e., within some tens of milliseconds) and may be driven by the high-frequency changes of the respective image parameters. Several physiological components of motion adaptation have been described at the different levels of the fly visual system (e.g., Maddess and Laughlin, 1985; Brenner et al, 2000a; Harris et al, 2000; Fairhall et al, 2001; Kurtz, 2007; Kalb et al, 2008; Liang et al, 2008). To what extent the time constants of these processes, which have been identified with experimenter designed motion stimuli, match the dynamics of parameter changes in the natural visual input, and how these adaptive processes are controlled, is still not clear.…”

Section: Processing Of Optic Flow In the Insect Nervous Systemmentioning

confidence: 99%

Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action

Egelhaaf¹,

Boeddeker²,

Kern³

et al. 2012

Front. Neural Circuits

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126

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Insects such as flies or bees, with their miniature brains, are able to control highly aerobatic flight maneuvres and to solve spatial vision tasks, such as avoiding collisions with obstacles, landing on objects, or even localizing a previously learnt inconspicuous goal on the basis of environmental cues. With regard to solving such spatial tasks, these insects still outperform man-made autonomous flying systems. To accomplish their extraordinary performance, flies and bees have been shown by their characteristic behavioral actions to actively shape the dynamics of the image flow on their eyes (“optic flow”). The neural processing of information about the spatial layout of the environment is greatly facilitated by segregating the rotational from the translational optic flow component through a saccadic flight and gaze strategy. This active vision strategy thus enables the nervous system to solve apparently complex spatial vision tasks in a particularly efficient and parsimonious way. The key idea of this review is that biological agents, such as flies or bees, acquire at least part of their strength as autonomous systems through active interactions with their environment and not by simply processing passively gained information about the world. These agent-environment interactions lead to adaptive behavior in surroundings of a wide range of complexity. Animals with even tiny brains, such as insects, are capable of performing extraordinarily well in their behavioral contexts by making optimal use of the closed action–perception loop. Model simulations and robotic implementations show that the smart biological mechanisms of motion computation and visually-guided flight control might be helpful to find technical solutions, for example, when designing micro air vehicles carrying a miniaturized, low-weight on-board processor.

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Adaptation changes directional sensitivity in a visual motion-sensitive neuron of the fly

Cited by 9 publications

References 33 publications

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow

Octopaminergic modulation of contrast sensitivity

Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action

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