Abstract

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.

Highlights

  • How animals perceive their environment depends on their behavioral state

  • We analyzed the responses of the wide-field motion-sensitive neuron V1, one of the fly’s lobula plate tangential cells (LPTCs), to naturalistic optic flow

  • How the processing of the optic flow perceived under a natural condition is affected by state-dependent modulation is still unresolved, because in all previous experiments periodic gratings drifting with experimenter-designed velocity profiles were used to address state-dependent modulation

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Summary

Introduction

How animals perceive their environment depends on their behavioral state. The neuromodulator octopamine, which is the invertebrate analogue of norepinephrine in the vertebrate neural system (Hurley et al, 2004; Sara and Bouret, 2012), is a key candidate for the control of state-dependent sensory processing (Roeder, 2005). Octopamine is released in high quantities during flight (Goosey and Candy, 1980). In flies as well as in locusts, administration of octopamine or its agonist chlordimeform (CDM) was shown to affect visual processing (Bacon et al, 1995; Longden and Krapp, 2009, 2010; Jung et al, 2011; Haan et al, 2012; Rien et al, 2012)

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