Octopaminergic modulation of temporal frequency coding in an identified optic flow-processing interneuron.

Kit D Longden,Holger G Krapp

doi:10.3389/fnsys.2010.00153

Abstract

Flying generates predictably different patterns of optic flow compared with other locomotor states. A sensorimotor system tuned to rapid responses and a high bandwidth of optic flow would help the animal to avoid wasting energy through imprecise motor action. However, neural processing that covers a higher input bandwidth itself comes at higher energetic costs which would be a poor investment when the animal was not flying. How does the blowfly adjust the dynamic range of its optic flow-processing neurons to the locomotor state? Octopamine (OA) is a biogenic amine central to the initiation and maintenance of flight in insects. We used an OA agonist chlordimeform (CDM) to simulate the widespread OA release during flight and recorded the effects on the temporal frequency coding of the H2 cell. This cell is a visual interneuron known to be involved in flight stabilization reflexes. The application of CDM resulted in (i) an increase in the cell's spontaneous activity, expanding the inhibitory signaling range (ii) an initial response gain to moving gratings (20–60 ms post-stimulus) that depended on the temporal frequency of the grating and (iii) a reduction in the rate and magnitude of motion adaptation that was also temporal frequency-dependent. To our knowledge, this is the first demonstration that the application of a neuromodulator can induce velocity-dependent alterations in the gain of a wide-field optic flow-processing neuron. The observed changes in the cell's response properties resulted in a 33% increase of the cell's information rate when encoding random changes in temporal frequency of the stimulus. The increased signaling range and more rapid, longer lasting responses employed more spikes to encode each bit, and so consumed a greater amount of energy. It appears that for the fly investing more energy in sensory processing during flight is more efficient than wasting energy on under-performing motor control.

Highlights

There are many examples of reflexes in which the animal’s locomotor state alters the activity of the peripheral sensory interneurons supporting the response (Clarac et al, 2000; Hultborn, 2001)
To this end we presented gratings moving at different, constant velocities for 0.5 s and calculated the velocity tuning curves from the responses over the stimulus duration
Functional implications and conclusion The presumed function of the H2 cell is to provide information about horizontal motion in the contralateral visual field to the horizontal system (HS) cells, that disambiguates between rotation and translation-induced optic flow (Hausen, 1982a,b; Hausen and Wehrhahn, 1990; Haag and Borst, 2001; Krapp et al, 2001; Kern et al, 2005)

Summary

Introduction

There are many examples of reflexes in which the animal’s locomotor state alters the activity of the peripheral sensory interneurons supporting the response (Clarac et al, 2000; Hultborn, 2001). Recent work indicates that the locomotor state can alter the gain of neural responses of central visual neurons involved in diverse behavioral tasks (mouse: Niell and Stryker, 2010; rat: Agrochão et al, 2010; fruit fly: Chiappe et al, 2010; Maimon et al, 2010). These boosted responses must provide the animals with substantial energetic benefits because the increased neural signaling will add a significant energetic cost during states when muscle tissue metabolism can be extremely high (Laughlin, 2001; Niven and Laughlin, 2008). Chiappe et al (2010) have recently shown that locomotion can alter the velocity tuning of optic flowprocessing interneurons in the blowfly

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Conclusion