Modulation of speed-sensitivity of a motion-sensitive neuron during walking
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1
HHMI, Janelia Farm Research Campus, United States
Motion-sensitive neurons of the fly visual system respond selectively to specific features of the optic flow fields elicited when the animal moves through its natural environment. Flies use optic flow to guide their locomotion, and the activity of neurons in the motion pathway ultimately instructs motor commands used for course control [1]. However, motion in the extrinsic world can also cause global retinal image flow (consider, for example, a fly standing on a leaf on a windy day). This creates a potential confound between ego-motion and motion originating externally that must be resolved by incorporating feedback from other sensory and motor pathways. To examine this idea, we explored whether neurons involved in a visual-motor circuit modulate their dynamic range depending on the animal’s own movement. We expressed the genetically encoded calcium indicator GCaMP3 in a subset of neurons of the lobula plate of the fruit fly, and used two-photon imaging to record from the so-called Horizontal System Equatorial (HSE) neuron. This neuron, which receives directionally selective retinotopic input from as yet unidentified motion detecting neurons, responds preferentially to motion along the horizontal axis. During the recording, tethered flies were allowed to walk on an air-suspended ball and stimulated with global optic flow fields delivered using an LED arena. We monitored the ball’s rotation at high resolution and used this readout as a proxy for the tethered fly’s own walking activity. We compared calcium responses of the HSE neuron to global optic flow when the fly was standing to those recorded when the fly was walking. We found that HSE neurons show significantly greater responses during walking. Moreover, peak calcium responses increased in direct correlation with the tethered fly’s walking speed. Interestingly, this correlation was more evident when neurons were stimulated at higher temporal frequencies (stimuli moving at higher speeds). When the fly was standing, the temporal frequency tuning curve of the HSE neuron peaked at 1 Hz; during walking periods, the neuron responses increased in amplitude and peaked at higher temporal frequencies. Finally, the modulation of the neuron’s response due to walking activity showed temporal frequency sensitivity: response gains were higher for higher temporal frequencies. By recording the activity of neurons in behaving animals, we can evaluate the performance of a circuit under more naturalistic circumstances, i.e. including sensory and mechanical feedback. Here, we show that motion-sensitive neurons quickly adjust their bandwidth depending on the behavioral state of the animal. Increasing a system’s sensitivity during behavior is beneficial from an energy minimization standpoint. The temporal-frequency- and walking-speed-dependent gain modulation we observe may additionally be used to accommodate the increased optic flow caused by a freely moving animal’s own movements. We are now investigating possible mechanisms for this adaptive behavior of the circuitry, including the possibility that it is mediated by octopamine [2].
References
1. Eggelhaaf et al (2002) TINS, 25: 96-102.
2. Longden and Krapp (2009). J.Neurophysiol (doi: 10.1152/jn.00395.2009).
Conference:
Computational and Systems Neuroscience 2010, Salt Lake City, UT, United States, 25 Feb - 2 Mar, 2010.
Presentation Type:
Poster Presentation
Topic:
Poster session II
Citation:
Chiappe
EM,
Seelig
JD,
Reiser
MB and
Jayaraman
V
(2010). Modulation of speed-sensitivity of a motion-sensitive neuron during walking.
Front. Neurosci.
Conference Abstract:
Computational and Systems Neuroscience 2010.
doi: 10.3389/conf.fnins.2010.03.00331
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Received:
08 Mar 2010;
Published Online:
08 Mar 2010.
*
Correspondence:
Eugenia M Chiappe, HHMI, Janelia Farm Research Campus, Ashburn, United States, chiappee@janelia.hhmi.org