Impact of fasting and motion adaptation on how walking modulates visual motion processing in the blowfly
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1
Imperial College London, Department of Bioengineering, United Kingdom
Studies in awake, behaving animals suggest that sensory information processing is finely tuned to both the internal state as well as the external sensor inputs. In particular, locomotor states have been shown to alter visual motion processing in a diverse range of model systems that includes mice, rats, zebra fish, locust and flies. The resting activity, response gain, and temporal frequency tuning may all be affected.
Blowflies are an ideal system for studying this phenomenon, having distinct modes of locomotion, and well-characterised visual systems which have been used to identify many computational principles that apply across phyla. We have developed a head-fixed in vivo setup, in which we record spiking neurons extracellularly while the fly walks on a trackball and experiences motion stimuli. We recorded from spiking neurons in the third visual neuropil, the lobula plate, which are sensitive to wide-field optic flow, and thought to be involved in optomotor and gaze-stabilisation reflexes. The cells are tuned to the temporal frequency of a moving grating, rather than its velocity. So we characterise the cells’ responses to visual motion as a function of temporal frequency, i.e. the ratio of angular velocity and spatial wavelength of the grating.
Our first hypothesis was that locomotion causes a shift in the cells’ temporal frequency tuning according to the visual motion they would experience while walking. To test this, we adapted the cells to different temporal frequencies, and measured how walking modulated the cells’ responses to moving gratings. In agreement with previous studies, motion adaptation had a dramatic effect on the temporal frequency tuning of the cells, significantly reducing the responses to high temporal frequencies in stationary flies. In walking flies, we found that walking doubled the spontaneous activity, reduced the response latency by 15%, and restored sensitivity to high temporal frequencies which is normally reduced by motion adaptation. These effects did not depend on the temporal frequency of the adapting stimulus, and were maintained even for adapting stimuli with low temporal frequencies ≤1 Hz. Meanwhile, the response magnitude and latency reduction correlated with walking speed. The results indicate that the walking speed, rather than the temporal frequency of the stimulus, determines how locomotion modulates motion vision.
We next hypothesised that the locomotion-induced modulation of motion vision may allow the fly to save energy while not moving, by reducing neural activity when stationary. To investigate our hypothesis, we altered the fly’s energy budget by starving the fly for up to 3 days. We found that fasting reduced the changes in spontaneous activity and responses to high temporal frequency stimuli that accompany walking, without altering the activity of the cells when the fly was stationary.
Our results confirm that motion adaptation shapes the responses of optic flow-processing neurons to the external sensory input. In addition, the results show how the changes in visual motion processing that accompany walking depend on the internal state of the animal, including its walking speed and available energy reserves, and do not merely depend on the external sensory input.
Keywords:
Locomotion,
motion vision,
motion adaptation,
Fasting,
Blowfly,
Octopamine
Conference:
International Conference on Invertebrate Vision, Fjälkinge, Sweden, 1 Aug - 8 Aug, 2013.
Presentation Type:
Oral presentation preferred
Topic:
Motion vision
Citation:
Longden
KD and
Krapp
HG
(2019). Impact of fasting and motion adaptation on how walking modulates visual motion processing in the blowfly.
Front. Physiol.
Conference Abstract:
International Conference on Invertebrate Vision.
doi: 10.3389/conf.fphys.2013.25.00083
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Received:
26 Feb 2013;
Published Online:
09 Dec 2019.
*
Correspondence:
Dr. Kit D Longden, Imperial College London, Department of Bioengineering, London, SW7 2AZ, United Kingdom, kitlongden@gmail.com