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The Journal of Neuroscience, April 25, 2007, 27(17):4621-4633; doi:10.1523/JNEUROSCI.4615-06.2007

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Behavioral/Systems/Cognitive
Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Stephen M. Rogers,1 Holger G. Krapp,1,2 Malcolm Burrows,1 and Thomas Matheson1,3

1Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom, 2Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom, and 3Department of Biology, University of Leicester, Leicester LE1 7RH, United Kingdom

Correspondence should be addressed to Stephen M. Rogers, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. Email: smr34{at}cam.ac.uk

We characterized homeostatic plasticity at an identified sensory-motor synapse in an insect, which maintains constant levels of motor drive as locusts transform from their solitarious phase to their gregarious swarming phase. The same mechanism produces behaviorally relevant changes in response timing that can be understood in the context of an animal's altered behavioral state. For individual animals of either phase, different looming objects elicited different spiking responses in a visual looming detector interneuron, descending contralateral movement detector (DCMD), yet its synaptic drive to a leg motoneuron, fast extensor tibiae (FETi), always had the same maximum amplitude. Gregarious locust DCMDs produced more action potentials and had higher firing frequencies, but individual postsynaptic potentials (PSPs) elicited in FETi were half the amplitude of those in solitarious locusts. A model suggested that this alone could not explain the similarity in overall amplitude, and we show that facilitation increased the maximum compound PSP amplitude in gregarious animals. There was the same linear relationship between times of peak DCMD firing before collision and the size/velocity of looming objects in both phases. The DCMD-FETi synapse transformed this relationship nonlinearly, such that peak amplitudes of compound PSPs occurred disproportionately earlier for smaller/faster objects. Furthermore, the peak PSP amplitude occurred earlier in gregarious than in solitarious locusts, indicating a differential tuning. Homeostatic modulation of the amplitude, together with a nonlinear synaptic transformation of timing, acted together to tune the DCMD-FETi system so that swarming gregarious locusts respond earlier to small moving objects, such as conspecifics, than solitarious locusts.

Key words: homeostatic plasticity; sensory-motor integration; DCMD; nonlinear transformation; locust; phenotypic plasticity


Received Oct. 24, 2006; revised March 20, 2007; accepted March 21, 2007.

Correspondence should be addressed to Stephen M. Rogers, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. Email: smr34{at}cam.ac.uk




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F. C. Rind, R. D. Santer, and G. A. Wright
Arousal Facilitates Collision Avoidance Mediated by a Looming Sensitive Visual Neuron in a Flying Locust
J Neurophysiol, August 1, 2008; 100(2): 670 - 680.
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H. Fotowat and F. Gabbiani
Relationship between the Phases of Sensory and Motor Activity during a Looming-Evoked Multistage Escape Behavior
J. Neurosci., September 12, 2007; 27(37): 10047 - 10059.
[Abstract] [Full Text] [PDF]



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