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The Journal of Neuroscience, September 15, 2004, 24(37):8039-8048; doi:10.1523/JNEUROSCI.2021-04.2004

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Behavioral/Systems/Cognitive
Nonlinear Response Properties of Combination-Sensitive Electrosensory Neurons in the Midbrain of Gymnarchus niloticus

Bruce A. Carlson and Masashi Kawasaki

Department of Biology, University of Virginia, Charlottesville, Virginia 22904

The jamming avoidance response of the weakly electric fish Gymnarchus niloticus relies on determining the sign of the frequency difference (Df) between the fish's own electric organ discharge (EOD) and that of a neighbor, which is achieved by comparing modulations in amplitude (AM) and phase (PM) that result from the summation of their EODs. These two stimulus features are processed in separate pathways that converge in the torus semicircularis on combination-sensitive neurons, many of which are selective for the sign of Df. We recorded extracellular single-unit responses to independent stimulation with AM and PM and combined AM-PM stimulation to determine how sign selectivity is established. Responses to AM and PM frequently summated nonlinearly, leading to sign-selective responses as a result of facilitation to the preferred sign of Df and/or suppression to the nonpreferred sign of Df. Facilitation typically occurred when responses to AM and PM were aligned, whereas suppression typically occurred when they were offset. By experimentally manipulating the degree of alignment between these two responses, we found that the summed response was dependent on their relative timing. In addition, we found a unique class of units that were sensitive to differences in amplitude between two body surfaces. This sensitivity rendered such units immune to the problem of orientation ambiguity, in which the sign selectivity of a single neuron reverses with changes in stimulus orientation. We discuss potential synaptic mechanisms for driving nonlinear responses in these and other combination-sensitive neurons.

Key words: electric fish; mormyriform; facilitation; suppression; torus semicircularis; jamming avoidance response

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Received May 25, 2004; revised July 28, 2004; accepted July 30, 2004.

This article has been cited by other articles:

				J. T. Sanchez, D. Gans, and J. J. Wenstrup Glycinergic "Inhibition" Mediates Selective Excitatory Responses to Combinations of Sounds J. Neurosci., January 2, 2008; 28(1): 80 - 90. [Abstract] [Full Text] [PDF]

				B. A. Carlson and M. Kawasaki Stimulus Selectivity Is Enhanced by Voltage-Dependent Conductances in Combination-Sensitive Neurons J Neurophysiol, December 1, 2006; 96(6): 3362 - 3377. [Abstract] [Full Text] [PDF]

				B. A. Carlson and M. Kawasaki Ambiguous Encoding of Stimuli by Primary Sensory Afferents Causes a Lack of Independence in the Perception of Multiple Stimulus Attributes J. Neurosci., September 6, 2006; 26(36): 9173 - 9183. [Abstract] [Full Text] [PDF]

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