A labeled line code proves insufficient for Apteronotus leptoryhnchus during three dimensional electrolocation
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1
University of Ottawa, Department of Cellular and Molecular Medicine, Canada
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2
University of Ottawa, Department of Physics, Canada
Apteronotus leptorhynchus navigates its environment and detects prey using a weak electric sense. The basis of this sensory modality is a quasi-sinusoidal electric field referred to as the electric organ discharge (EOD), which, in the absence of stimulus, is approximately constant in amplitude. When objects with an electrical conductivity different than that of the surrounding water are present in the vicinity of the animal, the EOD amplitude is perturbed. The presence of a relative non-conductor, such as a rock, causes electric current to flow around the object, through the lower resistance water. This causes a local decrease in EOD amplitude. Stimuli that are more conductive than the surrounding water, such as prey, provide a lower resistance path for current to be shunted through and give rise to local increases in EOD amplitude.
These modulations in EOD amplitude are sensed by electroreceptors distributed over the fish’s body. The electroreceptor afferents project to a first order electrosensory processing region (ELL). In the ELL there are two types of efferent pyramidal neurons, dubbed E and I cells, which are believed to categorically encode the perturbations caused by relative conductors and relative non-conductors respectively. A functional analogy can be made between the E and I cells and their preferred stimulus types, to the ON and OFF retinal ganglion cells of the mammalian retina.
Previous studies have shown that when objects are moved along a trajectory parallel to the longitudinal body axis, E cells respond to metal objects with strong discharge while I cells respond vigorously to plastic objects. These findings are consistent with the notion of a labeled line code for conductive versus non-conductive objects.
Behavioral experiments demonstrate that these fish are also adept at estimating the position of objects moving at right angles to the skin, that is, perpendicular to the longitudinal body axis. Our results demonstrate that the hypothesis of a labeled line code does not hold under these conditions. As expected, we find that movement of a metal sphere towards the fish (looming) causes a strong increase in E cell firing rate. However, movement away from the skin (receding) causes E cell firing to decrease below baseline. Instead, we found that I cells respond to receding movements of the metal sphere. Similarly, I cells respond to looming plastic spheres, while E cells discharge in response to a receding plastic stimulus. This discovery raises a new problem: How is an invariant representation of the stimulus maintained if a cell’s response can encode either stimulus class? We present evidence that spike patterning can disambiguate the approach of an ON stimulus from the withdrawal of an OFF stimulus. Finally, we demonstrate that this surprising result can be understood in terms of the strong adaptation of electroreceptor discharge; a response feature specially developed for encoding high frequency communication signals.
We conclude that spatial navigation and hunting in three dimensions requires population encoding that combines both E and I cell channels, and a more complex decoding scheme than that envisaged by a labeled line code.
Keywords:
computational neuroscience,
Electric Fish,
Labeled line code,
motion processing,
population coding,
Stimulus Invariance
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for student poster award)
Topic:
Sensory: Electrosensory
Citation:
Clarke
S,
Longtin
A and
Maler
L
(2012). A labeled line code proves insufficient for Apteronotus leptoryhnchus during three dimensional electrolocation.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00126
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Received:
26 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Mr. Stephen Clarke, University of Ottawa, Department of Cellular and Molecular Medicine, Ottawa, Ontario, K1H 8M5, Canada, stephen.elisha.clarke@gmail.com