Preparing for the unexpected: predictive feedback boosts the response to unpredictable communication signals in weakly electric fish.
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1
University of Ottawa, Cellular and Molecular Medicine & Centre for Neural Dynamics, Canada
To interact with the environment efficiently, the nervous system must generate expectations about redundant sensory signals and detect unexpected ones. Neural circuits can, for example, compare a prediction of the sensory signal that was generated by the nervous system with the incoming sensory input, in order to generate a response selective to novel stimuli. This task is particularly important for communication signals where background must be suppressed for the signal to be reliably detected.
We used the communication signals of the weakly electric fish to investigate the neural mechanism used to perform this task. We focus on communication signals –called small chirps– typical of male-male agonistic encounters. In addition to chirps, interacting fish are constantly exposed to redundant a sinusoidal amplitude modulation (beat) resulting from the interaction of the two fishes’ electric fields. Chirps must therefore be distinguished from the background beat by the nervous system. In the first order electrosensory neurons of electric fish, a negative image of low-frequency redundant communication signals is subtracted from the neural response via feedback, allowing unpredictable signals to be extracted (Marsat et al., 2012). The mechanism by which this canceling feedback is generated and operates is well understood and has been the focus of many studies.
Here we show that the canceling feedback not only suppresses the predictable signal, but also actively enhances the response to the unpredictable communication signal. A mismatch between the canceling feedback and incoming sensory input causes both to become positive: at a phase where the soma is normally not depolarized by feedforward sensory inputs caused by the redundant beat, the unpredictable input transiently depolarizes it while the neuron’s apical dendrites are still depolarized by the lagging predictive feedback. The apical dendrites allow the backpropagation of somatic spikes, a mechanism that underlie the bursting propensity of the cell. Using in vivo intracellular dendritic recordings, we show that backpropagation is enhanced when the dendrites are depolarized by feedback. Therefore the soma is initially depolarized by the feedforward input from the chirp, a depolarization that is then increased by the enhanced backpropagating spike leading to the production of spike bursts. We conclude that the feedback driven by a predictable low-frequency signal not only suppresses the response to a redundant stimulus, but also induces a bursting response triggered by unpredictable communication signals.
References
Marsat G, Longtin A and Maler L. (2012) Cellular and circuit properties supporting different sensory coding strategies in electric fish and other systems. Curr Op Neurobiol, DOI:10.1016/j.conb.2012.01.009.
Keywords:
backpropagation,
bursting,
Communication signals,
Feedback,
sensory processing
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster Presentation (see alternatives below as well)
Topic:
Sensory: Electrosensory
Citation:
Marsat
G and
Maler
L
(2012). Preparing for the unexpected: predictive feedback boosts the response to unpredictable communication signals in weakly electric fish..
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00163
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Received:
27 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Gary Marsat, University of Ottawa, Cellular and Molecular Medicine & Centre for Neural Dynamics, Ottawa, Canada, gary.marsat@mail.wvu.edu