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Calcium-dependent control of temporal processing in an auditory interneuron: a computational analysis

Abstract

Sensitivity to acoustic amplitude modulation in crickets differs between species and depends on carrier frequency (e.g., calling song vs. bat-ultrasound bands). Using computational tools, we explore how Ca2+-dependent mechanisms underlying selective attention can contribute to such differences in amplitude modulation sensitivity. For omega neuron 1 (ON1), selective attention is mediated by Ca2+-dependent feedback: [Ca2+]internal increases with excitation, activating a Ca2+-dependent after-hyperpolarizing current. We propose that Ca2+ removal rate and the size of the after-hyperpolarizing current can determine ON1’s temporal modulation transfer function (TMTF). This is tested using a conductance-based simulation calibrated to responses in vivo. The model shows that parameter values that simulate responses to single pulses are sufficient in simulating responses to modulated stimuli: no special modulation-sensitive mechanisms are necessary, as high and low-pass portions of the TMTF are due to Ca2+-dependent spike frequency adaptation and post-synaptic potential depression, respectively. Furthermore, variance in the two biophysical parameters is sufficient to produce TMTFs of varying bandwidth, shifting amplitude modulation sensitivity like that in different species and in response to different carrier frequencies. Thus, the hypothesis that the size of after-hyperpolarizing current and the rate of Ca2+ removal can affect amplitude modulation sensitivity is computationally validated.

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Abbreviations

Ahp:

After-hyperpolarizing

ERB:

Equivalent rectangular bandwidth

I/O:

Input/output

ON1:

Omega neuron 1

PSP:

Postsynaptic potential

SFP:

Spike frequency peak

SNR:

Signal-to-noise ratio

τfast :

Fast adaptation time constant

TMTF:

Temporal modulation transfer function

τremoval :

Time constant for Ca2+ removal

τslow :

Slow adaptation time constant

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Acknowledgments

Two anonymous reviewers as well as C. Canavier, S. Selvakumar, S. Achuthan and W. Gordon provided useful comments on the project and/or manuscript. N. Bazan generously provided equipment and software. No animals were used for this computational project. The study was funded in part by the NIH Grant # P20RR016816 to N. Bazan.

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Correspondence to Hamilton E. Farris.

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Ponnath, A., Farris, H.E. Calcium-dependent control of temporal processing in an auditory interneuron: a computational analysis. J Comp Physiol A 196, 613–628 (2010). https://doi.org/10.1007/s00359-010-0547-z

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Keywords

  • Adaptation
  • Temporal processing
  • Roex filter
  • Evolution
  • Temperature