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A rapid form of activity-dependent recovery from short-term synaptic depression in the intensity pathway of the auditory brainstem

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Abstract

Short-term synaptic plasticity acts as a time- and firing rate-dependent filter that mediates the transmission of information across synapses. In the avian auditory brainstem, specific forms of plasticity are expressed at different terminals of the same auditory nerve fibers and contribute to the divergence of acoustic timing and intensity information. To identify key differences in the plasticity properties, we made patch-clamp recordings from neurons in the cochlear nucleus responsible for intensity coding, nucleus angularis, and measured the time course of the recovery of excitatory postsynaptic currents following short-term synaptic depression. These synaptic responses showed a very rapid recovery, following a bi-exponential time course with a fast time constant of ~40 ms and a dependence on the presynaptic activity levels, resulting in a crossing over of the recovery trajectories following high-rate versus low-rate stimulation trains. We also show that the recorded recovery in the intensity pathway differs from similar recordings in the timing pathway, specifically the cochlear nucleus magnocellularis, in two ways: (1) a fast recovery that was not due to recovery from postsynaptic receptor desensitization and (2) a recovery trajectory that was characterized by a non-monotonic bump that may be due in part to facilitation mechanisms more prevalent in the intensity pathway. We tested whether a previously proposed model of synaptic transmission based on vesicle depletion and sequential steps of vesicle replenishment could account for the recovery responses, and found it was insufficient, suggesting an activity-dependent feedback mechanism is present. We propose that the rapid recovery following depression allows improved coding of natural auditory signals that often consist of sound bursts separated by short gaps.

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Authors and Affiliations

  1. Department of Biology, University of Maryland, College Park, MD, 20742, USA

    Katrina M. MacLeod

  2. Department of Electrical and Computer Engineering, The Institute for Systems Research, University of Maryland, College Park, MD, 20742, USA

    Timothy K. Horiuchi

  3. Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD, 20742, USA

    Katrina M. MacLeod & Timothy K. Horiuchi

Authors
  1. Katrina M. MacLeod
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  2. Timothy K. Horiuchi
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Correspondence to Katrina M. MacLeod.

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ESM 1 (TIF 12,592 kb)

Fig. S1 EGTA slows the recovery but fails to eliminate cross over a, Recovery following 50 Hz trains under control and two EGTA incubation concentrations. Steady state levels are plotted using corresponding markers on the far left. b, Recovery following 200 Hz trains under control and two EGTA concentrations. c, Comparison of recovery following 50 Hz and 200 Hz trains under 0.1 mM EGTA showing the cross over. d, e Recovery curves from a and b replotted as fractional recovery to normalize for differences in steady state depression. Note the similarity of the 0.02 mM EGTA curve with control, and the flatness of the 50 Hz 0.1mM EGTA curve, suggesting that EGTA affected the recovery rate. Data are mean ± s.e.m. Control, n = 5; 0.02 mM EGTA-AM, n = 3; 0.1mM EGTA-AM, n = 6.

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MacLeod, K.M., Horiuchi, T.K. A rapid form of activity-dependent recovery from short-term synaptic depression in the intensity pathway of the auditory brainstem. Biol Cybern 104, 209–223 (2011). https://doi.org/10.1007/s00422-011-0428-8

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  • DOI: https://doi.org/10.1007/s00422-011-0428-8

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