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ARTICLE, Development/Plasticity/Repair

Primordial Rhythmic Bursting in Embryonic Cochlear Ganglion Cells

Timothy A. Jones, Sherri M. Jones and Kristina C. Paggett
Journal of Neuroscience 15 October 2001, 21 (20) 8129-8135; https://doi.org/10.1523/JNEUROSCI.21-20-08129.2001
Timothy A. Jones
1Department of Surgery, Division of Otolaryngology, University of Missouri School of Medicine, Columbia, Missouri 65212
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Sherri M. Jones
1Department of Surgery, Division of Otolaryngology, University of Missouri School of Medicine, Columbia, Missouri 65212
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Kristina C. Paggett
1Department of Surgery, Division of Otolaryngology, University of Missouri School of Medicine, Columbia, Missouri 65212
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  • Fig. 1.
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    Fig. 1.

    The primary digitized records (40 μsec per point) of two neural spike trains are shown here. The records illustrate the range of signal-to-noise ratios encountered in this study. The process of expanding traces for high resolution computerized analysis is shown for neuron 88tm01. Spike detection was accomplished using an initial voltage threshold criterion. Records were divided into contiguous data blocks in which for each block, the voltage threshold could be adjusted to accommodate fluctuations in baseline. The entire record was examined on screen at high resolution for falsely detected spikes and for failed detection of spikes. Each action potential was individually confirmed.

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    Fig. 2.

    Discharge rates (spikes per second) for individual ganglion cells are plotted as a function of developmental stage. Data for stages 44 and 45 are from earlier work (Jones and Jones, 2000). Spike discharge rates increase steadily during development (regression slope = 4.13 Sp/sec per stage; p < 0.001;r2 = 0.2). Discharge rates for stages 39–43 ranged from 0.09 to 40 Sp/sec, and the overall mean discharge rate was 9 ± 10 Sp/sec (n = 44).

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    Fig. 3.

    Bursting spontaneous discharge patterns. Five examples of discharge patterns are represented at progressively later stages of development from stage 39 to 43 (top tobottom, respectively). Eighteen of the 44 spontaneously active ganglion cells produced rhythmic bursting patterns. Eachvertical line represents a single action potential. Total time represented is 60 sec. Over these developmental stages, the rate of bursting ranged from 1 to 54 bursts per minute. Burst rates for each neuron were based on the FFT spectrum of the ACF (Fig. 4). Rates in bursts per minute for neurons shown were 9.78 for 91tm01, 5.88 for 89tm01, 5.88 for 87tm01, 13.68 for 80tm01, and 15.6 for 84tm02. Five cells that demonstrated regular bursting patterns (all at stages 42–43) also responded to sound.

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    Fig. 4.

    Autocorrelation functions (ACF; also referred to as probability density functions) and their fast Fourier transforms (FFT) are shown for three representative neurons. The ACF of spike discharge activity was examined for evidence of periodicities. Neuron 80tm01 (top) shows a robust periodicity, and the FFT spectrum demonstrates a fundamental frequency (f0) of 0.228 Hz. A portion of the spike train for neuron is shown in Figure 3. Similarly, the spike activity of neuron 91tm01 of Figure 3 was subjected to ACF and FFT analysis, revealing a clear periodicity at 0.163 Hz, despite the low spike rate in this case. Neuron 76tm01 exhibited no rhythmic bursting, and as can be seen in the ACF, there were no periodicities present. FFT amplitudes are represented in arbitrary units.

  • Fig. 5.
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    Fig. 5.

    Rhythmic discharge rates (bursts per minute) are plotted as a function of developmental stage (top). Rate of rhythmic bursting increased on average with increasing developmental stage. The range of burst rates was 1–54 bursts per minute. The regression slope for data shown was 5.68 bursts per minute per stage (p < 0.01;r2 = 0.3). At stages 40–43, both rhythmic and irregular bursting patterns were present. Rates indicated here are for rhythmic bursting only. Bursting patterns are irregular when present at stages beyond 43. The relative number of neurons exhibiting rhythmic bursting decreased with increasing stage (bottom). Circles represent both rhythmic and nonrhythmic bursting patterns, whereas trianglesrepresent proportions of rhythmically bursting neurons only. The fraction of rhythmically bursting cells decreases at later stages. * indicates that in the case of stage 39, most cells were silent. The two cells that were active had very low spike rates, and only one had a sufficient number of spikes to evaluate for bursting patterns. This cell exhibited rhythmic bursting. The other cell generated only eight spikes in 90 sec, thus precluding a determination of bursting status.

  • Fig. 6.
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    Fig. 6.

    Labeled neuron for animal 87tm01. Spontaneous discharge pattern for this animal is shown in Figure 2.Top, The neural edge; bottom, the abneural edge; right, the base; and left, the apex. Scale bar, 50 μm.

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    Table 1.

    Staging and incubation day equivalence, according toHamburger and Hamilton (1951)

    Observed stageEquivalent incubation day (37.5°C)
    38 to 39E12
    38+ to 40−E13
    40− to 40E14
    40− to 41E15
    41+ to 42E16
    42 to 43E17
    42 to 44E18
    • +, Late; −, early.

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The Journal of Neuroscience: 21 (20)
Journal of Neuroscience
Vol. 21, Issue 20
15 Oct 2001
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Primordial Rhythmic Bursting in Embryonic Cochlear Ganglion Cells
Timothy A. Jones, Sherri M. Jones, Kristina C. Paggett
Journal of Neuroscience 15 October 2001, 21 (20) 8129-8135; DOI: 10.1523/JNEUROSCI.21-20-08129.2001

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Primordial Rhythmic Bursting in Embryonic Cochlear Ganglion Cells
Timothy A. Jones, Sherri M. Jones, Kristina C. Paggett
Journal of Neuroscience 15 October 2001, 21 (20) 8129-8135; DOI: 10.1523/JNEUROSCI.21-20-08129.2001
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Keywords

  • functional ontogeny
  • bird
  • spontaneous activity
  • embryonic development
  • primary afferents
  • chicken
  • audition
  • hearing

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