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Maintenance of neuronal size gradient in MNTB requires sound-evoked activity

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ABSTRACT

Neurons of the medial nucleus of the trapezoid body (MNTB) act as fast-spiking inhibitory interneurons within the auditory brain stem. The MNTB is topographically organized, with low sound frequencies encoded laterally and high frequencies medially. We discovered a cell size gradient along this axis: lateral neurons are larger than medial neurons. The absence of this gradient in deaf mice lacking plasma membrane calcium ATPase 2 suggests an activity-dependent, calcium-mediated mechanism that controls neuronal soma size.

No MeSH data available.


Lateral MNTB neurons have a larger membrane capacitance and larger calyceal inputs in wild type but not in dfw2J mutants. A: cell membrane capacitance was acquired for visually identified neurons in voltage-clamp mode. Dye labeling of each neuron via the patch pipette allowed off-line measurements of the neurons' position within the MNTB. B: capacitance measurements corroborate histology data showing that lateral cells are significantly larger than medial cells in wild type (P ≤ 0.001) but there is no significant difference between cells in +/dfw2J and dfw2J/dfw2J mutants (n.s.). Error bars show SE. C: calyceal EPSCs are larger in lateral than in medial MNTB wild-type neurons. No significant difference was found between EPSC amplitudes of medial and lateral neurons in dfw2J/dfw2J mutants. D: in in vivo recordings of single MNTB neurons in wild types, characteristic frequency is used as a measure for medial-to-lateral position. No significant correlation was found between medial-to-lateral position and firing rate. E: the coefficient of variation for the first spike latency (FSL) showed a positive correlation with characteristic frequency. Unfortunately, because of the deafness phenotype these data could not be acquired in the dfw2J/dfw2J mutants. ***P ≤ 0.001, n.s., not significant.
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Figure 4: Lateral MNTB neurons have a larger membrane capacitance and larger calyceal inputs in wild type but not in dfw2J mutants. A: cell membrane capacitance was acquired for visually identified neurons in voltage-clamp mode. Dye labeling of each neuron via the patch pipette allowed off-line measurements of the neurons' position within the MNTB. B: capacitance measurements corroborate histology data showing that lateral cells are significantly larger than medial cells in wild type (P ≤ 0.001) but there is no significant difference between cells in +/dfw2J and dfw2J/dfw2J mutants (n.s.). Error bars show SE. C: calyceal EPSCs are larger in lateral than in medial MNTB wild-type neurons. No significant difference was found between EPSC amplitudes of medial and lateral neurons in dfw2J/dfw2J mutants. D: in in vivo recordings of single MNTB neurons in wild types, characteristic frequency is used as a measure for medial-to-lateral position. No significant correlation was found between medial-to-lateral position and firing rate. E: the coefficient of variation for the first spike latency (FSL) showed a positive correlation with characteristic frequency. Unfortunately, because of the deafness phenotype these data could not be acquired in the dfw2J/dfw2J mutants. ***P ≤ 0.001, n.s., not significant.

Mentions: PMCA2 regulates transmitter release in the MNTB. A and B: immunohistochemical labeling for MAP2 and PMCA2 in the MNTB (A) and in an individual MNTB neuron (B). A cross section through the calyx is marked “calyx.” Arrows show where PMCA2 appears to be localized presynaptically in the outer membrane of the calyx. C: voltage-clamp recordings from postsynaptic MNTB neurons in acute brain slices show a higher frequency of miniature excitatory postsynaptic currents (mEPSCs) in the MNTB of dfw2J/dfw2J mice compared with wild type (WT). D: calyceal EPSCs evoked by midline stimulation are larger in dfw2J/dfw2J mice compared with WT. Stimulus artifacts have been deleted for clarity. WT data include 7 medial cells, 3 lateral cells, and 8 cells with no information about location in the MNTB. dfw2J/dfw2J data include 7 medial cells, 6 lateral cells, and 4 cells with no information about location in the MNTB (see also Fig. 4C). E and F: in vivo single-unit recordings of MNTB neurons measured higher spontaneous firing rates (E) and shorter synaptic delays (F) in dfw2J/dfw2J mice compared with WT. ***P ≤ 0.001, **P ≤ 0.01, *P ≤ 0.05, n.s., Not significant.


Maintenance of neuronal size gradient in MNTB requires sound-evoked activity
Lateral MNTB neurons have a larger membrane capacitance and larger calyceal inputs in wild type but not in dfw2J mutants. A: cell membrane capacitance was acquired for visually identified neurons in voltage-clamp mode. Dye labeling of each neuron via the patch pipette allowed off-line measurements of the neurons' position within the MNTB. B: capacitance measurements corroborate histology data showing that lateral cells are significantly larger than medial cells in wild type (P ≤ 0.001) but there is no significant difference between cells in +/dfw2J and dfw2J/dfw2J mutants (n.s.). Error bars show SE. C: calyceal EPSCs are larger in lateral than in medial MNTB wild-type neurons. No significant difference was found between EPSC amplitudes of medial and lateral neurons in dfw2J/dfw2J mutants. D: in in vivo recordings of single MNTB neurons in wild types, characteristic frequency is used as a measure for medial-to-lateral position. No significant correlation was found between medial-to-lateral position and firing rate. E: the coefficient of variation for the first spike latency (FSL) showed a positive correlation with characteristic frequency. Unfortunately, because of the deafness phenotype these data could not be acquired in the dfw2J/dfw2J mutants. ***P ≤ 0.001, n.s., not significant.
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Figure 4: Lateral MNTB neurons have a larger membrane capacitance and larger calyceal inputs in wild type but not in dfw2J mutants. A: cell membrane capacitance was acquired for visually identified neurons in voltage-clamp mode. Dye labeling of each neuron via the patch pipette allowed off-line measurements of the neurons' position within the MNTB. B: capacitance measurements corroborate histology data showing that lateral cells are significantly larger than medial cells in wild type (P ≤ 0.001) but there is no significant difference between cells in +/dfw2J and dfw2J/dfw2J mutants (n.s.). Error bars show SE. C: calyceal EPSCs are larger in lateral than in medial MNTB wild-type neurons. No significant difference was found between EPSC amplitudes of medial and lateral neurons in dfw2J/dfw2J mutants. D: in in vivo recordings of single MNTB neurons in wild types, characteristic frequency is used as a measure for medial-to-lateral position. No significant correlation was found between medial-to-lateral position and firing rate. E: the coefficient of variation for the first spike latency (FSL) showed a positive correlation with characteristic frequency. Unfortunately, because of the deafness phenotype these data could not be acquired in the dfw2J/dfw2J mutants. ***P ≤ 0.001, n.s., not significant.
Mentions: PMCA2 regulates transmitter release in the MNTB. A and B: immunohistochemical labeling for MAP2 and PMCA2 in the MNTB (A) and in an individual MNTB neuron (B). A cross section through the calyx is marked “calyx.” Arrows show where PMCA2 appears to be localized presynaptically in the outer membrane of the calyx. C: voltage-clamp recordings from postsynaptic MNTB neurons in acute brain slices show a higher frequency of miniature excitatory postsynaptic currents (mEPSCs) in the MNTB of dfw2J/dfw2J mice compared with wild type (WT). D: calyceal EPSCs evoked by midline stimulation are larger in dfw2J/dfw2J mice compared with WT. Stimulus artifacts have been deleted for clarity. WT data include 7 medial cells, 3 lateral cells, and 8 cells with no information about location in the MNTB. dfw2J/dfw2J data include 7 medial cells, 6 lateral cells, and 4 cells with no information about location in the MNTB (see also Fig. 4C). E and F: in vivo single-unit recordings of MNTB neurons measured higher spontaneous firing rates (E) and shorter synaptic delays (F) in dfw2J/dfw2J mice compared with WT. ***P ≤ 0.001, **P ≤ 0.01, *P ≤ 0.05, n.s., Not significant.

View Article: PubMed Central - PubMed

ABSTRACT

Neurons of the medial nucleus of the trapezoid body (MNTB) act as fast-spiking inhibitory interneurons within the auditory brain stem. The MNTB is topographically organized, with low sound frequencies encoded laterally and high frequencies medially. We discovered a cell size gradient along this axis: lateral neurons are larger than medial neurons. The absence of this gradient in deaf mice lacking plasma membrane calcium ATPase 2 suggests an activity-dependent, calcium-mediated mechanism that controls neuronal soma size.

No MeSH data available.