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Articles, Systems/Circuits

Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells

Friederice Pirschel and Jutta Kretzberg
Journal of Neuroscience 30 March 2016, 36 (13) 3636-3647; https://doi.org/10.1523/JNEUROSCI.1753-15.2016
Friederice Pirschel
1Computational Neuroscience, Department for Neuroscience, and
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Jutta Kretzberg
1Computational Neuroscience, Department for Neuroscience, and
2Cluster of Excellence “Hearing4all,” University of Oldenburg, D-26111 Oldenburg, Germany
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  • Figure 1.
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    Figure 1.

    Photograph of the body-wall preparation and sketch of the receptive fields of mechanoreceptors. Inset (right), A photomicrograph of the ganglion is shown with higher-magnification. Responses of up to three mechanosensory cells (T, P) were recorded intracellularly (positions of cell bodies and electrodes are marked in the inset), while the skin was stimulated mechanically by the poker (see Materials and Methods). The double-arrow line indicates the stimulation area at the middle annulus of the 10th segment. Ventral midline (the middle between the two black stripes on the skin) is defined as 0°. Stimulus locations to the right were denoted as a positive number of degrees and to the left as negative degrees. The left end of the preparation marks −180°, the right side +180°, black stripes are approximately at −90° and +90°. The sketch of the body wall preparation below the photograph shows the approximate locations and extents of the receptive fields of the full population of mechanoreceptors responding to mechanical stimulation at the ventral midline: two T cells (dashed gray) and two P cells (orange).

  • Figure 2.
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    Figure 2.

    Sketch of the stimulus estimation process, consisting of training and test phases. In this example, three stimuli of different intensities (A) were applied four times: for each of the stimuli, three response traces were included in the corresponding stimulus response class S1, S2, or S3 of the training dataset (B, top row, vertical lines indicate spike times), the remaining trace was used as test data (C, top row). B, Training: the analyzed response feature, here spike count, was determined for each trace in the training dataset. These numbers were sorted, and divided into three commensurate quantile classes (Q1, Q2, Q3) according to their ranks. We determined how often each possible spike count was contained in each quantile class Qi. For each spike count value, the index i of the most probable quantile class Qi determined to which rank class Ri all responses showing this spike count were assigned. The rank class look table gives the definitions of (R1, R2, R3) and line 5 shows the rank classes for each of the responses shown in line 1. The rank class matrix (B, bottom left) shows how many of the traces contained in each stimulus response class (S1, S2, S3) were assigned to each of the three rank classes (R1, R2, R3). The rank class matrix is used to create a stimulus estimation table (B, bottom right), giving for each rank class the stimulus, which has most probably elicited the response (maximum likelihood). C, Test: each trace in the test dataset is assigned to one of the rank classes based on the rank-class look table constructed in the training. Applying the stimulus estimation table, this rank class determines the estimated stimulus for each test response trace. The comparison of estimated and presented stimuli for all response traces leads to the percentage of correct estimations.

  • Figure 3.
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    Figure 3.

    Influences of touch location on neuronal responses of mechanoreceptors. A, Typical example of simultaneously intracellularly recorded responses of a right T cell (gray) and left P cell (orange) to a pressure stimulus of 50 mN for 200 ms at −20° (left) and +20° (right). B, Spike count and latency (mean and SD) of a typical T-cell double-recording with 10 repeated presentations of estimation task “location” (Table 1): a stimulus intensity of 50 mN applied for 200 ms at varied locations. Ventral midline is defined as 0°, stimulus locations to the right as positive and to the left as negative numbers of degrees. C, Spike count and latency (mean and SD of 10 responses) of a typical P-cell double-recording responding to the same stimulation as used in B. D, Dependencies of spike count and latency on stimulus location (mean and SD of the mean activity of 10 T cells and 10 P cells responding to 8–10 stimulus repetitions). Responses of left and right cells were pooled, displaying distances from receptive field centers rather than absolute stimulus locations on the body wall. The curves of both cell types are shifted relative to each other, because the receptive field centers of P cells are at −45° and 45°, and of T cells at −30° and 30° (Lewis and Kristan, 1998). Hence, stimulation of both cell types from −20° to +20° around the midline led to larger distances from receptive field centers of P cells than of T cells.

  • Figure 4.
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    Figure 4.

    Estimation results for stimulus location. A, Pairwise discrimination results for tactile stimulation at 0° compared with stimulus locations between 5° and 40°. Responses of T and P cells (5 TT and 5 PP cell double-recordings, 8–10 stimulus presentations for each cell) were analyzed for two stimulus intensities, 10 and 50 mN. The black dashed lines show chance level and 75% threshold. Asterisks indicate mean values that are significantly (p < 0.05, t test) above threshold. B, Classification result for nine locations of a 50 mN pressure stimulus. Black dashed line shows chance level, black dots mark the median values, and circles indicate statistical outliers (see Material and Methods). Response features: C, spike count; L, latency; I, first ISI; RD, response duration; CD, spike count difference; LD, latency difference; ID, first ISI difference; SC, summed spike count; BC, burst spike count; BD, burst duration.

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    Figure 5.

    Influences of stimulus intensity on neuronal responses of mechanoreceptors. A, Typical example of simultaneously, intracellularly recorded responses of a T cell (gray) and a P cell (orange) to a mechanical stimulus of 20 mN (left) and 100 mN (right) for 200 ms at 0° (ventral midline). B, C, Dependencies of B spike count and C latency on stimulus intensity. Mean and SD of 27 T cells (gray) and 22 P cells (orange) with 10 stimulus repetitions each, for intensities of 5–100 mN applied at 0° (Table 1, estimation task intensities high).

  • Figure 6.
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    Figure 6.

    Estimation results for stimulus intensity. A, Pairwise discrimination of responses to 10 mN steps of stimulus intensities between 20 and 100 mN. Black dashed lines show chance level and 75% threshold. Asterisks indicate mean values that are significantly (p < 0.05, t test) above threshold. Response features see B. B, Classification results for five stimulus intensities between 10 and 100 mN (Table 1, estimation task intensities high), which were applied at 0° for 200 ms. The black dashed line shows chance level, black dots mark the median values, and circles indicate statistical outliers (see Material and Methods). Response features: C, spike count; L, latency; I, first ISI; RD, response duration; CD, spike count difference; LD, latency difference; ID, first ISI difference; SC, summed spike count; BC, burst spike count; BD, burst duration.

  • Figure 7.
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    Figure 7.

    Influences of the stimulus duration on neuronal responses of mechanoreceptors. A, Spike count (mean and SD) for P cells (orange; N = 12) and T cells (gray; N = 10) for stimuli of 20 and 60 mN with 50, 200, and 500 ms duration, applied at 0° stimulus location (Table 1, estimation task duration). B, Classification results for 60 mN stimulus intensity with three durations (50, 200, and 500 ms). The black dashed line shows chance level, black dots mark the median values, and circles indicate statistical outliers (see Material and Methods). Response features: C, spike count; L, latency; I, first ISI; RD, response duration. P-cell features are shown in orange; T-cell features in gray. C, Classification results for two intensities (20 and 60 mN) in combination with three durations (50, 200, and 500 ms; Table 1, estimation task duration and intensity). For response features and legend see B.

  • Figure 8.
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    Figure 8.

    Estimation results for combination of location and intensity. A, Estimation results for combination of three locations (−20°, 0°, 20°) and two intensities (10 and 50 mN; Table 1, estimation task: location and intensity). C, Spike count; L, latency; I, first ISI; CD, spike count difference; LD, latency difference; ID, first ISI difference; SC, summed spike count; BC, burst spike count; BD, burst duration. Black dashed lines show chance level black dots mark median values, and circles indicate statistical outliers. B, Results for combination of summed spike count (SC) for intensity estimation (Int) and latency difference (LD) for location estimation (Loc) for the same location and intensity estimation task as in A. P-cell pairs in orange; T-cell pairs in light gray. Pooled data analysis: P cell SC and T cell LD in red, and T cell SC and P cell LD in dark gray; SC of P cell and T cell pooled data with LD of T cells in purple and with LD of P cells in blue. In the top row of the x-axis labels, the cells used for location estimation based on latency differences are listed; the second row shows cells used for intensity estimation based on summed counts. Asterisk indicates significant difference between estimation results (p < 0.05, Kruskal–Wallis test).

Tables

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    Table 1.

    Details of stimulation protocols and numbers of recorded cells for seven different estimation tasks analyzed in this study

    Estimation taskStimulus propertiesNumbers of cells
    Location, degreesIntensity, mNDuration, msT cellsTT pairsP cellsPP pairsTP pairs
    Location−20°, −15°, −10°, −5°, 0°, 5°, 10°, 15°, 20°10, 50200105105—
    Intensities low010, 20, 30, 40, 502001472412—
    Intensities high010, 20, 50, 70, 10020027823511
    Duration06050, 200, 50010—12——
    Duration and intensity020, 6050, 200, 50010—12——
    Location and intensity−20 , 0°, +2010, 50200105105—
    Location and intensity, 15 combinations−20°, −10°, 0°, +10°, +20°10, 20, 50200105105—
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    Table 2.

    Normalized mutual information of response features with stimulus properties (mean ± SD)

    CellsCountLatencySum countLatency diff
    Encoding task: 9 locations
        Fixed Int & Dur
            10 mN, 200 msT0.35 ± 0.120.49 ± 0.150.30 ± 0.110.73 ± 0.12
            10 mN, 200 msP0.35 ± 0.070.36 ± 0.070.25 ± 0.070.45 ± 0.12
            50 mN, 200 msT0.33 ± 0.040.51 ± 0.160.28 ± 0.080.61 ± 0.09
            50 mN, 200 msP0.36 ± 0.040.49 ± 0.100.33 ± 0.060.62 ± 0.09
    Encoding task: 5 intensities
        Fixed Loc & Dur
            0°, 200 msT0.44 ± 0.150.46 ± 0.160.48 ± 0.150.28 ± 0.17
            0°, 200 msP0.40 ± 0.090.39 ± 0.120.47 ± 0.110.25 ± 0.11
            0°, 200 msP-T0.52 ± 0.180.38 ± 0.11
    Encoding task: 3 locations and 2 intensities
        Fixed time
            200 msT0.38 ± 0.140.56 ± 0.070.36 ± 0.110.71 ± 0.08
            200 msP0.53 ± 0.140.49 ± 0.150.52 ± 0.130.52 ± 0.20
    • Bold numbers indicate the response feature with the highest mutual information obtained for the estimation task. Sum, Summed; Diff, difference; Int, Intensity; Loc, location; Dur, duration. Estimation tasks correspond to the stimulation protocols listed in Table 1.

    • View popup
    Table 3.

    Normalized mutual information of response features with stimulus properties (mean ± SD)

    CellsCountLatency1st ISIResp dur
    Encoding task: 3 durations
        Fixed Int & Loc
            60 mN, 0°T0.60 ± 0.240.11 ± 0.150.12 ± 0.120.59 ± 0.17
            60 mN, 0°P0.84 ± 0.110.10 ± 0.080.18 ± 0.090.72 ± 0.12
    Encoding task: 3 durations and 2 intensities
        Fixed Location
            0°T0.42 ± 0.130.34 ± 0.210.32 ± 0.130.49 ± 0.12
            0°P0.50 ± 0.070.30 ± 0.70.32 ± 0.090.53 ± 0.05
    • Bold numbers indicate the response feature with the highest mutual information obtained for the estimation task. Resp, response; Dur, duration; Int, intensity; Loc, Location; ISI, interspike interval. Estimation tasks correspond to the stimulation protocols listed in Table 1.

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The Journal of Neuroscience: 36 (13)
Journal of Neuroscience
Vol. 36, Issue 13
30 Mar 2016
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Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells
Friederice Pirschel, Jutta Kretzberg
Journal of Neuroscience 30 March 2016, 36 (13) 3636-3647; DOI: 10.1523/JNEUROSCI.1753-15.2016

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Multiplexed Population Coding of Stimulus Properties by Leech Mechanosensory Cells
Friederice Pirschel, Jutta Kretzberg
Journal of Neuroscience 30 March 2016, 36 (13) 3636-3647; DOI: 10.1523/JNEUROSCI.1753-15.2016
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Keywords

  • local bend network
  • mechanoreceptors
  • multiplexing
  • sensory coding
  • tactile
  • touch

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