Auditory cortex spatial sensitivity sharpens during task performance

Journal name:
Nature Neuroscience
Volume:
14,
Pages:
108–114
Year published:
DOI:
doi:10.1038/nn.2713
Received
Accepted
Published online

Abstract

Activity in the primary auditory cortex (A1) is essential for normal sound localization behavior, but previous studies of the spatial sensitivity of neurons in A1 have found broad spatial tuning. We tested the hypothesis that spatial tuning sharpens when an animal engages in an auditory task. Cats performed a task that required evaluation of the locations of sounds and one that required active listening, but in which sound location was irrelevant. Some 26–44% of the units recorded in A1 showed substantially sharpened spatial tuning during the behavioral tasks as compared with idle conditions, with the greatest sharpening occurring during the location-relevant task. Spatial sharpening occurred on a scale of tens of seconds and could be replicated multiple times in ~1.5-h test sessions. Sharpening resulted primarily from increased suppression of responses to sounds at least-preferred locations. That and an observed increase in latencies suggest an important role of inhibitory mechanisms.

At a glance

Figures

  1. Task-dependant modulation of spatial sensitivity.
    Figure 1: Task-dependant modulation of spatial sensitivity.

    (a) Poststimulus time histogram (PSTH) showing activity as a function of time (horizontal axis) and head-centered stimulus location (vertical axis) for one example unit in A1 in the right hemisphere during the idle condition (ERRF width = 217°). Colors indicate mean spike activity. The thin white lines at the bottom of the plots indicate the 80-ms stimulus duration. White gaps crossing the plot corresponded to the spatial bins centered at ipsilateral and contralateral 90°, which were omitted from analysis. (b) PSTH of the same unit during the periodicity detection task (ERRF width = 173°). (c) PSTH of the same unit during the localization task (ERRF width = 143°). (d) Average spike rates during the onset response (10–40 ms) as functions of azimuth. Black, blue and red lines plot rate-azimuth functions in the idle condition, the periodicity detection task and the localization task, respectively. The data for three conditions were obtained in a single behavioral session, which lasted about 100 min. For the computation of the ERRF width, see Supplementary Figure 1.

  2. Modulation of spatial sensitivity in sequential conditions.
    Figure 2: Modulation of spatial sensitivity in sequential conditions.

    (a) PSTH of an example unit from the left hemisphere recorded during the first block of localization trials from the beginning of the recording (0 min) to the first 13 min. (b) The same unit recorded during a subsequent idle period (13–18 min). (c) Rate-azimuth functions of the onset responses for the first localization task (red) and the subsequent idle condition (black). (d) A second block of localization trials (25–34 min). (e) A second idle period (34–39 min). (f) Rate-azimuth functions of the onset responses for the second localization task (red) and the subsequent idle condition (black). Data are presented as in Figure 1.

  3. PSTH plots in three task conditions from two units recorded from the left hemisphere that showed offset-dominant responses to 150-ms stimuli.
    Figure 3: PSTH plots in three task conditions from two units recorded from the left hemisphere that showed offset-dominant responses to 150-ms stimuli.

    (ac) One unit recorded across three conditions (a, idle; b, periodicity detection; c, localization) in a 105-min session. (df) One unit recorded across three conditions (d, idle; e, periodicity detection; f, localization) in a 120-min session. For each unit, the ratio of offset to onset responses increased from idle to periodicity detection to localization conditions. Data are presented as in Figure 1.

  4. Comparisons of ERRF width across conditions for all units that showed excitatory responses in the first 40 ms after stimulus onset.
    Figure 4: Comparisons of ERRF width across conditions for all units that showed excitatory responses in the first 40 ms after stimulus onset.

    (ac) Each symbol represents one unit, with the value in horizontal and vertical axes corresponding to its ERRF width in two different conditions. The symbols lying below the diagonal line represent units for which spatial tuning sharpened (and the ERRF width narrowed) for the condition indicated on the ordinate. o, units that did not show significant sharpening or broadening of ERRF widths; +, units that showed significant sharpening; x, units that showed significant broadening according to the ROC test. (d) Cumulative distributions of ERRF widths across three conditions. The horizontal dashed line crosses the curves at the median values. The percentages of the distributions to the left of the vertical dashed line had ERRF widths narrower than a hemifield (that is, ≤160°).

  5. Percentage of units that showed significant sharpening or broadening of spatial tuning between condition pairs.
    Figure 5: Percentage of units that showed significant sharpening or broadening of spatial tuning between condition pairs.

    Portions of the bars above or below the 0% line represent the percentage of units for which the ERRF width sharpened or broadened significantly for each two-way comparison. The upper portions of the middle and right bars are divided to represent units that sharpened their tuning significantly in the periodicity detection versus idle contrast (dark) or those that did not (light).

  6. First spike latency for preferred locations was longer during behavioral conditions.
    Figure 6: First spike latency for preferred locations was longer during behavioral conditions.

    Distributions of the trial-by-trial medians of first spike latencies for preferred locations are plotted for three conditions. Analysis of variance showed a significant effect of condition for the median first spike latency (P < 0.05). Differences were significant in two-way comparison between the idle condition and the periodicity detection task (t test, P < 0.01) and between the idle condition and the localization task (t test, P < 0.01), but not between the periodicity detection and localization tasks (t test, P = 0.89). Each box shows the upper and lower quartile and median as horizontal lines. + indicate points beyond the quartiles.

  7. Spike rates decreased in the localization task primarily for stimuli at least-preferred locations.
    Figure 7: Spike rates decreased in the localization task primarily for stimuli at least-preferred locations.

    (a) Distributions of spike rates averaged across all stimulus locations for units that showed significant sharpening in the ROC analysis (Fig. 5). Mean spike rates decreased significantly across task conditions (Kruskal-Wallis test, P < 0.01). (b) Mean spike rates for stimuli at preferred locations showed no significant difference between the localization task and the idle condition (Wilcoxon rank sum test, P = 0.88). (c) Mean spike rates for least-preferred locations were suppressed significantly for the localization task compared with the idle condition (P < 0.05).

  8. Time course of the task-dependent modulation of the response at single location that showed strongest suppression when the localization task was compared with the idle condition.
    Figure 8: Time course of the task-dependent modulation of the response at single location that showed strongest suppression when the localization task was compared with the idle condition.

    (a) Normalized spike rates during four consecutive hit trials (1–4) followed by the four consecutive non-hit trials (5–8). The mean normalized spike rate for each of the four non-hit trials was significantly higher than the mean of all the hit presentations (Wilcoxon rank sum test, P < 0.0001 to P < 0.01, depending on trial). (b) Four non-hit trials (1–4) followed by four hit trials (5–8). The normalized spike rate for each of the first three non-hit trials was significantly higher than the mean of all the hit presentations that followed (P < 0.001 to P < 0.005). Error bars indicate the s.e.m.

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Affiliations

  1. Kresge Hearing Research Institute, Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, Michigan, USA.

    • Chen-Chung Lee
  2. Department of Otolaryngology-Head and Neck Surgery and Center for Hearing Research, University of California, Irvine, California, USA.

    • Chen-Chung Lee &
    • John C Middlebrooks

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The authors declare no competing financial interests.

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