Location coding by opponent neural populations in the auditory cortex

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Abstract

Although the auditory cortex plays a necessary role in sound localization, physiological investigations in the cortex reveal inhomogeneous sampling of auditory space that is difficult to reconcile with localization behavior under the assumption of local spatial coding. Most neurons respond maximally to sounds located far to the left or right side, with few neurons tuned to the frontal midline. Paradoxically, psychophysical studies show optimal spatial acuity across the frontal midline. In this paper, we revisit the problem of inhomogeneous spatial sampling in three fields of cat auditory cortex. In each field, we confirm that neural responses tend to be greatest for lateral positions, but show the greatest modulation for near-midline source locations. Moreover, identification of source locations based on cortical responses shows sharp discrimination of left from right but relatively inaccurate discrimination of locations within each half of space. Motivated by these findings, we explore an opponent-process theory in which sound-source locations are represented by differences in the activity of two broadly tuned channels formed by contra- and ipsilaterally preferring neurons. Finally, we demonstrate a simple model, based on spike-count differences across cortical populations, that provides bias-free, level-invariant localization - and thus also a solution to the "binding problem" of associating spatial information with other nonspatial attributes of sounds. © 2005 Stecker et al.

Figures

  • Figure 2. Classification Performance of Accurate PAF Units from [14] Neural spike patterns were classified according to the stimulus location most likely to have elicited them. In each panel, a confusion matrix plots the relative proportion of classifications of each target azimuth (x-axis) to each possible response azimuth (y-axis). Proportions are indicated by the area of a circle located at the intersection of target and response locations. Example units were selected from among those transmitting the most spatial information in their responses. In each case, discrimination of contralateral azimuths (negative values) from ipsilateral azimuths (positive values) is apparent, accompanied by significant within-hemifield confusion. As such, neural responses are sufficient for left/right discrimination only, and the spatial information transmitted by the most accurate units tends not to be much greater than one bit per stimulus. DOI: 10.1371/journal.pbio.0030078.g002
  • Figure 1. Example RAFs Plotted are normalized mean spike counts (y-axis) elicited by broadband stimuli (20 dB above unit threshold) varying in azimuth (x-axis). Lines represent units recorded in cortical area DZ. Left: contralaterally responsive units. Right: ipsilaterally responsive units. DOI: 10.1371/journal.pbio.0030078.g001
  • Figure 3. RAF Slopes Are Steepest near the Interaural Midline Plotted are summaries of preferred locations (centroids) and points of maximum RAF slope for 254 units recorded in A1 (left), 411 in PAF (middle), and 298 in DZ (right) for levels 20 and 40 dB above threshold (thr) (bottom and top rows, respectively). In each panel, units are sorted by centroid (blue crosses) on the y-axis. Thin red lines denote the region of azimuth (x-axis) containing the centroid and bounded by the points of steepest slope. For units with centroids lateralized more than 108 from the midline, we marked either the steepest positive slope (for ipsilaterally tuned units) or negative slope (for contralateral units) with a black circle. These points represent the location of most rapid response change that occurs toward the front of the animal (relative to the centroid; for units that respond throughout the frontal hemifield, this point can occur toward the rear). Distributions of centroid (blue line) and peak slope (black line), calculated using kernel density estimation with 208 rectangular bins, are plotted below each panel. These indicate that while preferred locations (centroids) are strongly biased toward contralateral azimuths, peak slopes are tightly packed about the interaural midline, consistent with the opponent-channel hypothesis. DOI: 10.1371/journal.pbio.0030078.g003
  • Figure 4. Discrimination Analysis Based on Responses of One PAF Unit Left: raster plot of spike times (x-axis) recorded in response to broadband noise stimuli varying in azimuth (y-axis). Note the strong modulation of spike count, response latency, and temporal features of the response between contralateral and ipsilateral locations. Right: pairwise spatial discrimination. Colors indicate d9 values for pairs of stimulus locations varying in separation (y-axis) and overall azimuth (x-axis, midpoint of two azimuths). The dashed line indicates threshold discrimination (d9 = 1), and the red circle marks the unit’s MDA (y-axis) and BA (x-axis). DOI: 10.1371/journal.pbio.0030078.g004
  • Figure 5. MDA by BA MDA (y-axis) is plotted against BA (x-axis) for each unit exhibiting suprathreshold spatial discrimination (see Materials and Methods). Symbols indicate the cortical area of each unit. Left and lower panels plot distributions of MDA and BA (in numbers of units per rectangular 208 bin), respectively. DOI: 10.1371/journal.pbio.0030078.g005
  • Figure 6. Difference between Channel Responses Is Less Sensitive to Changes in Level Than Are Channel Responses Themselves Left: population responses (y-axis; see Materials and Methods) are plotted as a function of azimuth (x-axis) for stimuli presented 20 dB (red) and 40 dB (blue) above unit thresholds. Population responses were computed separately for subpopulations composed of contralateral units (top) or ipsilateral units (middle) corresponding to hypothetical ‘‘left’’ and ‘‘right’’ channels of an opponent-channel spatial coding mechanism. The difference (bottom) between responses of the two subpopulations is more consistent across stimulus level than is either subpopulation response alone. Error bars indicate the standard deviation of responses across 120 simulated trials. Right: stimulus–response matrices (confusion matrices; see Figure 2) showing the proportion (area of black circle) of responses to a given (unknown) stimulus azimuth (x-axis) classified at each response azimuth (y-axis). Classification assigned each neural population response in the ‘‘test’’ set to the stimulus azimuth whose mean population response in an independently selected set of ‘‘training’’ trials was most similar. In some conditions, test and training trials were drawn from the same set of (matching level) trials: 20 dB (first column) or 40 dB (far right column). In others, test and training trials reflected different-level stimuli: 40-dB test stimuli classified based on a 20-dB training set (second column), or 20-dB test stimuli classified based on a 40-dB training set (third column). The contralateral and ipsilateral subpopulation responses (top and middle rows) accurately localize fixed-level stimuli, but are strongly biased when tested at non-trained stimulus levels. In contrast, the difference between responses (bottom row) remains relatively unbiased in all conditions, although responses to stimuli at untrained levels do exhibit compressed range and increased variability of classification. DOI: 10.1371/journal.pbio.0030078.g006

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CITATION STYLE

APA

Stecker, G. C., Harrington, I. A., & Middlebrooks, J. C. (2005). Location coding by opponent neural populations in the auditory cortex. In PLoS Biology (Vol. 3, pp. 0520–0528). https://doi.org/10.1371/journal.pbio.0030078

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