Sound localization behavior in ferrets: comparison of acoustic orientation and approach-to-target responses

Abstract

Auditory localization experiments typically either require subjects to judge the location of a sound source from a discrete set of response alternatives or involve measurements of the accuracy of orienting responses made toward the source location. To compare the results obtained by both methods, we trained ferrets by positive conditioning to stand on a platform at the center of a circular arena prior to stimulus presentation and then approach the source of a broadband noise burst delivered from 1 of 12 loudspeakers arranged at 30 degrees intervals in the horizontal plane. Animals were rewarded for making a correct choice. We also obtained a non-categorized measure of localization accuracy by recording head-orienting movements made during the first second following stimulus onset. The accuracy of the approach-to-target responses declined as the stimulus duration was reduced, particularly for lateral and posterior locations, although responses to sounds presented in the frontal region of space and directly behind the animal remained quite accurate. Head movements had a latency of approximately 200 ms and varied systematically in amplitude with stimulus direction. However, the final head bearing progressively undershot the target with increasing eccentricity and rarely exceeded 60 degrees to each side of the midline. In contrast to the approach-to-target responses, the accuracy of the head orienting responses did not change much with stimulus duration, suggesting that the improvement in percent correct scores with longer stimuli was due, at least in part, to re-sampling of the acoustical stimulus after the initial head turn had been made. Nevertheless, for incorrect trials, head orienting responses were more closely correlated with the direction approached by the animals than with the actual target direction, implying that at least part of the neural circuitry for translating sensory spatial signals into motor commands is shared by these two behaviors.

Fig. 1

Effect of stimulus duration and direction on auditory localization accuracy. (A) Percent correct scores at each of the 12 speakers positioned at equal intervals in the horizontal plane. 0° Is directly in front of the animal; negative speaker angles indicate stimulus locations on the animal’s left. Data are shown for a sound duration of 40 ms. The performance of individual animals is indicated by the thin lines and the overall mean performance by the thick black line. The gray area corresponds to 1 standard deviation on either side of this group mean. (B) Mean percentage correct scores for all animals at each sound duration and azimuth location tested. Data obtained at the speaker location directly behind the animals are shown as both 180° and − 180° in order to highlight the left–right symmetry of the responses. (C) Data pooled from all animals and speaker locations showing the percentage of correct trials, front–back error trials and all other error trials for each stimulus duration.

Fig. 2

Variation in localization error magnitude with stimulus duration and target direction. (A) Incidence of error magnitude (in increments of 30°, the intervals between the speakers) at each sound duration; data are pooled for all speaker locations. (B) Incidence of error magnitude at each of the 12 speaker locations; data are pooled for different sound durations.

Fig. 3

Effect of sound level on auditory localization accuracy. Percentage correct scores at each of the 12 speakers for 40 ms (A), 200 ms (B) and 1000 ms (C) noise bursts. The mean values obtained at each of the five sound levels used (from 56 to 84 dB SPL) are indicated by the thin lines and the overall mean performance by the thick black line. The gray area corresponds to 1 standard deviation on either side of this group mean. Varying sound level had little effect on localization accuracy at any of the stimulus durations.

Fig. 4

Response time in the auditory localization approach-to-target task. (A) Distribution of times between stimulus onset and the animal licking a reward spout, subdivided by whether the animals approached the correct reward spout (‘correct trials’) or not (‘incorrect trials’). The thick lines represent all trials, whereas the thin lines represent only the trials for the three shortest stimulus durations (40, 100 and 200 ms). (B) Proportion of correct and incorrect trials for different response times, grouped in 1 s intervals, for all sound durations and target locations. Note that correct responses tended to be made more quickly than incorrect ones.

Fig. 5

Sound-evoked head orienting responses. (A) Plot showing how the mean horizontal angle of the head changes over time after stimulus onset for the different target locations. Only data from correct approach-to-target trials are shown. Negative values indicate positions toward the left and positive values to the right. (B) Mean final head bearing plotted against stimulus location. Mean values from individual animals are indicated by thin lines and the overall mean by the thick line. The gray area corresponds to ±1 SD of the overall mean. Note the increasing undershoot in the final head bearing with increasing eccentricity of the target location and the greater variability for targets at 180°.

Fig. 6

Mean latency (thin lines) and end time (thick lines) of the initial head turns, shown for trials in which the animal approached and licked either the correct or incorrect reward spout. Note that head orienting movements tended to have shorter latencies on correct trials.

Fig. 7

Distribution of final head bearings in response to target location at 180°, grouped in 10° intervals. The direction and magnitude of these head movements were highly variable and showed no correlation with the consistently high percent correct score for that target location (shown by the thick black line; the dashed line is the linear regression line for the percentage correct score versus head bearing angle).

Fig. 8

Distribution of the conditional probabilities of final head bearings given the target locations shown on the x axis for stimulus durations of 40 ms (A) and 2000 ms (B). See main text for details. These conditional probabilities were estimated from the observed response frequencies.

Fig. 9

Distribution for the three shortest stimulus durations (40–200 ms) of the conditional probabilities of the final head bearings as a function of target location for correct trials (A, n = 13443) and for trials where the approach-to-target response was incorrect (B, n = 7475). The distribution for the incorrect trials shown in B shows greater dispersion than that for the correct trials shown in A. (C) Conditional probabilities of final head bearing for each approach-to-target response location in the trials where the animal approached the wrong reward spout (same trials as in B). Note that the data shown in B are more dispersed than those in C, suggesting that the head orienting response is more closely related to the location approached by the animals than by the actual direction of the target.

Fig. 10

Histogram of differences between the conditional probabilities p(target location | final head bearing) and p(response location | final head bearing) for the 7475 incorrect trials obtained with stimulus durations of ≤200 ms. The histogram is centered around slightly negative values (mean= -0.016), which indicates that, on average, head bearing predicts approach-to-target response direction more accurately than stimulus direction.