Role of auditory cortex in sound localization in the midsagittal plane

Abstract

Although the auditory cortex is known to be essential for normal sound localization in the horizontal plane, its contribution to vertical localization has not so far been examined. In this study, we measured the acuity with which ferrets could discriminate between two speakers in the midsagittal plane before and after silencing activity bilaterally in the primary auditory cortex (A1). This was achieved either by subdural placement of Elvax implants containing the GABA A receptor agonist muscimol or by making aspiration lesions after determining the approximate location of A1 electrophysiologically. Psychometric functions and minimum audible angles were measured in the upper hemifield for 500-, 200-, and 40-ms noise bursts. Muscimol-Elvax inactivation of A1 produced a small but significant deficit in the animals' ability to localize brief (40-ms) sounds, which was reversed after removal of the Elvax implants. A similar deficit in vertical localization was observed after bilateral aspiration lesions of A1, whereas performance at longer sound durations was unaffected. Another group of ferrets received larger lesions, encompassing both primary and nonprimary auditory cortical areas, and showed a greater deficit with performance being impaired for long- and short-duration (500- and 40-ms, respectively) stimuli. These data suggest that the integrity of the auditory cortex is required to successfully utilize spectral localization cues, which are thought to provide the basis for vertical localization, and that multiple cortical fields, including A1, contribute to this task.

Fig. 1

Summary of animals used in this study. Gray boxes indicate that an animal was tested for its ability to localize sound in the midsagittal plane in the condition indicated. For example, animal F0206 was trained and tested at all stimulus durations, providing control data (“normal”). These measurements were then repeated with 40-ms noise bursts after inactivating primary auditory cortex (A1) bilaterally with muscimol-Elvax (“elvax”), again after Elvax removal (“post-elvax”), and once more after making bilateral aspiration lesions of A1 (“small lesion”); “large lesion” refers to animals in which more extensive regions of auditory cortex were removed bilaterally. Dark gray boxes indicate that the animal was used for behavioral testing only, whereas light gray boxes (i.e., all A1 small lesions) indicate that electrophysiological recordings were made as well, before aspirating the cortex. Empty boxes indicate that the animal was used for electrophysiological recordings only.

Fig. 2

Floor plan (A) and side view (B) of the testing arena used to measure vertical localization. Animals were trained to discriminate between two broadband sound sources located on the midsagittal plane and differing only in their vertical locations. The testing chamber was circular in shape (radius 75 cm). To initiate a trial the ferret stood on the central platform and licked the start spout. This triggered the presentation of a noise burst from one of 2 speakers located on a curved rail outside the wire-mesh dome that enclosed the chamber. Response spouts were located at +90 and –90°.

Fig. 3

Effects of muscimol-Elvax (A) and drug-free Elvax (B) implants on activity in ferret visual cortex. Recordings were made 2 h after implantation. Surface-normal electrode penetrations were made either directly beneath the Elvax (through a small hole that had been bored before implantation) or close to the lateral edge of the implant. Recordings were made every 50 μm and each sampling site is represented by a box: black boxes indicate that no activity was recorded, gray boxes indicate spontaneous activity, and white boxes mark positions where visual activity was recorded. Muscimol-Elvax largely eliminated activity throughout the depth of the cortex, whereas the drug-free control implants appeared to have no effect on the activity of the cortex.

Fig. 4

Location of the cortical lesions in 2 of the ferrets (0139 and 0206) used in this study. A: schematic of a ferret brain illustrating the location of the major gyri (OB, olfactory bulb; OBG, orbital gyrus; ASG, anterior sigmoid gyrus; PSG, posterior sigmoid gyrus; LG, lateral gyrus; SSG, suprasylvian gyrus; MEG, middle ectosyslvian gyrus; PEG, posterior ectosyslvian gyrus; AEG, anterior ectosyslvian gyrus) and sulci (prs, presylvian sulcus; prs, perirhinal sulcus; cng, coronal sulcus; as, anterior sigmoid; ls, lateral sulcus; sss, suprasylvian sulcus; pss, pseudosylvian sulcus). Inset: auditory cortex, located on the ectosyslvian gyrus, with functional subdivisions marked (A1, primary auditory cortex; AAF, anterior auditory field; PPF, posterior pseudo-sylvian field; PSF, posterior suprasylvian field; VP, ventral posterior field; ADF, anterior dorsal field; AVF, anterior ventral field; fAES, anterior ecto-syslvian sulcal field). B: horizontal MRI slice showing the location (in white) of the large bilateral temporal lobe lesions in animal F0139. C–E: coronal sections stained for Nissl substance taken at the approximate locations indicated by the dashed lines in B. F and G: photographs of the brain of animal F0206, in which A1 had been aspirated bilaterally. H–J: coronal sections stained for Nissl substance taken at the approximate locations marked by the dashed lines in F and G. Note that this lesion has maintained the integrity of the white matter.

Fig. 5

Schematics showing the size and location of the aspiration lesions made in each animal. In each case the suprasylvian sulcus and the pseudosyl-vian sulcus are shown with the lesion shaded in gray. A: schematic showing the location of auditory cortical fields (abbreviations as in Fig. 4). B–D: animals F9932, F0139, and F0140 received “large” lesions that included both the primary auditory fields and varying extents of the more ventral nonprimary fields. More restricted lesions were made in the other animals (E–H) after electrophysiological identification of the ventral low-frequency border of A1. D, dorsal; R, rostral.

Fig. 6

Localization in the midsagittal plane. A: raw data (% correct scores for 40-ms noise bursts as a function of the vertical angular separation of the speakers) and the fitted psychometric function, from which the minimum audible angle (MAA) was calculated, for animal F0249. These data were obtained before any cortical manipulation. B–D: control data for all the animals. Each line represents the psychometric function from a different animal for stimulus durations of 500 ms (B), 200 ms (C), and 40 ms (D). Mean MAAs, corresponding to the 75% score, were 27.0 ± 7.7° at 500 ms, 31.7 ± 6.3° at 200 ms, and 35.3 ± 9.6° at 40 ms.

Fig. 7

Effects of loss of activity in A1 on sound localization in the midsagittal plane. A: data from 6 animals showing the mean percentage correct score for each animal at the speaker separation indicated before implantation of muscimol-Elvax (open symbols) and with the implants in place (filled symbols). B: data from 4 animals showing the scores obtained before (open symbols) and after bilateral removal of A1 (filled symbols). Note that the ferrets tend to make lower scores after inactivation or aspiration of A1. One exception to this was F0318, whose data are indicated by the diamonds in A, in which the Elvax sheet became encapsulated by dura and displaced from the surface of the left A1. This is the same animal, again indicated by the diamonds in B, whose auditory cortex lesion was effective unilaterally only.

Fig. 8

Effect of bilateral inactivation of A1 by muscimol-Elvax on psychometric functions in the midsagittal plane. Stimuli were 40-ms noise bursts. Data from individual animals are shown in each panel. Each line shows the fitted psychometric function obtained before implantation of muscimol-Elvax (gray line) and with the implants in place (black line) for a different ferret. Two animals were retested after the muscimol-Elvax implants had been removed (A, B, stippled line). Note that the data in F are from F0318, the animal in which the Elvax had become encapsulated by dura and displaced from the surface of the cortex.

Fig. 9

Effect of lesioning A1 on localization in the midsagittal plane. Stimuli were 40-ms noise bursts. Data from individual animals are shown in each panel. Each line shows the fitted psychometric function obtained before (gray lines) and after (black lines) A1 was removed bilaterally. Note that the data in D are from F0318, the animal in which A1 turned out to be lesioned on one side only.

Fig. 10

Effect of lesioning larger regions of auditory cortex on localization in the midsagittal plane. A: bar chart showing the mean (±SD) number of trials taken by the control animals and by each the animals with large bilateral lesions of auditory cortex to reach a criterion level of performance (>85% correct with 500-ms noise bursts at the maximum speaker separation). B–D: each line shows the fitted psychometric function for these animals at different stimulus durations. Mean (±SD) scores achieved by the control animals (n = 9) are shown by the solid lines and error bars. Other lines show the psychometric functions for the 3 ferrets with large cortical lesions, which all lie below the range of values obtained for the control group. Animal F9932 was unable to perform above the level expected by chance with either 200- or 40-ms noise bursts.