Functional selection of adaptive auditory space map by GABA(a)-mediated inhibition

Science

Volumn 284, Issue 5416, 1999, Pages 962-965

  Zheng, Weimin ^a   Knudsen, Eric I ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; BIRD; BRAIN MAPPING; CENTRAL NERVOUS SYSTEM; GABAERGIC SYSTEM; INFERIOR COLLICULUS; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; BICUCULLINE; BRAIN MAPPING; CUES; INFERIOR COLLICULUS; LEARNING; NERVE NET; NEURAL INHIBITION; NEURONAL PLASTICITY; PHOTIC STIMULATION; RECEPTORS, GABA-A; SOUND LOCALIZATION; STRIGIFORMES; SUPERIOR COLLICULUS; VISUAL FIELDS; VISUAL PATHWAYS;

ANIMALIA; AVES; STRIGIFORMES; TYTO ALBA;

EID: 0033532336     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.284.5416.962     Document Type: Article

References (30)

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14. Neurophysiology: We prepared the owls for repeated neurophysiological recording sessions as described (3). We discontinued anesthesia (1.5% halothane in a 55:45 mixture of oxygen and nitrous oxide) after the owl was positioned and secured in a sound chamber. The owls remained calm for the duration of the experiment. We conducted the experiments in the rostrolateral ICX, where neurons are tuned to frontal space in normal owls (ITDs range from 0 to 20 μs, contralateral ear leading). In prism-reared owls, the ITD tuning of neurons in this region has been shown to shift reliably in response to juvenile prism experience (3, 16). We recorded unit activity with a five-barrel glass microelectrode, the central barrel of which contained a carbon fiber 7 μm in diameter. The remaining four barrels had 2-to 4-μm tips and were used to apply bicuculline methiodide (Sigma) (10 mM in 0.9% saline, adjusted to pH 3.0 with HCI). Units were isolated with a waveform detector. We consistently attempted to isolate the largest unit waveforms. We do not know, however, the degree to which these waveforms corresponded to the discharges of single neurons. We used unit response properties (tuning for frequency, ITD, and interaural level difference) and the progression of these properties with electrode advance to indicate that the recording sites were in the ICX (3, 8). The experimental protocol was approved by the Animal Care and Use Committee at Stanford University School of Medicine.
15. Auditory stimulation: ITD tuning properties were characterized as described in (3). Briefly, broadband (4 to 12 kHz) noise stimuli were generated digitally and presented dichotically at 10 dB above unit threshold. We determined unit tuning for ITD by presenting a series of 50-ms noise bursts in which ITD was varied in a random, interleaved pattern. We measured ITD tuning by using the optimal interaural level difference for the site. Responses were defined as the number of spikes in the 100 ms after stimulus onset minus the number of spikes in the 100 ms before stimulus onset (baseline).
16. Iontophoresis protocol: At each site, we first assessed ITD tuning three to seven times without drug ejection by using a 20-repetition stimulus series. We then applied bicuculline iontophoretically at a current that resulted in a clear increase in responses; this current ranged from 30 to 60 nA. Once responses were stable, we reassessed ITD tuning three to seven times by using the same 20-repetition stimulus series. Finally, we halted drug ejection, allowed responses to recover to the predrug level and assessed ITD tuning again.
17. Rearing conditions: This study is based on neurophysiological recordings from eight barn owls (Tyto alba), all of which were raised together in our colony. Two of the owls were raised normally and six were raised wearing Fresnel prismatic lenses (VisionCare/3M), mounted in spectacle frames, that displaced the visual field horizontally 23° to the left or right. The spectacle frames were secured with a bolt that was cemented to the skull when the owls were 60 to 70 days old, the age at which they are full grown and leave the nest The flight room in which they lived provided them with a rich visual and auditory environment. Neurophysiological recordings began when the owls were 130 days old, after they had worn spectacles continuously for at least 60 days.
18. Predicting normal best ITD: The value of ITD to which a site in the ICX will be tuned in a normal owl can be predicted (±10 μs) by recording units along a transect that passes through the representation of a given value of ITD both in the central nucleus of the inferior colliculus (ICC) and in the optic tectum (3). In normal owls, sites in the ICX that lie along this transect are also tuned to this same value of ITD. In prism-reared owls, the representation of ITD in the ICC is not altered from normal, and normal ITD tuning in the optic tectum can be inferred from the location of a site's visual receptive field, which is also unaltered by prism experience (3). In this study, the predicted normal ITD tuning for a transect was determined at the beginning of each experiment from the best ITD measured in the ICC and from the best ITD inferred from the visual receptive field measured in the optic tectum. All ICX recordings were made along this transect.
19. We calculated effectiveness of inhibition for each ITD that evoked at least 15% of the maximum response at each site. To compare the effectiveness of inhibition across different groups of owls (Fig. 3A), we averaged the values of this metric across all sites from each group for a given ITD value [C. Koch, T. Poggio, V. Torre, Proc. Natl. Acad. Sci. U.S.A. 80, 2799 (1983); N. Qian and T. J. Sejnowski, Ibid. 87, 8145 (1990)].
20. We calculated effectiveness of inhibition for each ITD that evoked at least 15% of the maximum response at each site. To compare the effectiveness of inhibition across different groups of owls (Fig. 3A), we averaged the values of this metric across all sites from each group for a given ITD value [C. Koch, T. Poggio, V. Torre, Proc. Natl. Acad. Sci. U.S.A. 80, 2799 (1983); N. Qian and T. J. Sejnowski, Ibid. 87, 8145 (1990)].
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26. To evaluate whether an ITD tuning curve was fully returned back to normal after prism removal, we compared the responses on the two flanks of the tuning curve. A tuning curve was deemed fully returned back to normal when the sum of the responses to ITDs 30, 40, and 50 μs on each side away from the predicted normal best ITD were not significantly different (two-tailed t test, P > 0.05).
27. Unpaired two-tailed t tests were used throughout this study.
28. At 12 of 28 ICX sites tested in prism-reared owls, responses to normal ITDs were significantly weaker than responses to learned ITDs when inhibition was blocked (two-tailed t tests, P < 0.05; Fig. 3B, filled circles) (at the remaining 16 sites, responses to normal and teamed ITDs were not significantly different when inhibition was blocked; P > 0.05). In addition, with inhibition blocked, responses to normal ITDs were weaker in prism-reared owls than in normal owls (P = 0.009; Fig. 3B, open circles versus filled circles) even though there was no difference between the strengths of responses to normal ITDs in normal owls and responses to learned ITDs in prism-reared owls (P = 0.19).
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30. Supported by a grant from the McKnight Foundation and by grant 5 R01 DC00155-18 to E.I.K. from the Notional Institute on Deafness and Other Communication Disorders. NIH; by a Stanford University School of Medicine Dean's Postdoctoral Fellowship; and by NIH Individual National Research Service Award F32 DC00307-01 to W.Z. We thank P. Knudsen for technical support throughout this study and W. DeBello, P. Hyde, and G. Miller for critical review of the manuscript.