Midbrain-Level Neural Correlates of Behavioral Tone-in-Noise Detection: Dependence on Energy and Envelope Cues.

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  • Additional Information
    • Source:
      Publisher: Society for Neuroscience Country of Publication: United States NLM ID: 8102140 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1529-2401 (Electronic) Linking ISSN: 02706474 NLM ISO Abbreviation: J Neurosci Subsets: MEDLINE
    • Publication Information:
      Publication: Washington, DC : Society for Neuroscience
      Original Publication: [Baltimore, Md.] : The Society, c1981-
    • Subject Terms:
      Acoustic Stimulation* ; Signal-To-Noise Ratio*; Auditory Pathways/*physiology ; Auditory Threshold/*physiology ; Conditioning, Operant/*physiology ; Inferior Colliculi/*physiology ; Melopsittacus/*physiology ; Neurons/*physiology; Animals ; Brain Mapping ; Cues ; Electrodes, Implanted ; Female ; Inferior Colliculi/cytology ; Male ; Noise ; Pitch Perception/physiology
    • Abstract:
      Hearing in noise is a problem often assumed to depend on encoding of energy level by channels tuned to target frequencies, but few studies have tested this hypothesis. The present study examined neural correlates of behavioral tone-in-noise (TIN) detection in budgerigars ( Melopsittacus undulatus , either sex), a parakeet species with human-like behavioral sensitivity to many simple and complex sounds. Behavioral sensitivity to tones in band-limited noise was assessed using operant-conditioning procedures. Neural recordings were made in awake animals from midbrain-level neurons in the inferior colliculus, the first processing stage of the ascending auditory pathway with pronounced rate-based encoding of stimulus amplitude modulation. Budgerigar TIN detection thresholds were similar to human thresholds across the full range of frequencies (0.5-4 kHz) and noise levels (45-85 dB SPL) tested. Also as in humans, thresholds were minimally affected by a challenging roving-level condition with random variation in background-noise level. Many midbrain neurons showed a decreasing response rate as TIN signal-to-noise ratio (SNR) was increased by elevating the tone level, a pattern attributable to amplitude-modulation tuning in these cells and the fact that higher SNR tone-plus-noise stimuli have flatter amplitude envelopes. TIN thresholds of individual neurons were as sensitive as behavioral thresholds under most conditions, perhaps surprisingly even when the unit's characteristic frequency was tuned an octave or more away from the test frequency. A model that combined responses of two cell types enhanced TIN sensitivity in the roving-level condition. These results highlight the importance of midbrain-level envelope encoding and off-frequency neural channels for hearing in noise. SIGNIFICANCE STATEMENT Detection of target sounds in noise is often assumed to depend on energy-level encoding by neural processing channels tuned to the target frequency. In contrast, we found that tone-in-noise sensitivity in budgerigars was often greatest in midbrain neurons not tuned to the test frequency, underscoring the potential importance of off-frequency channels for perception. Furthermore, the results highlight the importance of envelope processing for hearing in noise, especially under challenging conditions with random variation in background noise level over time.
      (Copyright © 2021 the authors.)
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    • Grant Information:
      R01 DC001641 United States DC NIDCD NIH HHS; R01 DC017519 United States DC NIDCD NIH HHS
    • Contributed Indexing:
      Keywords: budgerigar; envelope; inferior colliculus; operant conditioning; roving level; tone in noise
    • Publication Date:
      Date Created: 20210716 Date Completed: 20211203 Latest Revision: 20240402
    • Publication Date:
      20240403
    • Accession Number:
      PMC8387112
    • Accession Number:
      10.1523/JNEUROSCI.3103-20.2021
    • Accession Number:
      34266898