Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song

Abstract

The interplay between inhibition and excitation can regulate behavioral expression and control, including the expression of communicative behaviors like birdsong. Computational models postulate varying degrees to which inhibition within vocal motor circuitry influences birdsong, but few studies have tested these models by manipulating inhibition. Here we enhanced and attenuated inhibition in the cortical nucleus HVC (used as proper name) of Bengalese finches ( Lonchura striata var. domestica). Enhancement of inhibition (with muscimol) in HVC dose-dependently reduced the amount of song produced. Infusions of higher concentrations of muscimol caused some birds to produce spectrally degraded songs, whereas infusions of lower doses of muscimol led to the production of relatively normal (nondegraded) songs. However, the spectral and temporal structures of these nondegraded songs were significantly different from songs produced under control conditions. In particular, muscimol infusions decreased the frequency and amplitude of syllables, increased various measures of acoustic entropy, and increased the variability of syllable structure. Muscimol also increased sequence durations and the variability of syllable timing and syllable sequencing. Attenuation of inhibition (with bicuculline) in HVC led to changes to song distinct from and often opposite to enhancing inhibition. For example, in contrast to muscimol, bicuculline infusions increased syllable amplitude, frequency, and duration and decreased the variability of acoustic features. However, like muscimol, bicuculline increased the variability of syllable sequencing. These data highlight the importance of inhibition to the production of stereotyped vocalizations and demonstrate that changes to neural dynamics within cortical circuitry can differentially affect spectral and temporal features of song. NEW & NOTEWORTHY We reveal that manipulations of inhibition in the cortical nucleus HVC affect the structure, timing, and sequencing of syllables in Bengalese finch song. Enhancing and blocking inhibition led to opposite changes to the acoustic structure and timing of vocalizations, but both caused similar changes to vocal sequencing. These data provide support for computational models of song control but also motivate refinement of existing models to account for differential effects on syllable structure, timing, and sequencing.

Partially observable Markov models inferred using statistical tests reveal context-dependent syllable transitions in Bengalese finch songs

“…This increase is mostly due to the branching points that have dominant transitions becoming more "equalized", such that the branches have 22 similar transition probabilities. Similar effects were seen in real-time manipulation of auditory feedback (Sakata and Brainard, 2006), cooling HVC (Zhang et al, 2017) or enhancing inhibition (Isola et al, 2020) in HVC of the Bengalese finch. It would be interesting to investigate whether there is a common neural mechanism across these manipulations.…”

“…in studies involving perturbations of auditory feedback (Sakata and Brainard, 2006), cooling of the HVC (Zhang et al, 2017), and the enhancement of inhibition within the HVC (Isola et al, 2020) in Bengalese finches. Exploring the potential for a unified neural mechanism underlying these diverse manipulations presents an intriguing avenue for further research.…”

Plasticity of stereotyped birdsong driven by chronic manipulation of cortical-basal ganglia activity

“…CMA 7 microdialysis probes were modified into an untethered reservoir system to allow for passive diffusion of drug in freely behaving birds. 22,28,86 Briefly, the inlet and outlet tubes were shortened, and the inlet tube was connected via an adaptor (CMA) to PE-20 tubing that served as a reservoir. For the duration of the experiment, the reservoirs were filled several times per day with 0.025 M phosphate buffered saline (PBS; pH = 7.4) or drug.…”

Norepinephrine in the avian auditory cortex enhances developmental song learning

“…After 4-7 days of recovery from surgery, dummy probes in the guide cannulae were replaced with microdialysis probes (Harvard Apparatus, Hollison, MA, CMA 7). CMA 7 microdialysis probes were modified into an untethered reservoir system to allow for passive diffusion of drug in freely behaving birds (51)(52)(53)(54). Specifically, inlet and outlet tubes were cut to 4-6 cm in length and served as a reservoir for fluids.…”