Neural correlates of behavioral amplitude modulation sensitivity in the budgerigar midbrain

Abstract

Amplitude modulation (AM) is a crucial feature of many communication signals, including speech. Whereas average discharge rates in the auditory midbrain correlate with behavioral AM sensitivity in rabbits, the neural bases of AM sensitivity in species with human-like behavioral acuity are unexplored. Here, we used parallel behavioral and neurophysiological experiments to explore the neural (midbrain) bases of AM perception in an avian speech mimic, the budgerigar (Melopsittacus undulatus). Behavioral AM sensitivity was quantified using operant conditioning procedures. Neural AM sensitivity was studied using chronically implanted microelectrodes in awake, unrestrained birds. Average discharge rates of multiunit recording sites in the budgerigar midbrain were insufficient to explain behavioral sensitivity to modulation frequencies <100 Hz for both tone- and noise-carrier stimuli, even with optimal pooling of information across recording sites. Neural envelope synchrony, in contrast, could explain behavioral performance for both carrier types across the full range of modulation frequencies studied (16-512 Hz). The results suggest that envelope synchrony in the budgerigar midbrain may underlie behavioral sensitivity to AM. Behavioral AM sensitivity based on synchrony in the budgerigar, which contrasts with rate-correlated behavioral performance in rabbits, raises the possibility that envelope synchrony, rather than average discharge rate, might also underlie AM perception in other species with sensitive AM detection abilities, including humans. These results highlight the importance of synchrony coding of envelope structure in the inferior colliculus. Furthermore, they underscore potential benefits of devices (e.g., midbrain implants) that evoke robust neural synchrony.

Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise

“…The budgerigar is a small parrot species and speech mimic with human-like behavioral sensitivity to complex sounds including AM (Dooling and Searcy 1981;Carney et al 2013), consonants (Dooling et al 1989), synthesized speech tokens along the /ra-la/ continuum (Dooling et al 1995), and different vowels (Dooling and Brown 1990;reviewed in Dooling et al 2000). Neurons in the budgerigar midbrain have band-enhanced modulation tuning, similar to that observed in mammals (Henry et al 2016). Behavioral and neurophysiological experiments were conducted in quiet and in background noise.…”

“…Representative transformed neural recordings are shown in a previous publication (see Fig. 2 of Henry et al 2016). The response of the Teager energy operator is related to the instantaneous frequency and amplitude of the input signal and hence accentuates voltage spikes associated with neural action potentials.…”

“…The test apparatus and procedures used to estimate behavioral auditory thresholds in trained budgerigars have been described previously (Carney et al 2013;Henry et al 2016). Briefly, behavioral testing was conducted in a sound isolation chamber (0.3 m 3 inside volume) lined with 6.7-cm thick acoustic foam.…”

“…The materials and methods used to implant electrodes and record from the budgerigar IC have been described previously (Henry et al 2016). Briefly, tungsten microelectrodes (3-5 MΩ; Microprobes, Gaithersburg, MD USA) were fixed to a miniature microdrive ('nDrive'; Neuronexus, Ann Arbor, MI USA) and lowered through a~1-mm dorsal craniotomy site to the right IC under stereotaxic control in anesthetized birds.…”

“…The frequency and modulation tuning properties of recording sites in the budgerigar IC have been described previously (Henry et al 2016). Briefly, individual recording sites (N = 64) showed excitatory rate responses to tone stimuli with bandlimited frequency tuning (Fig.…”