Sensitivity to direction and velocity of fast frequency chirps in the inferior colliculus of awake rabbit

Abstract

AbstractNeurons in the mammalian inferior colliculus (IC) are selective for the direction of fast frequency sweeps (chirps) contained in Schroeder-phase harmonic complexes (SCHR). This selectivity suggests a feature sensitivity in the mammalian IC to fast-chirp direction and velocity. Here, we introduced a novel stimulus consisting of aperiodic random chirps (ARCs) to characterize neural sensitivity to chirp direction and velocity in isolation from periodicity. Extracellular, single-unit recordings were made in the IC of Dutch-belted rabbits. SCHR stimuli had a range of velocities and periodicities, and ARC stimuli had matched velocities. Periodicity tuning was characterized using sinusoidally amplitude-modulated (SAM) noise. The prevalence of direction sensitivity and direction bias to chirps in SCHR and ARC responses was quantified, demonstrating that the majority of IC neurons (90.5%) were selective to SCHR-chirp direction and that sensitivity to the direction of aperiodic chirps was nearly universal (99.6%). Rate-velocity functions were constructed from ARC responses, revealing that neurons were commonly sensitive to the direction of lower-velocity (0.40 – 1.59 kHz/ms) chirps and were insensitive to the direction of higher-velocity chirps (3.16 – 9.24 kHz/ms). ARC and SAM noise responses were combined using a generalized linear model (GLM) to predict SCHR response rates. The GLM analysis revealed that both velocity and periodicity cues were required to explain SCHR responses. In general, velocity cues had a stronger effect on responses for harmonic stimuli with lower fundamental frequencies. This result has implications for neural encoding of complex sounds that combine envelope periodicities and frequency-sweeps.SignificanceComplex sounds such as speech and music contain fast frequency sweeps (chirps). Recently, responses to a stimulus with well-controlled periodic chirps, the Schroeder-harmonic complex (SCHR), have revealed diverse patterns of selectivity for the direction and velocity of chirps in the inferior colliculus. We studied the interaction between periodicity tuning and chirp selectivity underlying SCHR responses. Using a novel, aperiodic chirp stimulus, we demonstrate through rate-velocity functions that selectivity to chirp direction and velocity is commonly observed even for single chirps. Both neural velocity tuning and periodicity tuning are necessary to predict neural SCHR response rates. The diversity of the observed selectivity challenges models for SCHR selectivity based on cochlear phase dispersion.