Multiple mechanisms shape FM sweep rate selectivity: complementary or redundant?

Anthony J Williams,Zoltan M Fuzessery

doi:10.3389/fncir.2012.00054

Abstract

Auditory neurons in the inferior colliculus (IC) of the pallid bat have highly rate selective responses to downward frequency modulated (FM) sweeps attributable to the spectrotemporal pattern of their echolocation call (a brief FM pulse). Several mechanisms are known to shape FM rate selectivity within the pallid bat IC. Here we explore how two mechanisms, stimulus duration and high-frequency inhibition (HFI), can interact to shape FM rate selectivity within the same neuron. Results from extracellular recordings indicated that a derived duration-rate function (based on tonal response) was highly predictive of the shape of the FM rate response. Longpass duration selectivity for tones was predictive of slowpass rate selectivity for FM sweeps, both of which required long stimulus durations and remained intact following iontophoretic blockade of inhibitory input. Bandpass duration selectivity for tones, sensitive to only a narrow range of tone durations, was predictive of bandpass rate selectivity for FM sweeps. Conversion of the tone duration response from bandpass to longpass after blocking inhibition was coincident with a change in FM rate selectivity from bandpass to slowpass indicating an active inhibitory component to the formation of bandpass selectivity. Independent of the effect of duration tuning on FM rate selectivity, the presence of HFI acted as a fastpass FM rate filter by suppressing slow FM sweep rates. In cases where both mechanisms were present, both had to be eliminated, by removing inhibition, before bandpass FM rate selectivity was affected. It is unknown why the auditory system utilizes multiple mechanisms capable of shaping identical forms of FM rate selectivity though it may represent distinct but convergent modes of neural signaling directed at shaping response selectivity for important biologically relevant sounds.

Highlights

The breakdown of complex sensory input into simpler components for extraction of specific cues that guide behavior is a common strategy utilized across sensory modalities
We focus on how more than one mechanism can interact to shape the selectivity for frequency modulated (FM) sweep rate
The remaining neurons (28%, 22/79) were not tuned to sweep rates, and instead exhibited slowpass rate selectivity (Figure 1B). This percentage of rate-tuned neurons is similar to that reported in previous studies of the pallid bat inferior colliculus (IC) (Fuzessery et al, 2010)

Summary

Introduction

The breakdown of complex sensory input into simpler components for extraction of specific cues that guide behavior is a common strategy utilized across sensory modalities. This involves a reduction of complex sounds into their individual spectrotemporal components (Brugge, 1992). Many species exhibit a strong selectivity for the rate and direction of frequency modulations (FMs), which are common components of complex sounds (Pollak and Park, 1995; Andoni and Pollak, 2011). Several underlying mechanisms have been identified that shape FM selectivity involving the spectrotemporal integration of excitatory and inhibitory inputs across the receptive field of an auditory neuron (Suga, 1968; Britt and Starr, 1976; Heil et al, 1992; Shannon-Hartman et al, 1992; Gordon and O’Neill, 1998; Gittelman et al, 2009; Fuzessery et al, 2010). The high-frequency region of the pallid bat inferior colliculus (IC) is ideal for this type of analysis due to a high degree of rate selectivity for the downward FM sweeps of their echolocation call (Brown, 1976; Bell, 1982; Fuzessery et al, 1993) and because the mechanisms driving FM rate selectivity have been identified (Fuzessery et al, 2010)

Methods

Results

Conclusion