Communication call-evoked gamma-band activity in the auditory cortex of awake bats is modified by complex acoustic features

Abstract

Mustached bats emit an acoustically rich variety of calls for social communication. In the posterior primary auditory cortex, activity of neural ensembles measured as local field potentials (LFPs) can uniquely encode each call type. Here we report that LFPs recorded in response to calls contain oscillatory activity in the gamma-band frequency range (> 20 Hz). The power spectrum of these high-frequency oscillations shows either two peaks of energy (at 40 Hz and 100 Hz), or just one peak at 40 Hz. The relative power of gamma-band activity in the power spectrum of a call-evoked LFP correlates significantly with the ‘harmonic complexity’ of a call. Gamma-band activity is attenuated with reversal of frequency-modulated calls. Amplitude modulation, even when asymmetric across call reversals, has no significant effect on gamma-band activity. These results provide the first experimental evidence that complex features within different groups of species-specific calls modify the power spectrum of evoked gamma-band activity.

Introduction

Neural encoding of spectrotemporal information for recognition of complex acoustic signals, such as speech sounds, is not well understood. One approach to tackling this complex problem is to study the neural responses simultaneously at the single cell and population levels. At the population level, synchronous oscillations provide a powerful mechanism to integrate activity within a local population of neurons as well as across long range, functionally connected neural structures (König et al., 1995). High-frequency gamma-band oscillation-driven temporal coordination of activity at the surface of the auditory cortex was previously described in response to tonal clicks and amplitude-modulated sounds (Barth and MacDonald, 1996, Brosch et al., 2002, Franowicz and Barth, 1995, MacDonald and Barth, 1995). These studies were based on epidural recordings in lightly anesthetized rats. The term “gamma-band” traditionally referred to high-frequency activity that is 30 to 80 Hz. More recently, Crone and co-workers have extended the upper limit of gamma-band activity to ∼ 150 Hz based on subdural electrocorticographic recordings in humans and define oscillation activity > 70 Hz as “high gamma” (Sinai et al., 2005). Although a few recent studies implicate the role of gamma-band oscillations on speech sound perception in humans (Crone et al., 2001, Sinai et al., 2005), there is no information nor any direct evidence for their role in processing social or communication calls in animals.

Mustached bats use a number of call types for social interactions and have proven to be useful animal models for understanding the neural coding of complex acoustic signals both for echolocation and communication. The posterior primary auditory cortex (AIp) of mustached bats contains a representation of the frequencies (from 7 kHz to 50 kHz) that are present within all communication calls emitted by this species (Kanwal et al., 1994). A previous study showed that the temporal response pattern of neuronal ensembles and possibly single neurons in this region of the primary auditory cortex changes consistently for each call type and could carry sufficient information to uniquely encode each call type (Medvedev and Kanwal, 2004). Both, slow-wave, local field potentials (LFPs) and spiking activity at any locus within AIp were patterned after call-specific dynamics. This dynamic activity contributed to a distributed representation of 14 different call types. This mechanism of neural encoding is in contrast to the ‘combination sensitivity’ (nonlinear facilitation of neural responses to combinations of sound features) that is rampant in other auditory cortical areas of mustached bats and is also present in many other vertebrate species (Fuzessery and Feng, 1983, Margoliash and Fortune, 1992, Ohlemiller et al., 1996, Rauschecker and Tian, 2004, Suga et al., 1978).

Here we performed a spectral analysis on some of the same and newly acquired LFP and spiking data to examine the contribution of oscillatory activity in the neural coding of social calls. We recorded single-unit activity and event-related LFPs simultaneously and at the same locus in response to the presentation of each of 7 frequency-shifted variants of 14 different types of simple syllabic calls. LFPs were used to examine the presence of gamma-band activity (this study) in response to different simple syllabic call types that constitute a large part of the vocal repertoire of mustached bats (Kanwal et al., 1994). The major question we address in this study is whether LFPs contain stimulus-specific oscillatory activity. If so, what role does this activity play in the representation of calls? Can a component of this type of synchronous activity be detected within simultaneously recorded single-unit activity at the same locus?

Our results suggest that a majority of species-specific calls presented to awake bats trigger “gamma-band” (20–100 Hz), activity within local field potentials (LFPs) recorded from the AIp area. The activity range that we observe from intracortical recordings overlaps the so-called “low” and “high” gamma-band activity as well as high beta (20–30 kHz) as classified by others. We refer to the range of frequencies 20 to 100 Hz, studied in our experiments, as simply “gamma-band activity.” This frequency range appears to be a more natural and continuous range for the effects observed in mustached bats. We further show that the pattern of the power spectrum of evoked gamma-band activity present within LFPs can be used to classify different call types into at least three distinct groups. These patterns of neural activity could provide a basis for a perceptual classification of different call types. Single- and/or few-unit spiking activity, although generally too sparse to visibly show gamma-band oscillations, is significantly correlated with the LFP data. These results provide the first experimental data for a proposed role of stimulus-locked gamma-band activity in a “call recognition event” within a neural network (Hopfield and Brody, 2000, Hopfield and Brody, 2001). As discussed, call recognition may be achieved via oscillatory activity within a local population of neurons that leads to perceptual grouping of acoustic features within a complex sound.