Understanding the neurophysiological basis of auditory abilities for social communication: A perspective on the value of ethological paradigms

Highlights

• Processing communication sounds depends on general auditory abilities.

• Advantages to ethological paradigms to study general auditory abilities.

• Neuroethology has elucidated higher-order processing and nonlinear sensitivity.

• Neuroethology can help elucidate categorization of naturally variable calls.

• To test vocalization specialization, must study call-to-behavior transformations.

Abstract

Acoustic communication between animals requires them to detect, discriminate, and categorize conspecific or heterospecific vocalizations in their natural environment. Laboratory studies of the auditory-processing abilities that facilitate these tasks have typically employed a broad range of acoustic stimuli, ranging from natural sounds like vocalizations to “artificial” sounds like pure tones and noise bursts. However, even when using vocalizations, laboratory studies often test abilities like categorization in relatively artificial contexts. Consequently, it is not clear whether neural and behavioral correlates of these tasks (1) reflect extensive operant training, which drives plastic changes in auditory pathways, or (2) the innate capacity of the animal and its auditory system. Here, we review a number of recent studies, which suggest that adopting more ethological paradigms utilizing natural communication contexts are scientifically important for elucidating how the auditory system normally processes and learns communication sounds. Additionally, since learning the meaning of communication sounds generally involves social interactions that engage neuromodulatory systems differently than laboratory-based conditioning paradigms, we argue that scientists need to pursue more ethological approaches to more fully inform our understanding of how the auditory system is engaged during acoustic communication.

This article is part of a Special Issue entitled “Communication Sounds and the Brain: New Directions and Perspectives”.

Introduction

Acoustic communication between individuals of the same (conspecific) or different (heterospecific) species is an essential ingredient for the reproductive success and survival of many animals, yet our understanding of its underlying neurobiological mechanisms is still limited. In particular, the neural bases for the functional abilities that enable auditory communication are not fully understood. For example, in order to communicate, animals have to detect, discriminate and categorize a vocalization before being able to use it within their ecological and social contexts to guide behavior (Cheney and Seyfarth, 1980, Fischer and Hammerschmidt, 2011, Ghazanfar and Santos, 2004). What neural-, circuit-, and systems-level properties within the auditory pathway facilitate these abilities?

For the complex task of acoustic communication between individuals, especially in mammals, our knowledge of its neural basis is limited because of the technical and methodological challenges in designing appropriate experiments. Instead, most auditory neurobiology studies have utilized more controlled laboratory paradigms, which investigate “general” auditory processing of sounds, and use behaviors that do not involve social communication. From these studies, scientists often infer how an animal and its brain would function in natural communication contexts. Such “generalist” approaches have certainly yielded important insights into the basic mechanisms and limits of auditory processing but applying that knowledge to elucidate what occurs in the natural communication context remains an open area of investigation.

This leads to the key motivation for our review. We make two overall arguments in favor of a continued expansion of a complementary, neuroethological approach to studying auditory processing with ever-more naturalistic communication paradigms, despite their technical challenges. Indeed, a long tradition of auditory neuroethological research in model organisms like crickets, frogs, bats and songbirds (Covey and Casseday, 1999, Gentner and Margoliash, 2003a, Hahnloser and Kotowicz, 2010, Konishi, 2004, Moss et al., 2011, Neuweiler, 1990, Pollak, 1992, Razak and Fuzessery, 2010, Suga, 1988, Tsuzuki and Suga, 1988, Woolley, 2012) has established a conceptual foundation that can be used to approach similar questions in what some have considered more generalist laboratory animal models, like non-human primates and rodents. For those studying these latter species, it may not always seem necessary to employ natural vocal stimuli and behaviors to understand the general auditory-processing abilities of sound detection, discrimination or categorization (Dylla et al., 2013, Heffner et al., 2001, Klink and Klump, 2004, Ohl et al., 2001, Recanzone et al., 1993, Talwar et al., 2001). Here, we first try to counter this impression by using a few recent examples to illustrate how ethologically motivated approaches using vocalizations (or other “ethologically valid” stimuli with acoustic features derived from natural sounds) can provide insights into neural mechanisms that might otherwise be difficult to uncover.

Building on this, our second main point is that an important new direction in vocalization studies is to develop experimental designs that comprehensively incorporate behavioral contexts into neurophysiological research. This is important because behavioral context can profoundly affect neural processing. Thus, if we are to make progress understanding the neural mechanisms underlying acoustic communication, we must try to study how these mechanisms are engaged in more naturalistic communication behaviors.

In making these two arguments, an important question that arises is whether the neural substrates for vocalization processing differ from those used to process other types of sounds. For example, vocalizations may be more intrinsically arousing than other sounds and, thus, increase engagement of limbic areas relative to those other sounds (Ehret, 2005). Do these differences arise from evolutionarily tuned innate mechanisms present at birth or because of extensive experience during development and/or adulthood for ethologically important communication sounds? In other words, are vocalizations processed just like any another complex sound, or are they “special” in engaging unique (or, at least, different) processing mechanisms? Whereas recent findings begin to speak to this question, it is likely irresolvable in many species. Indeed, the ideal experiment would require the prohibitively burdensome task of providing an animal from birth as much experience hearing and responding to a category of non-vocal (e.g. synthetic) sounds as a “natural” category of species-specific vocalizations, and then performing neurophysiological studies to uncover differences.

Instead, we advocate that hearing scientists embrace the basic principle from neuroethology (Ewert et al., 1983): neural activity needs to be considered in the full context of the elicited behaviors. Following this principle, we believe that the more tractable answer to the aforementioned problem is to identify how (1) vocalizations and (2) synthetic stimuli that become behaviorally salient through operant conditioning differentially modulate neural transformations along the auditory pathway from an acoustic input to behavioral output. In fact, several studies have already suggested that the neural representations of non-vocalizations (Bieszczad and Weinberger, 2010b, David et al., 2012, Polley et al., 2006) and vocalizations (Gentner and Margoliash, 2003b) depend on the details of a trained behavioral task (e.g. contingencies, rewards, strategy). It is precisely because of the importance of such details in the manifestation of auditory processing that we argue that to truly understand how such processing proceeds in the context of real acoustic communication, we must move toward experimental designs that may capture more of this natural behavioral context (DiMattina and Wang, 2006, Fortune et al., 2011).

To proceed, we first adopt a framework for testing how the neural representation of an acoustic-communication signal is linked in the brain to behavior that could also be used for other sounds that are not used in vocal communication. We make no attempt to ascribe any of the subsequent processing functions to specific brain regions. Instead, we discuss the computational and processing steps that we hypothesize must take place for an animal to use a communication signal to guide behavior (Griffiths and Warren, 2004).

Consider an animal hearing a species-specific vocalization that signals both the presence of food and contains information about the identity of the vocalizer. The first stage of auditory processing is to transduce the vocalization's acoustic energy into a neural signal reflecting the vocalization's spectral and temporal properties. Complex sounds such as vocalizations can be thought of as specific combinations of individual features, like a call's pitch or temporal envelope. The neural representations of such acoustic features are then bound together through sequential and simultaneous grouping principles to form an “auditory object”, which is the fundamental perceptual unit in audition (Griffiths and Warren, 2004, Shamma et al., 2011, Winkler et al., 2009). This representation must then be interpreted in a framework that converts this information into a behavioral judgment (i.e., an auditory decision). Throughout this process, the representation of the vocalization is presumably compared with memory stores to categorize this call and recognize its “meaning”. Once this information has been referenced, it has to be interpreted within the context of an animal's current behavioral goals. Ultimately then, the bottom–up representation of the acoustic signal must be interpreted in the top–down framework of the animal's behavioral and social experiences.

Importantly, these hypothesized steps could relate to any auditory stimulus that has behavioral relevance to the animal (i.e., those that inform an animal's current or future behavior). As outlined above, studying these steps for acoustic communication not only provides a concrete, ethologically relevant context for elucidating functional auditory processing abilities but also adds value to our ability to clarify neural mechanisms. To make this point explicit, we use the remainder of this review to discuss some of these general auditory steps (acoustic-feature encoding and categorization) in more detail and illustrate how ethological approaches have contributed to revealing their underlying mechanisms.