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

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.

Rodent auditory perception: Critical band limitations and plasticity

“…This may include recognition of novel or low-probability sounds, which likely involves adaptive processes such as short-term depression for filtering out behaviorally-irrelevant sensory information (Ulanovsky et al, 2003; 2004; Wehr and Zador, 2005). Mechanisms of longer-term plasticity could be involved in processing the behavioral significance of certain sounds (Froemke and Martins, 2011; Froemke et al, 2013), as indicated by studies in trained animals (Buonomano and Merzenich, 1998) and by examination of pup call representations in virgin female mice compared to dams (Liu et al, 2006; Bennur et al, 2013; Rothschild et al, 2013). …”

Contrast Enhancement without Transient Map Expansion for Species-Specific Vocalizations in Core Auditory Cortex during Learning

“…Indeed, even among nonsocial reinforcers, different receptive field effects are observed when appetitive instead of aversive operant conditioning is used (David et al, 2012). Much remains to be understood about how learning-related neuromodulatory systems are engaged to dynamically (Marlin et al, 2015; McGinley et al, 2015) or more persistently (Kilgard and Merzenich, 1998; Bao et al, 2001; Ji and Suga, 2003) alter AC responses to sounds, but the sensitivity to learning context motivates pursuing ethological paradigms to reveal intrinsic mechanisms of communication sound learning (Bennur et al, 2013). …”

Natural variability in species-specific vocalizations constrains behavior and neural activity

“…In contrast, they did not receive consistent reinforcement when the test vocalization was a non-reference vocalization (C1Cx or G1Gx trials). That is, we wanted the monkeys to “spontaneously” (Bennur et al, 2013; Gifford et al, 2005) report whether the reference and non-reference vocalizations were the same or different. We hypothesized that this approach (Ghazanfar and Santos, 2004) would reveal information that would not be apparent had the monkeys been given consistent reinforcement whenever they reported that specific non-reference vocalizations were the same as or different from the reference vocalization.…”

“…We chose this strategy because we did not want to explicitly train the monkey to report that any particular non-reference vocalization (i.e., a coo Cx or a grunt Gx) was the same as or different from the reference vocalization (i.e., coo C1 or grunt G1). That is, the goal of this portion of the behavioral task was to allow monkeys to “spontaneously” (Bennur et al, 2013; Gifford et al, 2005) report whether the two vocalizations were the same or different.…”

“…In the current study, we quantified the acoustic variability of rhesus vocalizations and simultaneously examined how this variability affected behavioral and neural discriminability (Bennur et al, 2013). Monkeys participated in a task requiring them to discriminate between utterances of vocalizations from the same acoustic class; specifically, coos or grunts .…”