Development of Echolocation Calls and Neural Selectivity for Echolocation Calls in the Pallid Bat Khaleel A. Razak,1 Zoltan M. Fuzessery2 1

Department of Psychology and Graduate Neuroscience Program, University of California, Riverside, California

2

Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming

Received 13 February 2014; revised 27 May 2014; accepted 14 August 2014

ABSTRACT: Studies of birdsongs and neural selectivity for songs have provided important insights into principles of concurrent behavioral and auditory system development. Relatively little is known about mammalian auditory system development in terms of vocalizations or other behaviorally relevant sounds. This review suggests echolocating bats are suitable mammalian model systems to understand development of auditory behaviors. The simplicity of echolocation calls with known behavioral relevance and strong neural selectivity provides a platform to address how natural experience shapes cortical receptive field (RF) mechanisms. We summarize recent studies in the pallid bat that followed development of echolocation calls and cortical processing of such calls. We also discuss similar studies in the mustached bat for comparison. These studies suggest: (1) there are different developmental sensitive periods for different acoustic features of the same vocalization. The underlying

INTRODUCTION The relative contribution of experience-dependent and -independent neural factors to the development Correspondence to: K.A. Razak ([email protected]) Conflict of interest: We have no conflict of interest to report. Contract grant sponsor: National Institutes of Health; contract grant number: DC05202 (Z.M.F.). Contract grant sponsor: NIH; contract grant number: R03 DC009882-01A. Contract grant sponsor: National Science Foundation; contract grant number: IOS 1252769 (K.A.R.). Ó 2014 Wiley Periodicals, Inc. Published online 00 Month 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/dneu.22226

basis is the capacity for some components of the RF to be modified independent of others. Some RF computations and maps involved in call processing are present even before the cochlea is mature and well before use of echolocation in flight. Others develop over a much longer time course. (2) Normal experience is required not just for refinement, but also for maintenance, of response properties that develop in an experience independent manner. (3) Experience utilizes millisecond range changes in timing of inhibitory and excitatory RF components as substrates to shape vocalization selectivity. We suggest that bat species and call diversity provide a unique opportunity to address developmental constraints in the evolution of neural mechanisms of vocalization processing. VC 2014 Wiley Periodicals, Inc. Develop Neurobiol 00: 000–000, 2014

Keywords: development; receptive fields; spectrotemporal processing; auditory cortex; vocalizations

of behavior is an issue of long-standing and fundamental interest. Although there is a rich literature in identifying the experience dependency of single neuron response properties and maps, relatively less is known about how changes in neural responses relate to sensory-perceptual capabilities or behavioral benchmarks (Sanes and Woolley, 2011). An important step in this endeavor is identifying appropriate model systems in which the behavior, relevant sensory signals, neural selectivity for features of these sensory signals and mechanisms shaping such feature selectivity are known in adults. This will facilitate experimental tracking of concurrent changes of these factors during development. 1

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Razak and Fuzessery

The development of species-specific vocalizations has been a major focus in studies of auditory systems to correlate neural processing and behavioral development (Doupe and Kuhl, 1999; Marler, 1997, 2004; Konishi, 2010). For example, it is well established that several brain areas of songbirds contain songselective neurons and the selectivity of these neurons are shaped by sensory and sensorimotor experiences (Doupe et al., 2004; Woolley 2012). Perhaps because of the spectrotemporal complexity of songs, the receptive field (RF) spectrotemporal properties shaping single-neuron song-selectivity are only beginning to be understood (Lewicki, 1996; Theunissen et al., 2000; Rosen and Mooney, 2003, 2006). The mechanisms through which experience shapes song selectivity are also only beginning to be understood (Woolley et al., 2012; Thompson et al., 2013). Considerably less is known about development of neural selectivity for vocalizations in mammalian auditory systems. This is partly due to the complexity of most vocalizations, call repertoire size and the fact that most neurons are selective for a broad range of calls (e.g., Carruthers et al., 2013; Suta et al., 2013). For the most part, developmental studies of mammalian auditory systems have focused on selectivity for simple sounds and tonotopic maps (Zhang et al., 2001; Bao et al., 2003; Chang et al., 2005; de Villers-Sidani et al., 2007). Echolocating bats may be useful mammalian model systems to address the issue of concerted behavioral and central auditory system development of natural sounds. Bats use relatively simple and stereotyped sounds to echolocate (Simmons et al., 1975; Jones and Holderied, 2007; Moss and Surlykke, 2010). Thus, sounds with known behavioral relevance can be used as physiological probes to study neural selectivity, RF spectrotemporal properties and development. Many auditory brain regions contain a preponderance of neurons selective for specific aspects of echolocation calls (Suga and O’Neill, 1979; Suga, 1990; Olsen and Suga, 1991; Wenstrup and Portfors, 2011; K€ossl et al., 2014). Species and call diversity (Jones and Teeling, 2006) can facilitate a comparative analysis of the development of behavior and neural responses. Natural and modified calls can be used to identify call properties used in different aspects of echolocation behavior (e.g., target distance vs. velocity). Such behavioral studies narrow the range of postulated proximate mechanisms thus guiding research on auditory feature detectors (Simmons, 2012). The relative simplicity of calls and the strong selectivity of neurons facilitate a systematic analysis of RF mechanisms that shape selectivity (Razak and Fuzessery, 2006, 2008, 2009; Fuzessery Developmental Neurobiology

et al., 2011; Gittelman et al., 2012; Wenstrup et al., 2012; Razak, 2013). Developmental changes in echolocation systems can be tracked in relation to both call development and behavioral benchmarks (onset of hearing, first flight, weaning) (Brown et al., 1978; Moss et al., 1997; Vater et al., 2003; Monroy et al., 2011) and neural selectivity for calls (Razak and Fuzessery, 2007a; Vater et al., 2010). The major goal of this review is to summarize studies in the pallid bat (Antrozous pallidus, family: Vespertilionidae) regarding the development of echolocation calls and neural selectivity for calls under normal and experience-manipulated conditions (Razak and Fuzessery, 2006, 2007a; Razak et al., 2008). Studies of development of calls and cortical selectivity in mustached bats (Pteronotus parnellii, family: Mormoopidae) are also discussed (Vater et al., 2010; K€ossl et al., 2012). Comparison of development of echolocation systems in these two species from different families of bats suggest early and experience-independent development of computations and maps that shape selectivity for some neural properties that serve echolocation behaviors. Adultlike selectivity for these features is present before cochlear maturation is complete and echolocation is used in flight. Other properties develop over a more prolonged time course in an experience-dependent manner indicating different sensitive periods for different acoustic properties of the same vocalization. As the spectrotemporal properties that shape frequency modulated (FM) rate and direction selectivity are known, it was possible to identify changes in the RF of individual neurons that explain experiencedependent changes in sweep selectivity. In particular, it is clear that millisecond-range changes in the timing of excitatory and inhibitory components of the RF are substrates for experience to shape neural selectivity for vocalizations. Moreover, the spectrotemporal properties of low-frequency sideband inhibition changed independent of the high-frequency sideband, suggesting different RF components can be modified individually. These findings implicate specific cellular mechanisms of experience-dependent cortical development.

DEVELOPMENT OF HEARING AND ECHOLOCATION CALL PROPERTIES IN THE PALLID BAT The pallid bat is a gleaning bat that listens to preygenerated noise to localize and glean terrestrial prey (e.g., crickets, scorpions), while reserving echolocation for obstacle avoidance and general orientation

Development of Vocalization Selectivity

[Fig. 1(A), Bell, 1982; Fuzessery et al., 1993; Barber et al., 2003]. The hearing range of the adult pallid bat covers frequencies between 5 and 80 kHz. For echolocation, pallid bats use downward FM sweeps with frequencies between 30 and 70 kHz, bandwidths between 30 and 40 kHz and durations between 2 and 5 ms [e.g., Fig. 1(D–F)]. The FM sweep rates of the calls are typically 15 kHz/ms. For preylocalization, the pallid bat depends on noise transients with relatively lower frequency energy (5 to 35 kHz). Pallid bats are altricial at birth with no fur or capacity to independently thermoregulate (Davis, 1969). At 4 weeks of age, they begin flying and using echolocation in flight. By 7 weeks, they are fully weaned and likely using passive prey-localization and echolocation. Using evoked responses in the inferior colliculus (IC), Brown et al. (1978) suggested that hearing onset is approximately postnatal day (P)7–P9 [Fig. 1(C)]. At this age, the sensitivity is restricted to low frequencies (

Development of echolocation calls and neural selectivity for echolocation calls in the pallid bat.

Studies of birdsongs and neural selectivity for songs have provided important insights into principles of concurrent behavioral and auditory system de...
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