ReviewMouse vocal communication system: Are ultrasounds learned or innate?
Graphical abstract
Top panel shows mouse song system connectivity, highlighting the presence of a direct projection from M1 cortex to the vocal motor neurons of nucleus ambiguous (Amb). The bottom panel shows pitch imitation between C57 and BxD male mice over the course of 8 weeks of co-housing in the presence of a female of either strain (conditions 1 and 2).
Highlights
► Mice have forebrain circuits active during singing. ► Mice have a direct motor cortical projection to vocal motor neurons. ► Mice make changes in vocalizations over early development that can not be explained by innate behavior alone. ► Mice have a partial dependence on auditory feedback to maintain acoustic features of their songs, but this is under debate. ► Mice can copy the pitch of another strain’s song as adults.
Introduction
Laboratory mice (Mus musculus) and rats (Rattus norvegicus) participate in a significant amount of communication using ultrasonic vocalizations (USVs) produced at frequencies ranging from 30 to 110 kHz (Constantini and D’Amato, 2006, Portfors, 2007). Traditionally, two types of USVs have been studied in laboratory rodents as measures of internal states: pup isolation calls (Branchi et al., 2001, Brudzynski et al., 1999, D’Amato et al., 2005, Elwood and Keeling, 1982, Hahn et al., 1987, Hofer and Shair, 1992, Ise and Ohta, 2009, Noirot and Pye, 1969, Sales and Smith, 1978, Wöhr, Dalhoff, et al., 2008) and adult USVs in aversive or rewarding conditions (Brudzynski, 2007, Brudzynski, 2009, Burgdorf et al., 2007, Knutson et al., 2002, Wöhr, Houx, et al., 2008). Reliable elicitation of isolation calls by quantifiable stimuli and a well characterized developmental trajectory have made pup USVs a useful tool for testing the effects of anxiogenic or anxiolytic compounds (Dirks et al., 2002, Fish et al., 2004, Fish et al., 2000) and for phenotyping mouse models of neuropsychiatric disorders associated with deficits in vocal communication (Scattoni, Crawley, & Ricceri, 2009).
Adult mouse USVs appear to both signal internal emotional states and facilitate social communication during non-aggressive encounters (Gourbal et al., 2004, Moles et al., 2007, Portfors, 2007). The most well characterized adult mouse USVs are those produced by males in a mating context. Males of many strains produce long bouts of USVs during courtship of a female and after copulation (Constantini and D’Amato, 2006, Gourbal et al., 2004, Nyby, 1983, Portfors, 2007). Male courtship USVs are sexually selective, and pheromones present in female urine are a strong and sufficient trigger (Guo & Holy, 2007). In two-choice experiments females responded with approach behavior preferentially to adult male USVs over pup isolation calls (Hammerschmidt et al., 2009, Musolf et al., 2010), and spent more time with vocalizing males (Pomerantz, Nunez, & Bean, 1983).
Although the general occurrence of male mouse USVs has been known for decades, the spectro-temporal and syntactic features of male courtship USVs were only recently analyzed in depth. Holy and Guo showed that courtship USVs from males contain identifiable syllable types produced in regular temporal patterns that differed between individuals (Holy & Guo, 2005). Moreover, the long strings of syllables they recorded sounded remarkably similar to some bird songs when the pitch of the USVs was shifted to the human audible frequency range and played in real time (Supplementary Audio 1). After observing the complexity of mouse USVs, individual differences, and their similarity to some birdsongs, many researchers wondered what is the neural substrate for USV production, whether mice might share central control mechanisms for vocalization with vocal learning species like songbirds and humans, and whether mouse vocalizations are innate or learned.
The generally accepted list of vocal learning species includes three lineages of birds (songbirds, parrots, hummingbirds) and up to four lineages of mammals (humans, cetaceans [dolphins and whales], bats, elephants, and pinnipeds [sea lions and seals]) (Janik and Slater, 1997, Jarvis, 2004, Schusterman, 2008, Schusterman and Reichmuth, 2008). This vocal learning ability, which includes the ability to modify the spectral and syntactic composition of vocalizations, is a rare trait that serves as a critical substrate for human speech (Doupe and Kuhl, 1999, Jarvis, 2004, Marler, 1970a). It has been well studied in humans and songbirds because songbirds display a capacity for vocal mimicry using a process similar to human speech acquisition (Doupe and Kuhl, 1999, Marler, 1970a) and some species are easy to breed and study in the laboratory. Underlying the vocal learning process in both humans and song learning birds are specialized forebrain circuits so far not found in species that produce only innate vocalizations, despite decades of searching for them (Jarvis, 2004, Jürgens, 2009). Even closely related non-human primate species reportedly lack the behavioral and neural elements classically associated with a capacity for vocal learning (Hammerschmidt et al., 2001, Janik and Slater, 1997, Jürgens, 2009). Like non-human primates, mice have been assumed to be vocal non-learners (Enard et al., 2009, Fischer and Hammerschmidt, 2010, Jarvis, 2004), but this had not been tested. Here we discuss the concepts of innate versus learned vocal communication, give an overview of the neural pathways involved, critically review recent studies that have approached the issue of vocal plasticity mice (Arriaga et al., 2012, Chabout et al., 2012, Grimsley et al., 2011, Hammerschmidt et al., 2012, Kikusui et al., 2011), address some conflicting views, and propose avenues for reconciliation. The views we propose will be relevant to all studies on innate and learned vocal communication in vertebrates.
Section snippets
Vocalizations and the vocal organ
Many animals communicate by broadcasting species-typical acoustic signals including insects, frogs, birds, and mammals. However, not all of these sounds are classically defined vocalizations, which are produced by a vocal organ. The vocal organ in birds is the syrinx, and it is the larynx in frogs and most mammals. Dolphins, a marine mammal, are believed to vocalize using specialized nasal sacs in addition to the larynx (Madsen, Jensen, Carder, & Ridgway, 2012). Gross laryngeal anatomy is well
Brain pathways for vocal communication
It has been proposed that two different, but converging pathways are involved in the production of learned and innate vocalizations (Jarvis, 2004, Jürgens, 2009, Simonyan and Horwitz, 2011, Wild, 1994, Wild, 1997). According to this division of labor, innate calls are programmed by a phylogenetically older brainstem pathway, and the forebrain influences the context (i.e. usage) of calling but not acoustic structure. In contrast, control of the spectral content of learned calls would be given
Innate and learned features of mouse vocalizations
Like input from motor cortex, auditory experience seems to be more important for the production of learned vocalizations than innate calls. In humans and songbirds auditory experience plays a critical role at multiple stages in the ontogeny of vocal behavior: (1) a sensory phase during which an auditory memory or ‘template’ is formed following exposure to an appropriate model; (2) a sensorimotor phase during which vocal output is monitored and compared to the model in a guided learning process;
Conclusions and future directions
This perspective report has examined the underlying neural circuits that support production of ultrasonic courtship songs of male laboratory mice, and described some basic capabilities of adult mice to modify and maintain the spectral content of their songs. Some of the currently available data indicate that a combination of neural and behavioral features is present in laboratory mice that had previously only been reported in humans and song learning birds. Some of these findings are being
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