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10

Shared Developmental and Evolutionary Origins for Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling

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ANDREW H. BASS* AND BORIS P. CHAGNAUD

Acoustic signaling behaviors are widespread among bony vertebrates, which include the majority of living fishes and tetrapods. Developmental studies in sound-producing fishes and tetrapods indicate that central pattern-generating networks dedicated to vocalization originate from the same caudal hindbrain rhombomere (rh) 8-spinal compartment. Together, the evidence suggests that vocalization and its morphophysiological basis, including mechanisms of vocal–respiratory coupling that are widespread among tetrapods, are ancestral characters for bony vertebrates. Premotor-motor circuitry for pectoral appendages that function in locomotion and acoustic signaling develops in the same rh8-spinal compartment. Hence, vocal and pectoral phenotypes in fishes share both developmental origins and roles in acoustic communication. These findings lead to the proposal that the coupling of more highly derived vocal and pectoral mechanisms among tetrapods, including those adapted for nonvocal acoustic and gestural signaling, originated in fishes. Comparative studies further show that rh8 premotor populations have distinct neurophysiological properties coding for equally distinct behavioral attributes such as call duration. We conclude that neural network innovations in the spatiotemporal patterning of vocal and pectoral mechanisms of social communication, including forelimb gestural signaling, have their evolutionary origins in the caudal hindbrain of fishes.

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*Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853; and Department of Biology II, Ludwig-Maximilians-University Munich, 82152 Martinsried, Germany. To whom correspondence should be addressed. E-mail: ahb3@cornell.edu.



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10 Shared Developmental and Evolutionary Origins for Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling ANDREW H. BASS*‡ AND BORIS P. CHAGNAUD† Acoustic signaling behaviors are widespread among bony vertebrates, which include the majority of living fishes and tetrapods. Developmental studies in sound-producing fishes and tetrapods indicate that central pattern-generating networks dedicated to vocalization originate from the same caudal hindbrain rhombomere (rh) 8-spinal compartment. Together, the evidence suggests that vocalization and its morphophysi- ological basis, including mechanisms of vocal–respiratory coupling that are widespread among tetrapods, are ancestral characters for bony ver- tebrates. Premotor-motor circuitry for pectoral appendages that function in locomotion and acoustic signaling develops in the same rh8-spinal compartment. Hence, vocal and pectoral phenotypes in fishes share both developmental origins and roles in acoustic communication. These find- ings lead to the proposal that the coupling of more highly derived vocal and pectoral mechanisms among tetrapods, including those adapted for nonvocal acoustic and gestural signaling, originated in fishes. Compara- tive studies further show that rh8 premotor populations have distinct neurophysiological properties coding for equally distinct behavioral attri- butes such as call duration. We conclude that neural network innovations in the spatiotemporal patterning of vocal and pectoral mechanisms of social communication, including forelimb gestural signaling, have their evolutionary origins in the caudal hindbrain of fishes. *Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853; and †Department of Biology II, Ludwig-Maximilians-University Munich, 82152 Martinsried, Germany. ‡To whom correspondence should be addressed. E-mail: ahb3@cornell.edu. 175

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176  /  Andrew H. Bass and Boris P. Chagnaud E arly hindbrain development in all major vertebrate lineages exhibits a shared anatomical blueprint of cranial motor nuclei and nerves originating in one or more serially arranged segments or rhombo- meres [rhs; e.g., Lumsden and Keynes (1989), Gilland and Baker (2005)]. Here, we consider the development and evolution of hindbrain circuitry leading to novel innovations in social signaling, integrating information across behavioral, neurophysiological, and morphological levels of analy- sis. Two neural networks are the focus: the sonic–vocal basis of acoustic signaling (Fig. 10.1A) and pectoral control of anterior appendages, fins, and forelimbs (Fig. 10.1B). For context, we first briefly review vertebrate phylogeny and the ancestral “blueprint” for hindbrain motor phenotypes. VERTEBRATE PHYLOGENY Living craniates include jawless vertebrates or agnathans and jawed vertebrates or gnathostomes [Fig. 10.1B; reviewed in Nelson (2006)]. Fossil evidence indicates several lineages of extinct agnathans [e.g., Osteostra- cans; Fig. 10.1B; e.g., Forey and Janvier (1993)]. Chondrichthyes (i.e., carti- laginous fishes) are the most basal group of jawed vertebrates and include two subclasses, Elasmobranchii (i.e., sharks, skates, and rays) and Holo- cephali or chimaeras. Bony vertebrates, the sister group to Chondrich- thyes, include Actinopterygii or rayfinned fishes and the Sarcopterygii or lobe-finned fishes. Sarcopterygians include the coelacanth (Latimeria), lungfish (Dipnoi), and tetrapods. Here, we mainly review recent evidence showing that a caudal hindbrain (rh8)-spinal cord compartment is the developmental origin of p ­ remotor-motor circuitry for sonic–vocal and pectoral behavioral pheno- types. Actinopterygians, which include nearly half of living vertebrate species, were the focus of these studies. By integrating these new findings into a single framework, we aim to achieve a more complete understand- ing of the evolutionary origins of vocal and pectoral motor systems among vertebrates in general, including the more highly derived pectoral systems of tetrapods that serve a range of functions including nonvocal sonic and forelimb gestural signaling. HINDBRAIN SEGMENTAL BLUEPRINT Vertebrates have two functional series of hindbrain motor nuclei, somatic and branchiomeric (Lumsden and Keynes, 1989; Gilland and Baker, 2005), that were likely present in the earliest, pregnathostome ver- tebrates (Northcutt, 1985). Somatic nuclei innervate head muscle derived from unsegmented (i.e., prechordal plate) and segmented paraxial meso- derm (i.e., occipital somites); branchiomeric nuclei target derivatives of

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  177 FIGURE 10.1  Evolution of vocal–pectoral motor systems in fishes and tetrapods. (A) Waveforms of representative social vocalizations of bullfrog (time base 1 s), zebra finch (250 ms), squirrel monkey (200 ms), midshipman fish (500 ms), catfish (250 ms), and club-winged manakin (100 ms). Vocal (v) and nonvocal pectoral (p) basis is indicated. (B) Cladogram of vertebrates, including jawless (agnatha) and jawed (gnathostome) radiations (Osteostracans represent an extinct agnathan group with pectoral fins). (C) Summary of location of vocal and sonic motor neu- rons. Among fishes, the occipitospinal motor column (black) gives rise to motor neurons innervating muscles of vocal organs dedicated to sonic functions (e.g., swim bladder) and pectoral fins that can also serve a sonic function. This same column gives rise to vocal motor neurons in tetrapods. Among tetrapods, forelimb motor neurons (orange) that function in both sonic and gestural signaling are lo- cated in the spinal cord. [A adapted from Bass et al. (2008); B and C adapted from Ma et al. (2010).] [Note: Figure can be viewed in color in the PDF version of this volume on the National Academies Press website, www.nap.edu.] paraxial mesoderm that migrate into the pharyngeal arches (Nieuwen- huys et al., 1998; Gilland and Baker, 2005; Noden and Francis-West, 2006). Comparative studies delineate a conserved pattern of hindbrain somatic and branchiomeric motor nuclei spatially segregated along the rostral–

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178  /  Andrew H. Bass and Boris P. Chagnaud caudal axis across eight rhs (Murakami et al., 2004; Gilland and Baker, 2005). Most nuclei originate in one or two rhs with little variation in extent or location across taxa (Gilland and Baker, 2005). Of particular interest for this review is rh8, which has two to three times the longitudinal extent of more anterior segments and can be subdivided into at least two to three subdivisions in teleost fishes and birds (Hanneman et al., 1988; Cambro- nero and Puelles, 2000; Bass et al., 2008). Additional evidence for hindbrain segmentation, including a distinct rh8-spinal boundary, comes from rh- specific patterns of gene expression [e.g., Prince et al. (1998), Tümpel et al. (2009), Ma et al. (2010)]. EVOLUTIONARY DEVELOPMENTAL “HOTSPOTS” FOR NOVEL PATTERN GENERATORS Caudal hindbrain rhs are a developmental and evolutionary “hotspot” [sensu Myers et al. (2000)] for innovations in neural networks controlling complex motor function. Bass and Baker (1997) hypothesized that the appearance of novel respiratory and cardiovascular pumps during the protochordate–vertebrate transition (Gans and Northcutt, 1983; Northcutt and Gans, 1983) depended upon the evolution of equally novel, genetically specified pattern-generating circuits developing in rhs 7 and 8. Rhombo- meres 7 and 8 were also proposed as the source of more recently derived premotor-motor networks unique to jawed vertebrates, such as those controlling sound production, that have social signaling functions (Bass and Baker, 1997). The development of precerebellar climbing fibers from a distinct rh8 nucleus, the inferior olive (Cambronero and Puelles, 2000), underscored a preeminent role for caudal hindbrain nuclei in the spatio- temporal patterning of complex motor behaviors such as vocalization and eye movement. SONIC–VOCAL PATTERN GENERATOR Sonic motor systems in fishes provide excellent models for directly linking neural mechanisms to behavioral outcomes, in part, because the physical attributes of acoustic signals (e.g., interpulse and intercall inter- vals, duration, amplitude), like their underlying neural activity, are easily quantified (Bradbury and Vehrencamp, 2011). Sonic mechanisms vary within and between fish lineages (Fine and Ladich, 2003; Ladich and Fine, 2006; Bass and Ladich, 2008). Although most species studied so far gener- ate acoustic signals by vibrating the swim bladder, a second well-known set of mechanisms depends on pectoral appendage vibration (Kratochvil, 1978; Bass and Baker, 1991; Fine et al., 1997). Neuronal patterning of sound production has been most extensively investigated in species using a sonic

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  179 swim bladder; hence, we first discuss these species. We will then turn our attention to pectoral-dependent mechanisms in the broader context of the motor control of pectoral appendages. Swim bladder vibration is driven by the contraction of a single pair of muscles attached directly or indirectly to the swim bladder. This bio- mechanical simplicity has provided a unique opportunity to show how acoustic characters are directly determined by the intrinsic and network properties of a hindbrain central pattern generator controlling one pair of muscles. Toadfishes, a single order and family (Batrachoidiformes, Batra- choididae) of teleost fishes commonly known as toadfish and midshipman fish, have been widely studied as neurobehavioral models for acoustic communication (Bass and McKibben, 2003; Bass and Remage-Healey, 2008; Greenfield et al., 2008). Among toadfishes, sonic muscles directly attached to the swim bladder are innervated by paired occipital nerve roots exiting the caudal hindbrain (Ladich and Fine, 2006; Bass and Ladich, 2008). The temporal properties of occipital nerve motor volleys directly set pulse repetition rate (equivalent to fundamental frequency of harmonic calls for fish), duration, and complex patterns of frequency and amplitude modulation of entire calls (Bass and Baker, 1990; Remage-Healey and Bass, 2004, 2006; Rubow and Bass, 2009). Individual sound pulses are matched 1:1 with each spike-like, occipital nerve potential (Fig. 10.2A and B) that results from the synchronous activity of an expansive vocal motor nucleus (VMN) extending from the caudal hindbrain into the rostral spinal cord (Fig. 10.2C and D) (Bass and Baker, 1990). Paired midline VMNs fire in synchrony (Bass and Baker, 1990), with bilaterally synchronous occipital spikes leading to simultaneous contraction of both vocal muscles and one sound pulse (Cohen and Winn, 1967). A descending vocal motor pathway in toadfishes extends from fore- brain preoptic-anterior hypothalamic to midbrain and caudal hindbrain levels (Bass et al., 1994; Goodson and Bass, 2002; Kittelberger et al., 2006). Premotor vocal pacemaker neurons (VPNs) densely innervate VMNs and receive input from a more rostral, anatomically separate prepacemaker [vocal prepacemaker (VPP)] nucleus (Fig. 10.2C and D) (Bass and Baker, 1990; Bass et al., 1994; Chagnaud et al., 2011). In an in vivo preparation, surgical isolation of the hindbrain-spinal region including the VPP–VPN– VMN network shows this region alone can produce a patterned output matching call temporal properties (Remage-Healey and Bass, 2004, 2006). Investigations of a toadfish known as midshipman, using in vivo intra- cellular recording and staining, show how the VPP–VPN–VMN network determines natural vocal attributes. Chagnaud et al. (2011, 2012) demon- strate that precise temporal patterning of natural vocalization (Fig. 10.2A and B) depends on extreme networkwide synchrony and distinct intrinsic properties for each vocal nucleus. Sustained depolarizations in VPP, sub-

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180  /  Andrew H. Bass and Boris P. Chagnaud FIGURE 10.2  Vocal behavior and neural network of plainfin midshipman fish. (A) Oscillogram record of repetitive series of natural calls (“grunt train”) recorded with hydrophone; lower trace shows one call. (B) Spontaneous vocal motor volley recorded from vocal occipital nerve (VOC) with temporal properties like those of natural vocalization; lower trace shows one VOC. VOC duration is time between first and last pulses; frequency is pulse repetition rate. (C) Vocal motor nuclei superimposed on lateral view of intact brain. Indicated are VPN, VPP, and VMN nuclei and vocal nerve (VN). Vocal midbrain (VMB) and forebrain preoptic area (POA) are vocally active sites. (D) Premotor compartmentaliza- tion of neurons code for distinct acoustic attributes. Representative intracellular records from vocal nuclei and vocal nerve superimposed on background sagittal image of caudal hindbrain. Descending input from vocal midbrain/forebrain neurons activates vocal hindbrain. Vocal prepacemaker nucleus is source of known corollary discharge informing auditory nuclei about a vocalization’s temporal properties. [Adapted from Chagnaud et al. (2011).] [Note: Figure can be viewed in color in the PDF version of this volume on the National Academies Press website, www.nap.edu.]

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  181 threshold membrane oscillations in VPN, and a combination of differential recruitment and low excitability in VMN directly code natural call dura- tion, frequency, and amplitude, respectively (Chagnaud et al., 2011, 2012) (Fig. 10.2D). In addition to coding duration, prepacemaker neurons are the source of input to a rostral hindbrain nucleus directly innervating the inner ear and lateral line organs that is the anatomical basis for a vocal corollary discharge (Fig. 10.2D) (Weeg et al., 2005). These new results for fishes, together with nerve recordings and more limited single-neuron recordings in tetrapods, led to the proposal that anatomically separate hindbrain populations code distinct call attributes in fishes and tetrapods (Chagnaud et al., 2011). Among tetrapods, the coupling of sound production and respiration leads to airflow-dependent vibration of sonic laryngeal and syringeal mem- branes [e.g., Gans (1973), Gans and Maderson (1973), Bradbury and Vehren- camp (2011)]. Despite the close connection between vocal and respiratory pattern generators in tetrapods, evidence for a vocal–respiratory pattern generator in more basal vertebrates such as fishes has been missing. Video and sound analysis of advertisement calling (“humming”) by midshipman fish (Brantley and Bass, 1994) reveals a strong rhythmic correlation between vocal, respiratory, and postural (i.e., pectoral) systems. Vocal–respiratory coupling in this case likely reflects the increased oxygen demands of repeti- tive muscle contractions during the unusually long duration (from minutes to 1 h) hum vocalizations. Pectoral fin motion may stabilize the body during prolonged calling and/or aid in the increased movement of oxygenated water across the gills during humming [e.g., Peterson (1975)]. We propose that vocal–respiratory coupling originated in fishes and was subsequently adopted by tetrapods. Neurophysiological support for this hypothesis comes from studies of the vocal pattern generator in fully aquatic frogs that produce sound independent of airflow and yet exhibit vocal–respiratory coupling in the caudal hindbrain (Zornik and Kelley, 2007). In birds and mammals, nuclei integrating vocal (i.e., laryngeal and syringeal) and respiratory activity are also positioned in the caudal hindbrain, adjacent to vocal motor neurons (Holstege, 1989; Zhang et al., 1995; Wild et al., 2009; Schmidt et al., 2012). Although a vocal–respiratory integration site has yet to be identified in fishes, it will likely be in the caudal hindbrain as in tetrapods. EVOLUTIONARY DEVELOPMENT OF SONIC–VOCAL PATTERN GENERATOR We originally adopted the term “vocal” to describe occipital-innervated sonic systems in fishes, like the toadfishes discussed earlier, because of multiple characters they share with tetrapods (Bass et al., 1994): (i) pro-

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182  /  Andrew H. Bass and Boris P. Chagnaud duction of social context-dependent signals, for example, agonistic vs. advertisement; (ii) dedication of muscles, like those of the tetrapod syrinx and larynx, to sound production; (iii) shared origins of sonic muscles in fishes and tetrapods from occipital somites; (iv) likely homology of occipi- tal nerve roots innervating fish sonic muscles and hypoglossal nerve roots innervating avian syringeal muscles; and (v) the same location in caudal hindbrain of fish sonic motor nucleus and avian tracheosyringeal division of hypoglossal motor nucleus innervating syringeal muscles (Nottebohm et al., 1976). Developmental studies in fishes now support the hypothesis that hindbrain pattern generators for vocalization in the two main clades of bony vertebrates, Actinopterygii and Sarcopterygii (Fig. 10.1B), share developmental and evolutionary origins. Fluorescent dextran-amine injec- tions into the developing vocal muscle of newly hatched midshipman and toadfish larvae showed a cigar-shaped VMN extending from caudal rh8 into the rostral spinal cord, a longitudinal extent more than twice that of the more anterior rhs 2 to 6 (Fig. 10.3A). Experimental mapping of VMN relative to highly conserved neuronal landmarks in vertebrates showed, for example, rostral VMN coincident with the caudal pole of the vagal motor column and the caudal pole of the precerebellar inferior olive, both of which originate from rh8 in tetrapods (Cambronero and Puelles, 2000). Transneuronal neurobiotin labeling in larvae also showed vocal premotor neurons positioned in caudal rh8 immediately lateral and rostral to VMN (Fig. 10.3B and C), matching the locations of VPN and VPP, respectively, in adults (e.g., Fig. 10.3D) (Bass et al., 2008). Taxonomic analysis, based on developing and adult hindbrain orga- nization, next showed vocal premotor-motor circuitry (including sites of vocal–respiratory coupling, as detailed earlier) in amphibians, birds, and mammals mapping to the same rh8-spinal compartment as the develop- ing VPP–VPN–VMN network of fish [reviewed in Bass et al. (2008); also see Nottebohm et al. (1976), Holstege (1989), Zhang et al. (1995), Straka et al. (2006), Jürgens and Hage (2007), Zornik and Kelley (2007), Wild et al. (2009), Schmidt et al. (2012); Fig. 10.3E). Together, the evidence led to the proposal that an rh8-spinal compartment is the developmental and evolutionary origin of hindbrain vocal pattern-generating circuitry among all the major lineages of vocal vertebrates. SHARED ORIGINS OF SONIC–VOCAL MUSCULATURE AND CENTRAL MECHANISMS Peripheral sonic mechanisms vary between and even within fish lin- eages (Fine and Ladich, 2003; Ladich and Fine, 2006; Bass and Ladich, 2008; Parmentier et al., 2011). For example, sculpin (Scorpaeniformes,

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  183 FIGURE 10.3  Map of developing vocal pattern generator in rh8-spinal compart- ment. (A) Fluorescently labeled neurons in plainfin midshipman fish larvae visu- alized with laser scanning confocal microscopy (horizontal plane). Simultaneous visualization of reticulospinal neurons labeled via retrograde transport from the spinal cord (Alexa 546 dextran-amine, red) and VMN (Alexa 488 dextran-amine, green) labeled via the developing vocal muscle. Yellow is composite overlap and does not indicate double labeling. Inset: Clusters of reticulospinal neurons (Alexa biocytin 488, green) in each rh, from 1 to 8. (Scale bars: 0.2 mm.) (B and C) Mapping in horizontal plane of VPP, VPN, and VMN neurons (black) in Gulf toadfish larvae; labeling via transneuronal transport of neurobiotin from devel- oping vocal muscle. Cresyl violet counterstain reveals segmental, reticulospinal clusters. (Scale bar: 0.2 mm.) (D) Transverse section in caudal hindbrain of toadfish showing transneuronal neurobiotin labeling (brown) of paired midline VMN and adjacent VPNs; VMNs and VPNs have extensive dendritic and axonal branching. VMN axons exit via occipital vocal nerve root (OVN; cresyl violet counterstain). (Scale bar: 100 μm.) (E) Sagittal view summarizing relative positions of hindbrain vocal premotor-motor networks in rh8-spinal compartment of fish, birds, frogs, and mammals including primates, based on early-stage and adult phenotypes [see Bass et al. (2008) for details]. Most laryngeal motor neurons that shape the temporal envelope of mammalian calls originate from caudal nucleus ambiguus (Amb). Drt, dorsal reticular nucleus; PAm, nucleus parambigualis; RAb, nucleus retroambiguus; RAm, nucleus retroambigualis; Ri, inferior reticular formation; XIIts, tracheosyringeal division of hypoglossal motor nucleus; XMNc, caudal XMN. [Adapted from Bass et al. (2008).] [Note: Figure can be viewed in color in the PDF version of this volume on the National Academies Press website, www. nap.edu.]

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184  /  Andrew H. Bass and Boris P. Chagnaud Cottidae) lack a swim bladder and instead vibrate a single pair of muscles attached to the pectoral girdle (Bass and Baker, 1991). Closely related sea robins (Scorpaeniformes, Triglidae), like distantly related midshipman and other toadfishes, have a pair of vocal muscles that are completely attached to the swim bladder (Bass and Baker, 1991). Important to the current discussion is that sound-generating muscles in sculpin and sea robins, like toadfishes and other families of sonic fishes, are innervated by occipital nerve roots (Bass and Baker, 1991). This suggests that vocal muscles among fishes share developmental origins from occipital somites (Tracy, 1959, 1961), irrespective of skeletal mechanics and degree of taxo- nomic relatedness. Occipital innervation of vocal muscles originating from a VMN at the same hindbrain (rh8)-spinal level is now documented for nine families of closely and distantly related teleost taxa (Bass and Baker, 1991; Ladich and Bass, 2005; Onuki and Somiya, 2007; Bass and Ladich, 2008). Piranhas (Characiformes) are an exception to the pattern, with spinal-only innerva- tion and a spinal-positioned VMN [Ladich and Bass (2005), Onuki and Somiya (2007); Onuki and Somiya (2007) describe other likely examples]. However, brain stimulation indicates vocal premotor, pattern-generating circuitry in piranhas in the same caudal hindbrain region as the VPP–VPN circuit in toadfishes (Kastberger, 1981). Like the sonic organs of fishes, the nonavian larynx and avian syrinx have lineage-specific skeletal characters [e.g., Bradbury and Vehrencamp (2011)], but share vocal muscle origins from occipital somites [see Huang et al. (1999) and Noden and Francis-West (2006) for tetrapods]. Laryngeal and syringeal premotor-motor networks are also located in the same rh8- spinal compartment as the vocal network in fishes (Fig. 10.3E). Hence, vocal premotor-motor circuitry, like vocal muscles, shares developmental and evolutionary origins among vertebrates. Studies of frogs further show that laryngeal nerve output resembles occipital nerve activity in fishes. Like the occipital motor volley in vocal fish, the laryngeal motor volley of frogs matches the temporal properties of natural calls (Schmidt, 1992; Yamaguchi and Kelley, 2000). These findings, together with those dis- cussed earlier for piranhas, direct our attention to the conserved nature of vocal premotor mechanisms, regardless of motor neuron targets [also see Zornik et al. (2010)]. Among fishes, acoustic communication is widespread and best known for the highly speciose teleosts [e.g., Ladich et al. (2006), Malavasi et al. (2008), Lobel et al. (2010), Parmentier et al. (2011)]. There is also well- documented behavioral evidence for acoustic signaling in more basal actinopterygians [see Nelson (2006) for phylogeny] including sturgeon (Acipenseriformes) (Johnston and Phillips, 2003), bichir (Polypteriformes) (Ladich and Tadler, 1988), and bowfin (Amiiformes) (Fülleborn, 1894).

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  185 Among basal sarcopterygians, sound production (“grunting”) is noted for lungfish (Dipnoi) (Günther, 1870; Thomson, 1968). A critical test of the hypothesis that occipital somite-derived vocal muscle and rh8/occipital- spinal-derived vocal networks are ancestral characters for both major clades of bony vertebrates awaits the demonstration of these characters in one of the more basal (i.e., nonteleost) actinopterygians and a basal sarcopterygian (i.e., nontetrapod). If evidence from one of these more basal groups does not support the hypothesis, we would conclude that the observed vocal characters have independently evolved among acti- nopterygian and sarcopterygian lineages. EVOLUTIONARY DEVELOPMENT OF PECTORAL APPENDAGE CIRCUITRY Developmental mapping of the VMN in toadfishes relative to other hindbrain landmarks showed VMN coextensive with the rostral pole of a pectoral motor nucleus (Cambronero and Puelles, 2000). This finding led to the suggestion that the rh8-spinal compartment may be the source of neuronal innovations in the central patterning of nonvocal, pectoral- dependent function such as forelimb movement (Cambronero and Puelles, 2000). Since that time, a pectoral motor nucleus in basal and derived groups of bony vertebrates has been shown conclusively to develop in the same rh8-spinal compartment as the vocal system. By using multiple neuronal markers and alignment of the neuroepithelium with myotomes during the pectoral fin bud stage, Ma et al. (2010) precisely mapped the entire extent of the pectoral column along with the cranial-vertebral and rh8-spinal boundaries in representative species from three orders of teleosts used extensively as neurobehavioral models: midshipman (­ atrachoidiformes), B salmon (Salmoniformes), and zebrafish (Cypriniformes). The results for teleosts were compared with those for paddlefish (Acipenseriformes), a more basal order of actinopterygians (Fig. 10.4A–C). Pectoral muscles were innervated by paired occipital (Oc1, Oc2) and anterior spinal (Sp1, Sp2) nerves (Fig. 10.4C, Left). Pectoral motor neurons, identified following retrograde transport of fluorescent dye from fin buds, were concurrently mapped with other neuronal landmarks including (i) foramina where occipital nerve roots exit the embryonic skull, (ii) genetic markers (hoxb4 expression) for rh8-spinal boundary (Ma et al., 2009), (iii) nonpectoral motor nuclei including an islet1-GFP line labeling cranial motor nuclei (Higashijima et al., 2000), and (iv) cerebellar input from the rh8-derived inferior olive nucleus (Cambronero and Puelles, 2000). Pectoral motor neurons extended between myotomes 2–3 and 5–6, with axons exiting via paired occipital roots (Oc1, Oc2) through a single fora- men rostral to the cranial-vertebral boundary; axons also exited via the

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186  /  Andrew H. Bass and Boris P. Chagnaud FIGURE 10.4 Map of developing pectoral motor nucleus in rh8-spinal compart- ment of basal and derived groups of actinopterygian fish (A and B, dorsal views). (A) Craniovertebral junction (asterisk) in postlarval, juvenile midshipman fish cleared and stained with alcian blue and alizarin red. (B) Demarcation of rh8- spinal boundary (yellow hatching) in zebrafish hoxb4a enhancer trap line. (C) Alignment of myotomes (“M”), occipital (Oc1, Oc2), and spinal (Sp1, Sp2) nerves and pectoral (red) and occipital (gray) motor neurons. Phylogeny of study spe- cies is also shown (Right). [Adapted from Ma et al. (2010).] [Note: Figure can be viewed in color in the PDF version of this volume on the National Academies Press website, www.nap.edu.] first one or two spinal roots (Sp1, Sp2) (Ma et al., 2010) (Oc1 and Oc2 also innervate vocal muscles; Fig. 10.4C, Left). Given the genetic mapping of cranial-vertebral (Fig. 10.4A) (Morin-Kensicki et al., 2002) and hindbrain- spinal (Ma et al., 2009) (Fig. 10.4B) boundaries between myotomes 3 and 4, the results demonstrated an rh8/occipital-spinal column innervating pectoral muscles in basal and derived actinopterygian species. To extend the conclusions more broadly, the actinopterygian innerva- tion pattern was compared with that of more basal cartilaginous fishes (Chondrichthyes, Chimaeriformes/ratfish), and representative fish spe- cies in the other major clade of bony vertebrates, Sarcopterygii (Dipnoi, lungfish), that includes tetrapods (Fig. 10.1B). Together with published accounts for a more basal sarcopterygian, the coelacanth (Latimeria) (Northcutt and Bemis, 1993; Millot and Anthony, 1965) (Fig. 10.1B), the results showed that occipital and spinal nerve innervation of pectoral muscles was a consistent character across all the investigated lineages of vertebrates. In sum, precise mapping in pre- and postlarval stages of development showed that the ancestral pattern for pectoral appendage innervation

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  187 in bony vertebrates is from the rh8/occipital-spinal compartment (Fig. 10.1C). Pectoral fins, considered more ancient than pelvic fins (Coates, 2003), were previously assumed to receive innervation only from the spinal cord, like the pectoral forelimbs of tetrapods [reviewed in Ma et al. (2010)]. However, the new results in fishes indicate that spinal-only pectoral innervation is a shared derived character (i.e., synapomorphy), along with decoupling of pectoral appendages from the skull and evolu- tion of a neck (Daeschler et al., 2006), only for tetrapod forelimbs (Fig. 10.1C). Despite the change in motor neuron location, premotor pectoral circuitry may be present in the caudal hindbrain of tetrapods, as it is in fishes (Auerbach and Bennett, 1969; Koyama et al., 2011). Although direct evidence is lacking, brain stimulation suggests that caudal hindbrain cir- cuits configure pectoral/forelimb motor neuron activity in mammals [e.g., Drew et al. (1986)]; single neuron recordings like those in fishes (Auerbach and Bennett, 1969; Koyama et al., 2011) are needed to more rigorously test this hypothesis. SHARED ORIGINS OF VOCAL AND PECTORAL CIRCUITRY Additional evidence from the studies reviewed here of pectoral motor development suggests that each functional segment of a myotome (e.g., vocal or pectoral) has an rh8/occipitospinal complement. Fluorescent dye labeling of occipital myotomes in midshipman, salmon, and zebrafish embryos showed an occipital motor column, inclusive of pectoral motor neurons, extending approximately one myotome anterior to the rostral pole of the pectoral column with axons exiting via Oc1 and Oc2 (Fig. 10.4C, Left). As vocal muscle develops from myotome 2 (Tracy, 1959, 1961), this more complete labeling of the developing occipital motor column would also include the vocal motor complement. Vocal motor neurons likely come from a vocal “segment” of the occipitospinal column, separate from a pectoral segment innervating pectoral muscle that is also derived, in part, from myotome 2 (Tracy, 1959, 1961). Together, the results indicate that vocal and pectoral motor systems in fishes share developmental origins from the rh8/occipitospinal compartment. As discussed later, this would also include pectoral-dependent mechanisms of acoustic signaling. Sonic mechanisms engaging the pectoral skeleton range from tendon snapping in croaking gouramis (Kratochvil, 1978) to pectoral spine vibra- tion in catfish (Fig. 10.1A) (Fine et al., 1997) and pectoral girdle vibration in sculpin that lack a swim bladder (Bass and Baker, 1991). Despite these divergent mechanisms, sonic motor neurons are positioned in the same hindbrain-spinal region of the pectoral motor column in sculpin (Bass and Baker, 1991; Ladich and Bass, 2005), catfish (Ladich and Fine, 1994; Ladich and Bass, 1998), and gouramis (Ladich and Fine, 1992). Sonic neurons

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188  /  Andrew H. Bass and Boris P. Chagnaud map to the same location in sea robins, close relatives of sculpin that have sonic muscles completely attached to the swim bladder as in distantly related toadfishes (Bass and Baker, 1991). Some species of catfish exhibit both swim bladder and pectoral-dependent sonic phenotypes (Ladich and Fine, 1994). These results highlight the developmental and evolutionary coupling of pectoral motor systems that are multifunctional (locomotion and sound production) with vocal systems that are dedicated to acoustic signaling (e.g., in toadfish and sea robins; Fig. 10.1C), a character that is observed among tetrapods as well (as detailed later). SHARED INTRINSIC AND NETWORK PROPERTIES FOR rh8 Precise temporal patterning of motor output and hence behavior, like that exemplified by vocalization, requires a suite of intrinsic and network properties to synchronize population-level activity [e.g., Van Vreeswijk et al. (1994), Perez Velazquez and Carlen (2000), Uhlhaas and Singer (2010)] including (i) repolarization conductances underlying oscillatory activity of premotor neurons; (ii) electrotonic coupling, within and between premo- tor and motor populations; (iii) widespread premotor excitatory input to target neurons; (iv) rhythmic firing of premotor and target population; (v) synchronous premotor firing; and (vi) inhibitory input to premotor neu- rons. Rhombomere 8/occipital premotor populations showing combina- tions of these characters include the VPP–VPN network (Chagnaud et al., 2011, 2012), pacemaker neurons in electromotor systems (Bennett, 1971), area I neurons of the occulomotor system (Pastor et al., 1994), T-reticular neurons (Kimmel et al., 1985; Koyama et al., 2011) driving pectoral motor neurons during the escape response (Auerbach and Bennett, 1969), and the inferior olive [e.g., Urbano et al. (2006); Llinás and Yarom (1981)]. Each rh8 premotor population has a distinct electroresponsive “sig- nature” coding for an equally distinct behavioral attribute. Pacemaker (i.e., VPN) membrane oscillations directly code vocal frequency, whereas VPP-sustained depolarizations code vocal duration (Fig. 10.5A and B) (Chagnaud et al., 2011). Oscillatory pacemaker neurons in weakly electric fish, a VPN analogue, directly set electric organ discharge frequency (a VPP analogue is likely missing given the constant electric organ discharge) (Bennett, 1971). Area I in fish codes for eye position (Fig. 10.5C) (Pastor et al., 1994; Aksay et al., 2000, 2003). Like the vocal system, inhibitory coupling and synchronous firing, in this case shown by paired record- ings, shape area I firing patterns (Aksay et al., 2001, 2003). Like VPN, rh8-derived inferior olive neurons (Cambronero and Puelles, 2000) tend to fire synchronously in an oscillatory fashion (Fig. 10.5D) (Llinás et al., 1974; Llinás and Yarom, 1986). In addition to voltage-dependent conductances underlying this rhythmicity, inferior olive neurons show strong gap junc-

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  189 FIGURE 10.5 Spatiotemporal coding of behavioral attributes by rh8 premotor nuclei. Shown are single traces of neuronal activity (black) of midshipman fish vocal pacemaker (A) and VPP (B), goldfish oculomotor (C) and guinea pig inferior olive (D), and corresponding behavioral readout (red). (A) Inset: Dependency of membrane oscillations (i.e., cycles) and pulse repetition rate/frequency of vocal output. (B) Inset: Dependency of duration of membrane-sustained depolarization and call duration (i.e., length). (D) Inset: Correlation in rats between tongue licking behavior (red) and cerebellar complex spike activity (black) that directly reflects levels of inferior olive activity. [A and B adapted from Chagnaud et al. (2011); C reprinted by permission from Macmillan Publishers Ltd: Nature Neuroscience (Aksay et al., 2001), copyright 2001; D reproduced with permission from John Wiley & Sons (Llinás and Yarom, 1986); D (Inset) reprinted by permission from Macmillan Publishers Ltd: Nature (Welsh et al., 1995), copyright 1995.] [Note: Figure can be viewed in color in the PDF version of this volume on the National Academies Press website, www.nap.edu.] tional coupling that synchronizes functional groups or patches of neurons involved in complex tasks such as tongue licking (Fig. 10.5D) (Llinás and Paré, 1994; Welsh et al., 1995; Urbano et al., 2006).

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190  /  Andrew H. Bass and Boris P. Chagnaud Although comparable investigations of intrinsic and network prop- erties are currently lacking for the pectoral motor system, the available neurophysiological data on the neural basis of escape behavior in hatch- etfish (Auerbach and Bennett, 1969) are consistent with the view that rh8 premotor populations provide a coherent timing signal synchronizing the activity of one or more neuromuscular compartments determining a behavior [sensu Llinás and Paré (1994)]. Recent studies of hindbrain cir- cuitry in zebrafish, including the pectoral network, have begun to identify developmental events establishing the neuronal complement of rh- and neurobehavioral-specific nuclei (Kinkhabwala et al., 2011; Koyama et al., 2011). COUPLING OF VOCAL AND PECTORAL–GESTURAL CIRCUITRY There has been much discussion regarding the vocal vs. gestural ori- gins of speech and language [e.g., Gentilucci et al. (2008), Liebal and Call (2012); also see Lieberman (2006), MacNeilage (2008)]. The comparison may, however, be a false dichotomy when we consider the shared devel- opmental origins and social signaling functions of vocal and pectoral systems. Birds and mammals, like fishes [as detailed earlier; also see Ladich et al. (1992)], exhibit vocal and pectoral-dependent mechanisms of acoustic communication. For example, various bird species that use the syrinx to vocalize also use pectoral wings innervated by forelimb spinal motor neurons (Fig. 10.1C) to generate nonvocal, sonic signals important for communication (e.g., manakin; Fig. 10.1A) (Prum, 1998; Hingee and Magrath, 2009; Miller and Baker, 2009; Bostwick et al., 2010; Barske et al., 2011). Examples of nonvocal, sonic pectoral signaling among mammals that use the larynx to vocalize include drumming by macaque monkeys and gorillas and acoustic gesturing by humans (Reynolds, 1965; Remedios et al., 2009). More generally, temporal coupling between vocalization and pectoral forelimb movement in humans has led to the hypothesis that “tasks requiring precisely timed movements of the vocal tract and hands and arms appear to share common brain mechanisms” [Iverson and Thelen (1999); also see Gentilucci et al. (2008)]. Vocal–gestural coupling is largely considered to depend on forebrain (e.g., premotor/motor cortex, Broca area) and cerebellar (Iverson and Thelen, 1999; Iverson and Fagan, 2004) mechanisms, with essentially no consideration of the potential role of hindbrain premotor circuitry. Collectively, the available developmental and behavioral evidence discussed here and in previous sections suggests that the neural basis for vocal and pectoral coupling observed among tetrapods, including nonvocal sonic and gestural signaling, has ancient origins among fishes at the most fundamental level of hindbrain pattern generators (Fig. 10.1C).

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Neural Basis of Vocal–Acoustic and Pectoral–Gestural Signaling  /  191 CONCLUDING COMMENTS Pattern-generating circuitry underlying the vocal basis for acoustic communication in fishes and tetrapods evolved from an ancestrally shared hindbrain, rh8-spinal compartment. This compartment also gave rise to premotor-motor circuitry for pectoral appendages that serve locomotion and nonvocal, sonic–acoustic signaling functions in fishes. These shared developmental origins suggest that the functional coupling between more highly derived vocal and pectoral mechanisms that have evolved for acoustic and gestural signaling in tetrapods originated in fishes. More broadly, we propose that, among vertebrates in general, rh8- spinal networks include anatomically separate premotor nuclei, each of which has a distinct suite of intrinsic and network properties determin- ing specific behavioral attributes (Fig. 10.5). Each network’s ensemble of premotor nuclei configures the spatiotemporal activity of one or more neuromuscular systems underlying entire behaviors such as vocalization [also see Llinás and Paré (1994)]. By comparing rh8-spinal networks across vertebrate lineages, we can identify ancestral characters contributing to evolutionarily derived networks, for example, the anatomical and neu- rophysiological properties of sonic–vocal networks in fishes found in the sonic–vocal networks of birds and mammals. This includes phylogeneti- cally deep homologies, that is, “molecular and cellular components . . . contributing to phenotypic novelties” that “enable us to reconstruct how a phenotype was built over evolutionary time” (McCune and Schimenti, 2012). ACKNOWLEDGMENTS We thank R. Baker, D. Deitcher, L.-H. Ma, R. G. Northcutt, K. Roh­mann, N. Segil, and the reviewers for helpful discussions and comments on ear- lier versions of the manuscript; R. Baker, E. Gilland, and L.-H. Ma for collaborations on research reviewed here; M. Nelson and M. Marchaterre for drawings in Fig. 10.1; M. Marchaterre for movies used in analysis; E. Adkins-Regan, K. Bostwick, F. Ladich, U. Jürgens, and M. Marchaterre for sound recordings; John Avise, Francisco Ayala, and Georg Striedter for the invitation to participate in the Sackler Colloquium. This work was supported by National Institutes of Health Grant DC00092 and National Science Foundation Grant IOS1120925.

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