In the Light of Evolution Volume VI: Brain and Behavior (2013) / Chapter Skim
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10 Shared Developmental and Evolutionary Origins for Neural Basis of VocalAcoustic and PectoralGestural Signaling--Andrew H. Bass and Boris P. Chagnaud
10 Shared Developmental and Evolutionary Origins for Neural Basis of VocalAcoustic and PectoralGestural Signaling--Andrew H. Bass and Boris P. Chagnaud
Pages 175-192
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From page 175... ...
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.
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From page 176... ...
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 understanding 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.
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From page 177... ...
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)
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From page 178... ...
, underscored a preeminent role for caudal hindbrain nuclei in the spatiotemporal 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 intervals, duration, amplitude)
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From page 179... ...
. 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)
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From page 180... ...
(B) Spontaneous vocal motor volley recorded from vocal occipital nerve (VOC)
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From page 181... ...
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)
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From page 182... ...
likely homology of occipital 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)
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From page 183... ...
. 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.
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From page 184... ...
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)
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From page 185... ...
. Pectoral motor neurons, identified following retrograde transport of fluorescent dye from fin buds, were concurrently mapped with other neuronal landmarks including (i)
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From page 186... ...
Chagnaud FIGURE 10.4 Map of developing pectoral motor nucleus in rh8-spinal compartment of basal and derived groups of actinopterygian fish (A and B, dorsal views)
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From page 187... ...
, 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)
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From page 188... ...
driving pectoral motor neurons during the escape response (Auerbach and Bennett, 1969) , and the inferior olive [e.g., Urbano et al.
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From page 189... ...
of midshipman fish vocal pacemaker (A)
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From page 190... ...
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.
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From page 191... ...
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, rh8spinal networks include anatomically separate premotor nuclei, each of which has a distinct suite of intrinsic and network properties determining specific behavioral attributes (Fig.
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