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evolution of feeding motor patterns in lizards: Modulatory complexity and possible constraints, The

American Zoologist, Dec 2001 by Herrel, Anthony, Meyers, Jay J, Nishikawa, Kiisa C, De Vree, Frits

SYNOPSIS. Previous research indicated that the evolution of feeding motor patterns across major taxonomic groups might have occurred without large modifications of the control of the jaw and hyolingual muscles. However, the proposal of this evolutionary scheme was hampered by the lack of data for some key taxa such as lizards. Recent data on jaw and hyolingual feeding motor patterns of a number of lizard families suggest extensive variability within and among species. Although most lizards respond to changes in the structural properties of food items by modulating the activation of the jaw and hyolingual muscles, some food specialists might have lost this ability. Whereas the overall similarity in motor patterns across different lineages of lizards is large for the hyolingual muscles, jaw muscle activation patterns seem to be more flexible. Nevertheless, all data suggest that both the jaw and hyolingual system are complexly integrated. The elimination of feedback pathways from the hyolingual system through nerve transection experiments clearly shows that feeding cycles are largely shaped by feedback interactions. Yet, novel motor patterns including unilateral control seem to have emerged in the evolution from lizards to snakes.

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INTRODUCTION The vertebrate head is a textbook example of a complex integrated system, where one function cannot be optimised without potentially compromising others (Lauder, 1989). In addition to being a major information gathering and processing centre, immensly diverse functions such as feeding, breathing, drinking, display, and in many tetrapods also vocalisation, have to be performed by the same elements. Yet, these diverse functions can only be performed through the interplay between the jaw and hyolingual systems. Both these systems are complex units composed of a large number of muscles attached to bony or cartilagenous elements. Moreover, as the hyolingual apparatus is a musculoskeletal system suspended between the jaws and the pectoral girdle, the potential number of degrees of freedom is enormous. To add to this complexity, both systems are largely innervated through different pathways. Whereas the jaw adductor system in lizards is mainly innervated by the trigeminal and facial nerves (providing both motor input and sensory afferents), the hyolingual system is mainly supplied by the glossopharyngeal (largely sensory), hypoglossal (predominantly motor input) and first spinal nerves (motor input into the hyoid retractors; Willard, 1915; Oelrich, 1956; Meyers and Nishikawa, 2000). Direct connections between the two systems exist, as the mandibular ramus of the n. trigeminus provides motor input into the m. intermandibularis (running inbetween the two rami of the lower jaw) and branches out into the tongue functioning as sensory afferent and physically connecting to the N. hypoglossus. Feedback from the visual, olfactory, gustatory, vomeronasal and somatosensory (e.g., muscle spindles, joint receptors) systems are also important in assuring optimal feeding.

Given this structural complexity, the control of the feeding apparatus is a complex task which appears to require continuous on-line control. Yet, for cyclical systems in general, a simple neuromotor steering based on a centralised pattern generator (or a set of coupled CPG's) is thought to exist, thus largely simplifying control (e.g., Grillner and Wallen, 1985; Szekely, 1989). Although this paradigm is largely based on studies on the locomotor apparatus, a similar control paradigm is usually put forward for mammalian chewing cycles (Thexton, 1974, 1976; Dellow, 1976). In accordance with this theoretical framework, it has been suggested that in lower tetrapods too, the feeding cycles might be driven by fairly simple motor pattern generators or neural oscillators (Bramble and Wake, 1985).

Based on the large similarities between lower tetrapod and mammalian feeding cycles, it was hypothesized that the evolution of feeding motor patterns across major taxonomic groups might have occurred without large modifications of the central pattern generators) controlling the jaw and hyolingual muscles (Bramble and Wake, 1985). The basic elements of the lower tetrapod feeding cycle were summarised in a theoretical model feeding cycle which was hypothesised to represent the primitive tetrapod condition. In analogy to the mammalian feeding cycle, the model feeding cycle was subdivided into five distinct phases: the slow opening of the jaws (I and II), fast opening, fast closing and a slow closing/ power stroke. Muscle activation patterns associated with these kinematic units were proposed as well. Whereas the slow opening phase was thought to be caused by an activation of the jaw opener, intrinsic tongue muscles, the intermandibularis group and the tongue and hyoid protractors, during fast opening coactivation of the cervical epaxial musculature, the jaw opener and hyoid retractors was expected to occur. Jaw closing on the other hand was thought to be associated with activity in the hyoid retractors (fast closing), jaw adductors and potentially the jaw opener (Bramble and Wake, 1985).

evolution of feeding motor patterns in lizards: Modulatory complexity and possible constraints, The

American Zoologist, Dec 2001 by Herrel, Anthony, Meyers, Jay J, Nishikawa, Kiisa C, De Vree, Frits

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