Non-invasive study of Octopus vulgaris arm morphology using ultrasound

SUMMARY Octopus arms are extremely dexterous structures. The special arrangements of the muscle fibers and nerve cord allow a rich variety of complex and fine movements under neural control. Historically, the arm structure has been investigated using traditional comparative morphological ex vivo analysis. Here, we employed ultrasound imaging, for the first time, to explore in vivo the arms of the cephalopod mollusc Octopus vulgaris. Sonographic examination (linear transducer, 18 MHz) was carried out in anesthetized animals along the three anatomical planes: transverse, sagittal and horizontal. Images of the arm were comparable to the corresponding histological sections. We were able, in a non-invasive way, to measure the dimensions of the arm and its internal structures such as muscle bundles and neural components. In addition, we evaluated echo intensity signals as an expression of the difference in the muscular organization of the tissues examined (i.e. transverse versus longitudinal muscles), finding different reflectivity based on different arrangements of fibers and their intimate relationship with other tissues. In contrast to classical preparative procedures, ultrasound imaging can provide rapid, destruction-free access to morphological data from numerous specimens, thus extending the range of techniques available for comparative studies of invertebrate morphology.

[1]  Georges Cuvier,et al.  Mémoires pour servir a l'histoire et a l'anatomie des mollusques , 1817 .

[2]  Forces exerted by Octopus vulgaris. , 1964 .

[3]  D. Newth THE ANATOMY OF THE NERVOUS SYSTEM OF OCTOPUS VULGARIS , 1972 .

[4]  A. Packard,et al.  CEPHALOPODS AND FISH: THE LIMITS OF CONVERGENCE , 1972 .

[5]  B. Runnegar,et al.  Molluscan Phylogeny: The Paleontological Viewpoint , 1974, Science.

[6]  D. Dewsbury,et al.  Octopus: Physiology and behaviour of an advanced invertebrate. , 1978 .

[7]  W. Kier The functional morphology of the musculature of squid (Loliginidae) arms and tentacles , 1982, Journal of morphology.

[8]  W. Kier,et al.  The musculature of squid arms and tentacles: Ultrastructural evidence for functional differences , 1985, Journal of morphology.

[9]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[10]  R. Goldstein,et al.  Pitfalls in femur length measurements. , 1987, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[11]  M. Chichery,et al.  Manipulative motor activity of the cuttlefish Sepia Officinalis during prey-capture , 1988, Behavioural Processes.

[12]  G. Fiorito,et al.  Problem solving ability of Octopus vulgaris Lamarck (Mollusca, Cephalopoda). , 1990, Behavioral and neural biology.

[13]  J. Davenport Ultrasonography: a Non-Invasive Tool for the Study of Structure and Mechanical Events in Marine Animals , 1993, Journal of the Marine Biological Association of the United Kingdom.

[14]  E.E. Pissaloux,et al.  Image Processing , 1994, Proceedings. Second Euromicro Workshop on Parallel and Distributed Processing.

[15]  James A. Zagzebski,et al.  Essentials Of Ultrasound Physics , 1996 .

[16]  Y Gutfreund,et al.  Organization of Octopus Arm Movements: A Model System for Studying the Control of Flexible Arms , 1996, The Journal of Neuroscience.

[17]  J A Mather,et al.  How do octopuses use their arms? , 1998, Journal of comparative psychology.

[18]  B. Hochner,et al.  Control of Octopus Arm Extension by a Peripheral Motor Program , 2001, Science.

[19]  S. Pillen,et al.  Quantitative ultrasonography of skeletal muscles in children: Normal values , 2003, Muscle & nerve.

[20]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[21]  Christopher C. Pagano,et al.  Continuum robot arms inspired by cephalopods , 2005, SPIE Defense + Commercial Sensing.

[22]  R. Full,et al.  Underwater Bipedal Locomotion by Octopuses in Disguise , 2005, Science.

[23]  S. Adamo,et al.  Using ultrasound to understand vascular and mantle contributions to venous return in the cephalopod Sepia officinalis L. , 2005, Journal of Experimental Biology.

[24]  Germán Sumbre,et al.  Neurobiology: Motor control of flexible octopus arms , 2005, Nature.

[25]  S. Adamo,et al.  The ventilatory, cardiac and behavioural responses of resting cuttlefish (Sepia officinalis L.) to sudden visual stimuli , 2006, Journal of Experimental Biology.

[26]  W. Kier,et al.  The arrangement and function of octopus arm musculature and connective tissue , 2007, Journal of morphology.

[27]  G. Fiorito,et al.  Using ultrasound to estimate brain size in the cephalopod Octopus vulgaris Cuvier in vivo , 2007, Brain Research.

[28]  F. Grasso Octopus sucker-arm coordination in grasping and manipulation* , 2008 .

[29]  B Mazzolai,et al.  Design of a biomimetic robotic octopus arm , 2009, Bioinspiration & biomimetics.

[30]  Chris L de Korte,et al.  Quantitative gray‐scale analysis in skeletal muscle ultrasound: A comparison study of two ultrasound devices , 2009, Muscle & nerve.

[31]  T. Tregenza,et al.  Defensive tool use in a coconut-carrying octopus , 2009, Current Biology.

[32]  E. Alleva,et al.  A catalogue of body patterning in cephalopoda , 2011 .