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      Cephalopods in neuroscience: regulations, research and the 3Rs

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      , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , ,
      Invertebrate Neuroscience
      Springer Berlin Heidelberg
      Cephalopods, Directive2010/63/EU, Animal welfare, 3Rs, Neuroscience

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          Abstract

          Cephalopods have been utilised in neuroscience research for more than 100 years particularly because of their phenotypic plasticity, complex and centralised nervous system, tractability for studies of learning and cellular mechanisms of memory (e.g. long-term potentiation) and anatomical features facilitating physiological studies (e.g. squid giant axon and synapse). On 1 January 2013, research using any of the about 700 extant species of “live cephalopods” became regulated within the European Union by Directive 2010/63/EU on the “Protection of Animals used for Scientific Purposes”, giving cephalopods the same EU legal protection as previously afforded only to vertebrates. The Directive has a number of implications, particularly for neuroscience research. These include: (1) projects will need justification, authorisation from local competent authorities, and be subject to review including a harm-benefit assessment and adherence to the 3Rs principles (Replacement, Refinement and Reduction). (2) To support project evaluation and compliance with the new EU law, guidelines specific to cephalopods will need to be developed, covering capture, transport, handling, housing, care, maintenance, health monitoring, humane anaesthesia, analgesia and euthanasia. (3) Objective criteria need to be developed to identify signs of pain, suffering, distress and lasting harm particularly in the context of their induction by an experimental procedure. Despite diversity of views existing on some of these topics, this paper reviews the above topics and describes the approaches being taken by the cephalopod research community (represented by the authorship) to produce “guidelines” and the potential contribution of neuroscience research to cephalopod welfare.

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          Most cited references307

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          Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules: Extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators.

          Cephalopods are extraordinary molluscs equipped with vertebrate-like intelligence and a unique buoyancy system for locomotion. A growing body of evidence from the fossil record, embryology and Bayesian molecular divergence estimations provides a comprehensive picture of their origins and evolution. Cephalopods evolved during the Cambrian (∼530 Ma) from a monoplacophoran-like mollusc in which the conical, external shell was modified into a chambered buoyancy apparatus. During the mid-Palaeozoic (∼416 Ma) cephalopods diverged into nautiloids and the presently dominant coleoids. Coleoids (i.e. squids, cuttlefish and octopods) internalised their shells and, in the late Palaeozoic (∼276 Ma), diverged into Vampyropoda and the Decabrachia. This shell internalisation appears to be a unique evolutionary event. In contrast, the loss of a mineralised shell has occurred several times in distinct coleoid lineages. The general tendency of shell reduction reflects a trend towards active modes of life and much more complex behaviour. Copyright © 2011 WILEY Periodicals, Inc.
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            An octopus-bioinspired solution to movement and manipulation for soft robots.

            Soft robotics is a challenging and promising branch of robotics. It can drive significant improvements across various fields of traditional robotics, and contribute solutions to basic problems such as locomotion and manipulation in unstructured environments. A challenging task for soft robotics is to build and control soft robots able to exert effective forces. In recent years, biology has inspired several solutions to such complex problems. This study aims at investigating the smart solution that the Octopus vulgaris adopts to perform a crawling movement, with the same limbs used for grasping and manipulation. An ad hoc robot was designed and built taking as a reference a biological hypothesis on crawling. A silicone arm with cables embedded to replicate the functionality of the arm muscles of the octopus was built. This novel arm is capable of pushing-based locomotion and object grasping, mimicking the movements that octopuses adopt when crawling. The results support the biological observations and clearly show a suitable way to build a more complex soft robot that, with minimum control, can perform diverse tasks.
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              Cephalopod chromatophores: neurobiology and natural history.

              The chromatophores of cephalopods differ fundamentally from those of other animals: they are neuromuscular organs rather than cells and are not controlled hormonally. They constitute a unique motor system that operates upon the environment without applying any force to it. Each chromatophore organ comprises an elastic sacculus containing pigment, to which is attached a set of obliquely striated radial muscles, each with its nerves and glia. When excited the muscles contract, expanding the chromatophore; when they relax, energy stored in the elastic sacculus retracts it. The physiology and pharmacology of the chromatophore nerves and muscles of loliginid squids are discussed in detail. Attention is drawn to the multiple innervation of dorsal mantle chromatophores, of crucial importance in pattern generation. The size and density of the chromatophores varies according to habit and lifestyle. Differently coloured chromatophores are distributed precisely with respect to each other, and to reflecting structures beneath them. Some of the rules for establishing this exact arrangement have been elucidated by ontogenetic studies. The chromatophores are not innervated uniformly: specific nerve fibres innervate groups of chromatophores within the fixed, morphological array, producing 'physiological units' expressed as visible 'chromatomotor fields'. The chromatophores are controlled by a set of lobes in the brain organized hierarchically. At the highest level, the optic lobes, acting largely on visual information, select specific motor programmes (i.e. body patterns); at the lowest level, motoneurons in the chromatophore lobes execute the programmes, their activity or inactivity producing the patterning seen in the skin. In Octopus vulgaris there are over half a million neurons in the chromatophore lobes, and receptors for all the classical neurotransmitters are present, different transmitters being used to activate (or inhibit) the different colour classes of chromatophore motoneurons. A detailed understanding of the way in which the brain controls body patterning still eludes us: the entire system apparently operates without feedback, visual or proprioceptive. The gross appearance of a cephalopod is termed its body pattern. This comprises a number of components, made up of several units, which in turn contains many elements: the chromatophores themselves and also reflecting cells and skin muscles. Neural control of the chromatophores enables a cephalopod to change its appearance almost instantaneously, a key feature in some escape behaviours and during agonistic signalling. Equally important, it also enables them to generate the discrete patterns so essential for camouflage or for signalling. The primary function of the chromatophores is camouflage. They are used to match the brightness of the background and to produce components that help the animal achieve general resemblance to the substrate or break up the body's outline. Because the chromatophores are neurally controlled an individual can, at any moment, select and exhibit one particular body pattern out of many. Such rapid neural polymorphism ('polyphenism') may hinder search-image formation by predators. Another function of the chromatophores is communication. Intraspecific signalling is well documented in several inshore species, and interspecific signalling, using ancient, highly conserved patterns, is also widespread. Neurally controlled chromatophores lend themselves supremely well to communication, allowing rapid, finely graded and bilateral signalling.
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                Author and article information

                Contributors
                cephres@cephalopodresearch.org
                Journal
                Invert Neurosci
                Invert. Neurosci
                Invertebrate Neuroscience
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1354-2516
                1439-1104
                3 January 2014
                3 January 2014
                2014
                : 14
                : 13-36
                Affiliations
                [ ]Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy
                [ ]Associazione Cephalopod Research ‘CephRes’, ONLUS, Via dei Fiorentini 21, 80133 Naples, Italy
                [ ]Animal Model Facility, BIOGEM SCARL, Via Camporeale Area PIP, Ariano Irpino, AV Italy
                [ ]Midlothian Innovation Centre, Pentland Management Systems, Pentlandfield, Roslin, EH25 9RE UK
                [ ]Biology Department, CUNY Graduate Center, Brooklyn College, 2900 Bedford Avenue, Brooklyn, NY 11210 USA
                [ ]Muséum National d’Histoire Naturelle, DMPA, Lab. BOREA, UMR MNHN CNRS 7208-IRD 207-UPMC, Paris Cedex, France
                [ ]Université Paris Diderot, Sorbonne Paris Cité, Paris, France
                [ ]Ministero della Salute, Via G. Ribotta 5, 00144 Rome, Italy
                [ ]BIOGEM SCARL, Via Camporeale Area PIP, Ariano Irpino, AV Italy
                [ ]Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
                [ ]Home Office, Animals in Science Regulation Unit, Dundee, DD1 9WW Scotland, UK
                [ ]Groupe Mémoire et Plasticité Comportementale, EA4259, GdR CNRS 2822 Ethology, University of Caen Basse-Normandy, Caen, France
                [ ]Department of Biology, University of Naples Federico II, Naples, Italy
                [ ]Department of Biological and Environmental Sciences, University of Sannio, Benevento, Italy
                [ ]Instituto de Investigaciones Marinas (IIM-CSIC), Vigo, Spain
                [ ]Center for GeoGenetics, University of Copenhagen, 1350 Copenhagen, Denmark
                [ ]Department of Psychology, BioMimetic and Cognitive Robotics, Brooklyn College, CUNY, Brooklyn, NY 11210 USA
                [ ]Institute of Marine Research, 5817 Bergen, Norway
                [ ]Max Planck Institute for Brain Research, 60438 Frankfurt, Germany
                [ ]Institute of Cognitive Sciences and Technologies, CNR, Via Aldovrandi 16b, Rome, Italy
                [ ]Integrative Ecophysiology, Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
                [ ]School of Life Sciences, University of Sussex, Brighton, E Sussex, BN1 9RH UK
                [ ]European Mouse Mutant Archive (CNR-EMMA), Consiglio Nazionale delle Ricerche, Campus A. Buzzati-Traverso, Viale E. Ramarini, 32, 00015 Monterotondo Scalo, Roma, Italy
                [ ]Department of Life Sciences, Ben-Gurion University of the Negev, Eilat Campus, 84105 Beer-Sheva, Israel
                [ ]Federation for Laboratory Animal Science Associations (FELASA), London, UK
                [ ]The Boyd Group, Hereford, UK
                [ ]Centre of Marine Sciences (CCMAR), Universidade do Algarve, 8005-139 Faro, Portugal
                [ ]Renewable Marine Resources Department, Institut de Ciències del Mar (CSIC), Barcelona, Spain
                [ ]Department of Biology, University of Oregon, Eugene, OR 97403 USA
                [ ]Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genoa, Italy
                [ ]Division of Biomedical Sciences, St George’s University of London, Cranmer Terrace, London, SW17 0RE UK
                Article
                165
                10.1007/s10158-013-0165-x
                3938841
                24385049
                ef57e7e1-7f77-4fa6-9c0f-f03a1218c99f
                © The Author(s) 2013

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

                History
                : 27 July 2013
                : 8 November 2013
                Categories
                Review Article
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                © Springer-Verlag Berlin Heidelberg 2014

                Neurosciences
                cephalopods,directive2010/63/eu,animal welfare,3rs,neuroscience
                Neurosciences
                cephalopods, directive2010/63/eu, animal welfare, 3rs, neuroscience

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