Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-26T07:04:42.012Z Has data issue: false hasContentIssue false
  • English
  • Français

The pig model in brain imaging and neurosurgery

Published online by Cambridge University Press:  01 August 2009

P. Sauleau ,
E. Lapouble ,
D. Val-Laillet  and
C.-H. Malbert
P. Sauleau
Affiliation:
INRA, UMR1079 SENAH, 35590 Saint-Gilles, France
E. Lapouble
Affiliation:
INRA, UMR1079 SENAH, 35590 Saint-Gilles, France
D. Val-Laillet
Affiliation:
INRA, UMR1079 SENAH, 35590 Saint-Gilles, France
C.-H. Malbert*
Affiliation:
INRA, UMR1079 SENAH, 35590 Saint-Gilles, France
*
†E-mail: [email protected]
Get access

Abstract

The pig model is increasingly used in the field of neuroscience because of the similarities of its brain with human. This review presents the peculiarities of the anatomy and functions of the pig brain with specific reference to its human counterpart. We propose an approximate mapping of the pig’s cortical areas since a comprehensive description of the equivalent of Brodmann’s areas is lacking. On the contrary, deep brain structures are received more consideration but a true three-dimensional (3D) atlas is still eagerly required. In the second section, we present an overview of former works describing the use of functional imaging and neuronavigation in the pig model. Recently, the pig has been increasingly used for molecular imaging studies using positron emission tomography (PET). Indeed, the large size of its brain is compatible with the limited spatial resolution of the PET scanner built to accommodate a human being. Similarly, neuronavigation is an absolute requirement to target deep brain areas in human and in pig since the surgeon cannot rely on external skull structures for zeroing the 3D reference frame. Therefore, a large body of methodological refinements has been dedicated to image guided surgery in the pig model. These refinements allow now a millimetre precision: an absolute requirement for basal nuclei targeting. In the third section, several examples of ongoing studies in our laboratory were presented to illustrate the intricacies of using the pig model. For both examples, after a brief description of the scientific context of the experiment, we present, in detail, the methodological steps required to achieve the experimental goals, which are specific to the porcine model. Finally, in the fourth section, the anatomical variations depending on the breed and age are discussed in relation with neuronavigation and brain surgery. The need for a digitized multimodality brain atlas is also highlighted.

Keywords

pigneuroimagingsingle photon emission tomographyneuronavigationdeep brain stimulation
Type
Full Paper
Information
animal , Volume 3 , Issue 8 , August 2009 , pp. 1138 - 1151
Copyright
Copyright © The Animal Consortium 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agarwal, RK, Chandna, VK, Engelking, LR, Lightbown, K, Kumar, MS 1993. Distribution of catecholamines in the central nervous system of the pig. Brain Research Bulletin 32, 285–291.CrossRefGoogle ScholarPubMed
Andersen, F, Watanabe, H, Bjarkam, C, Danielsen, EH, Cumming, P 2005. Pig brain stereotaxic standard space: mapping of cerebral blood flow normative values and effect of MPTP-lesioning. Brain Research Bulletin 66, 17–29.CrossRefGoogle ScholarPubMed
Andrews, RJ, Knight, RT, Kirby, RP 1990. Evoked potential mapping of auditory and somatosensory cortices in the miniature swine. Neuroscience Letters 114, 27–31.CrossRefGoogle ScholarPubMed
Baskin, DS, Browning, JL, Widmayer, MA, Zhu, ZQ, Grossman, RG 1994. Development of a model for Parkinson’s disease in sheep using unilateral intracarotid injection of MPTP via slow continuous infusion. Life Sciences 54, 471–479.CrossRefGoogle Scholar
Beale, AM, Higgins, RJ, Work, TM, Bailey, CS, Smith, MO, Shinka, T, Hammock, BD 1989. MPTP-induced Parkinson-like disease in sheep: clinical and pathologic findings. Journal of Environmental Pathology, Toxicology and Oncology 9, 417–428.Google ScholarPubMed
Berthoud, HR, Lynn, PA, Blackshaw, LA 2001. Vagal and spinal mechanosensors in the rat stomach and colon have multiple receptive fields. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 280, R1371–R1381.CrossRefGoogle ScholarPubMed
Bhalla, P, Saxena, PR, Sharma, HS 2002. Molecular cloning and tissue distribution of mRNA encoding porcine 5-HT7 receptor and its comparison with the structure of other species. Molecular and Cellular Biochemistry 238, 81–88.CrossRefGoogle ScholarPubMed
Bjarkam, CR, Cancian, G, Larsen, M, Rosendahl, F, Ettrup, KS, Zeidler, D, Blankholm, AD, Ostergaard, L, Sunde, N, Sorensen, JC 2004. A MRI-compatible stereotaxic localizer box enables high-precision stereotaxic procedures in pigs. Journal of Neuroscience Methods 139, 293–298.CrossRefGoogle ScholarPubMed
Bollen, P, Hansen, AK, Rasmussen, HJ 2000. The laboratory swine. CRC Press, Boca Raton, FL, USA.Google Scholar
Breazile, JE 1967. The cytoarchitecture of the brain stem of the domestic pig. The Journal of Comparative Neurology 129, 169–188.CrossRefGoogle Scholar
Breazile, JE, Swafford, BC, Thompson, WD 1966. Study of the motor cortex of the domestic pig. American Journal of Veterinary Research 27, 1369–1373.Google Scholar
Campbell, AW 1905. Histological studies on the localisation of cerebral function. Cambridge University Press, Cambridge.Google Scholar
Cottrell, DF, Iggo, A 1984. Mucosal enteroceptors with vagal afferent fibres in the proximal duodenum of sheep. The Journal of Physiology 354, 497–522.CrossRefGoogle ScholarPubMed
Craner, SL, Ray, RH 1991a. Somatosensory cortex of the neonatal pig: I. Topographic organization of the primary somatosensory cortex (SI). The Journal of Comparative Neurology 306, 24–38.CrossRefGoogle ScholarPubMed
Craner, SL, Ray, RH 1991b. Somatosensory cortex of the neonatal pig: II. Topographic organization of the secondary somatosensory cortex (SII). The Journal of Comparative Neurology 306, 39–48.CrossRefGoogle ScholarPubMed
Cumming, P, Danielsen, EH, Vafaee, M, Falborg, L, Steffensen, E, Sorensen, JC, Gillings, N, Bender, D, Marthi, K, Andersen, F, Munk, O, Smith, D, Moller, A, Gjedde, A 2001. Normalization of markers for dopamine innervation in striatum of MPTP-lesioned miniature pigs with intrastriatal grafts. Acta Neurologica Scandinavica 103, 309–315.CrossRefGoogle ScholarPubMed
Cumming, P, Møller, M, Benda, K, Minuzzi, L, Jakobsen, S, Jensen, SB, Pakkenberg, B, Stark, AK, Gramsbergen, JB, Andreasen, MF, Olsen, AK 2007. A PET study of effects of chronic 3,4-methylenedioxymethamphetamine (MDMA, “ecstasy”) on serotonin markers in Göttingen minipig brain. Synapse 61, 478–487.CrossRefGoogle ScholarPubMed
Cumming, P, Rosa-Neto, P, Watanabe, H, Smith, D, Bender, D, Clarke, PB, Gjedde, A 2003. Effects of acute nicotine on hemodynamics and binding of [11C]raclopride to dopamine D2,3 receptors in pig brain. NeuroImage 19, 1127–1136.CrossRefGoogle ScholarPubMed
Dall, AM, Danielsen, EH, Sorensen, JC, Andersen, F, Moller, A, Zimmer, J, Gjedde, AH, Cumming, P 2002. Quantitative [18F]fluorodopa/PET and histology of fetal mesencephalic dopaminergic grafts to the striatum of MPTP-poisoned minipigs. Cell Transplantation 11, 733–746.CrossRefGoogle Scholar
Dalmose, AL, Bjarkam, CR, Sorensen, JC, Djurhuus, JC, Jorgensen, TM 2004. Effects of high frequency deep brain stimulation on urine storage and voiding function in conscious minipigs. Neurourology and Urodynamics 23, 265–272.CrossRefGoogle ScholarPubMed
Danielsen, EH, Cumming, P, Andersen, F, Bender, D, Brevig, T, Falborg, L, Gee, A, Gillings, NM, Hansen, SB, Hermansen, F, Johansen, J, Johansen, TE, Dahl-Jorgensen, A, Jorgensen, HA, Meyer, M, Munk, O, Pedersen, EB, Poulsen, PH, Rodell, AB, Sakoh, M, Simonsen, CZ, Smith, DF, Sorensen, JC, Ostergard, L, Zimmer, J, Gjedde, A 2000. The DaNeX study of embryonic mesencephalic, dopaminergic tissue grafted to a minipig model of Parkinson’s disease: preliminary findings of effect of MPTP poisoning on striatal dopaminergic markers. Cell Transplantation 9, 247–259.CrossRefGoogle ScholarPubMed
Danielsen, EH, Smith, D, Hermansen, F, Gjedde, A, Cumming, P 2001a. Acute neuroleptic stimulates DOPA decarboxylase in porcine brain in vivo. Synapse 41, 172–175.CrossRefGoogle ScholarPubMed
Danielsen, EH, Smith, DF, Andersen, F, Gee, AD, Bender, D, Hansen, SB, Hermansen, F, Ostergaard, L, Cumming, P, Gjedde, A 2001b. FDOPA metabolism in the adult porcine brain: influence of tracer circulation time and VOI selection on estimates of striatal DOPA decarboxylation. Journal of Neuroscience Methods 111, 157–168.CrossRefGoogle ScholarPubMed
Danielsen, EH, Smith, DF, Gee, AD, Venkatachalam, TK, Hansen, SB, Hermansen, F, Gjedde, A, Cumming, P 1999. Cerebral 6-[(18)F]fluoro-L-DOPA (FDOPA) metabolism in pig studied by positron emission tomography. Synapse 33, 247–258.3.0.CO;2-6>CrossRefGoogle Scholar
Dellman, HD, McClure, RC 1975. Porcine nervous system. The anatomy of domestic animals. W.B. Saunders Co., Philadelphia, USA.Google Scholar
Dickerson, JWT, Dobbing, J 1967. Prenatal and postnatal growth and development of the central nervous system of the pig. Proceedings of the Royal Society – Series B, Biological Sciences 166, 384–395.Google ScholarPubMed
Duhaime, AC, Saykin, AJ, McDonald, BC, Dodge, CP, Eskey, CJ, Darcey, TM, Grate, LL, Tomashosky, P 2006. Functional magnetic resonance imaging of the primary somatosensory cortex in piglets. Journal of Neurosurgery 104, 259–264.Google ScholarPubMed
van Eerdenburg, FJ, Dierx, JA 2002. A new technique for long term, stress free, cannulation of the lateral ventricle in postpubertal, freely moving, pigs. Journal of Neuroscience Methods 121, 13–20.CrossRefGoogle ScholarPubMed
van Eerdenburg, FJ, Swaab, DF, van Leeuwen, FW 1992. Distribution of vasopressin and oxytocin cells and fibres in the hypothalamus of the domestic pig (Sus scrofa). The Journal of Comparative Neurology 318, 138–146.CrossRefGoogle ScholarPubMed
Fang, M, Lorke, DE, Li, J, Gong, X, Yew, JC, Yew, DT 2005. Postnatal changes in functional activities of the pig’s brain: a combined functional magnetic resonance imaging and immunohistochemical study. Neuro-Signals 14, 222–233.CrossRefGoogle Scholar
Fang, M, Li, J, Rudd, JA, Wai, SM, Yew, JC, Yew, DT 2006. fMRI mapping of cortical centers following visual stimulation in postnatal pigs of different ages. Life Sciences 78, 1197–1201.CrossRefGoogle ScholarPubMed
Felix, B, Leger, ME, Albe-Fessard, D, Marcilloux, JC, Rampin, O, Laplace, JP 1999. Stereotaxic atlas of the pig brain. Brain Research Bulletin 49, 1–137.CrossRefGoogle ScholarPubMed
Flynn, TJ 1984. Developmental changes of myelin-related lipids in brain of miniature swine. Neurochemical Research 9, 935–945.CrossRefGoogle ScholarPubMed
Gillian, LA 1943. The nuclear pattern of the nontectal portions of the midbrain and isthmus in ungulates. The Journal of Comparative Neurology 78, 289–364.CrossRefGoogle Scholar
Gizewski, ER, Schanze, T, Bolle, I, de Greiff, A, Forsting, M, Laube, T 2007. Visualization of the visual cortex in minipigs using fMRI. Research in Veterinary Science 82, 281–286.CrossRefGoogle ScholarPubMed
Grate, LL, Golden, JA, Hoopes, PJ, Hunter, JV, Duhaime, AC 2003. Traumatic brain injury in piglets of different ages: techniques for lesion analysis using histology and magnetic resonance imaging. Journal of Neuroscience Methods 123, 201–206.CrossRefGoogle ScholarPubMed
Groth, CG 2007. Prospects in xenotransplantation: a personal view. Transplantation Proceedings 39, 685–687.CrossRefGoogle ScholarPubMed
Grouselle, D, Chaillou, E, Caraty, A, Bluet-Pajot, MT, Zizzari, P, Tillet, Y, Epelbaum, J 2008. Pulsatile cerebrospinal fluid and plasma ghrelin in relation to growth hormone secretion and food intake in the sheep. Journal of Neuroendocrinology 20, 1138–1146.CrossRefGoogle ScholarPubMed
Hofman, MA 1985. Size and shape of the cerebral cortex in mammals. I. The cortical surface. Brain, Behavior and Evolution 27, 28–40.CrossRefGoogle ScholarPubMed
Holm, IE, Geneser, FA, Zimmer, J 1993. Cholecystokinin-, enkephalin-, and substance P-like immunoreactivity in the dentate area, hippocampus, and subiculum of the domestic pig. The Journal of Comparative Neurology 331, 310–325.CrossRefGoogle ScholarPubMed
Holm, IE, West, MJ 1994. Hippocampus of the domestic pig: a stereological study of subdivisional volumes and neuron numbers. Hippocampus 4, 115–125.CrossRefGoogle ScholarPubMed
Imai, H, Konno, K, Nakamura, M, Shimizu, T, Kubota, C, Seki, K, Honda, F, Tomizawa, S, Tanaka, Y, Hata, H, Saito, N 2006. A new model of focal cerebral ischemia in the miniature pig. Journal of Neurosurgery 104, 123–132.Google ScholarPubMed
Ishizu, K, Smith, DF, Bender, D, Danielsen, E, Hansen, SB, Wong, DF, Cumming, P, Gjedde, A 2000. Positron emission tomography of radioligand binding in porcine striatum in vivo: haloperidol inhibition linked to endogenous ligand release. Synapse 38, 87–101.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Jarvinen, MK, Morrow-Tesch, J, McGlone, JJ, Powley, TL 1998. Effects of diverse developmental environments on neuronal morphology in domestic pigs (Sus scrofa). Brain Research, Developmental Brain Research 107, 21–31.CrossRefGoogle ScholarPubMed
Jelsing, J, Rostrup, E, Markenroth, K, Paulson, OB, Gundersen, HJ, Hemmingsen, R, Pakkenberg, B 2005. Assessment of in vivo MR imaging compared to physical sections in vitro – a quantitative study of brain volumes using stereology. NeuroImage 26, 57–65.CrossRefGoogle ScholarPubMed
Jelsing, J, Hay-Schmidt, A, Dyrby, T, Hemmingsen, R, Uylings, HB, Pakkenberg, B 2006. The prefrontal cortex in the Göttingen minipig brain defined by neural projection criteria and cytoarchitecture. Brain Research Bulletin 70, 322–336.CrossRefGoogle ScholarPubMed
Jensen, SB, Smith, DF, Bender, D, Jakobsen, S, Peters, D, Nielsen, EO, Olsen, GM, Scheel-Kruger, J, Wilson, A, Cumming, P 2003. [11C]-NS 4194 versus [11C]-DASB for PET imaging of serotonin transporters in living porcine brain. Synapse 49, 170–177.CrossRefGoogle Scholar
Kirk, EJ, Kitchell, RL, Johnson, RD 1987. Neurophysiologic maps of cutaneous innervation of the hind limb of sheep. American Journal of Veterinary Research 48, 1485–1491.Google ScholarPubMed
Lange, W 1974. Regional differences in the distribution of golgi cells in the cerebellar cortex of man and some other mammals. Cell and Tissue Research 153, 219–226.CrossRefGoogle ScholarPubMed
Larsell, O 1954. The development of the cerebellum of the pig. The Anatomical Record 118, 73–107.CrossRefGoogle ScholarPubMed
Larsen, MO, Rolin, B 2004. Use of the Göttingen minipig as a model of diabetes, with special focus on type 1 diabetes research. ILAR Journal 45, 303–313.CrossRefGoogle Scholar
Larsen, M, Bjarkam, CR, Ostergaard, K, West, MJ, Sorensen, JC 2004. The anatomy of the porcine subthalamic nucleus evaluated with immunohistochemistry and design-based stereology. Anatomy and Embryology (Berlin) 208, 239–247.CrossRefGoogle ScholarPubMed
Laube, T, Schanze, T, Brockmann, C, Bolle, I, Stieglitz, T, Bornfeld, N 2003. Chronically implanted epidural electrodes in Gottinger minipigs allow function tests of epiretinal implants. Graefe’s Archive for Clinical and Experimental Ophthalmology 241, 1013–1019.CrossRefGoogle ScholarPubMed
Leshin, LS, Kraeling, RR, Kiser, TE, Barb, CR, Rampacek, GB 1995. Catecholaminergic region A15 in the bovine and porcine hypothalamus. Brain Research Bulletin 37, 351–358.CrossRefGoogle ScholarPubMed
Lind, NM, Gjedde, A, Moustgaard, A, Olsen, AK, Jensen, SB, Jakobsen, S, Arnfred, SM, Hansen, AK, Hemmingsen, RP, Cumming, P 2005a. Behavioral response to novelty correlates with dopamine receptor availability in striatum of Göttingen minipigs. Behavioural Brain Research 164, 172–177.CrossRefGoogle ScholarPubMed
Lind, NM, Olsen, AK, Moustgaard, A, Jensen, SB, Jakobsen, S, Hansen, AK, Arnfred, SM, Hemmingsen, RP, Gjedde, A, Cumming, P 2005b. Mapping the amphetamine-evoked dopamine release in the brain of the Göttingen minipig. Brain Research Bulletin 65, 1–9.CrossRefGoogle ScholarPubMed
Lind, NM, Moustgaard, A, Jelsing, J, Vajta, G, Cumming, P, Hansen, AK 2007. The use of pigs in neuroscience: modeling brain disorders. Neuroscience & Biobehavioral Reviews 31, 728–751.CrossRefGoogle ScholarPubMed
Lindsay, DB, Setchell, BP 1976. The oxidation of glucose, ketone bodies and acetate by the brain of normal and ketonaemic sheep. The Journal of Physiology 259, 801–823.CrossRefGoogle ScholarPubMed
Marcilloux, JC, Rampin, O, Felix, MB, Laplace, JP, Albe-Fessard, D 1989. A stereotaxic apparatus for the study of the central nervous structures in the pig. Brain Research Bulletin 22, 591–597.CrossRefGoogle Scholar
Mayhew, TM, Mwamengele, GL, Dantzer, V, Williams, S 1996. The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development. Journal of Anatomy 188 (Pt 1), 53–58.Google ScholarPubMed
Mikkelsen, M, Moller, A, Jensen, LH, Pedersen, A, Harajehi, JB, Pakkenberg, H 1999. MPTP-induced Parkinsonism in minipigs: a behavioral, biochemical, and histological study. Neurotoxicology and Teratology 21, 169–175.CrossRefGoogle ScholarPubMed
Minuzzi, L, Nomikos, GG, Wade, MR, Jensen, SB, Olsen, AK, Cumming, P 2005. Interaction between LSD and dopamine D2/3 binding sites in pig brain. Synapse 56, 198–204.CrossRefGoogle ScholarPubMed
Minuzzi, L, Olsen, AK, Bender, D, Arnfred, S, Grant, R, Danielsen, EH, Cumming, P 2006. Quantitative autoradiography of ligands for dopamine receptors and transporters in brain of Göttingen minipig: comparison with results in vivo. Synapse 59, 211–219.CrossRefGoogle ScholarPubMed
Montaurier, C, Morio, B, Bannier, S, Derost, P, Arnaud, P, Brandolini-Bunlon, M, Giraudet, C, Boirie, Y, Durif, F 2007. Mechanisms of body weight gain in patients with Parkinson’s disease after subthalamic stimulation. Brain 130, 1808–1818.CrossRefGoogle ScholarPubMed
Mwamengele, GL, Mayhew, TM, Dantzer, V 1993. Purkinje cell complements in mammalian cerebella and the biases incurred by counting nucleoli. Journal of Anatomy 183 (Pt 1), 155–160.Google ScholarPubMed
Niblock, MM, Kinney, HC, Luce, CJ, Belliveau, RA, Filiano, JJ 2004. The development of the medullary serotonergic system in the piglet. Autonomic Neuroscience 110, 65–80.CrossRefGoogle ScholarPubMed
Niblock, MM, Luce, CJ, Belliveau, RA, Paterson, DS, Kelly, ML, Sleeper, LA, Filiano, JJ, Kinney, HC 2005. Comparative anatomical assessment of the piglet as a model for the developing human medullary serotonergic system. Brain Research, Brain Research Reviews 50, 169–183.CrossRefGoogle Scholar
Okada, Y, Lahteenmaki, A, Xu, C 1999. Comparison of MEG and EEG on the basis of somatic evoked responses elicited by stimulation of the snout in the juvenile swine. Clinical Neurophysiology 110, 214–229.CrossRefGoogle ScholarPubMed
Opdam, HI, Federico, P, Jackson, GD, Buchanan, J, Abbott, DF, Fabinyi, GC, Syngeniotis, A, Vosmansky, M, Archer, JS, Wellard, RM, Bellomo, R 2002. A sheep model for the study of focal epilepsy with concurrent intracranial EEG and functional MRI. Epilepsia 43, 779–787.CrossRefGoogle Scholar
Ostergaard, K, Holm, IE, Zimmer, J 1992. Tyrosine hydroxylase and acetylcholinesterase in the domestic pig mesencephalon: an immunocytochemical and histochemical study. The Journal of Comparative Neurology 322, 149–166.CrossRefGoogle ScholarPubMed
Otabe, JS, Horowitz, A 1970. Morphology and cytoarchitecture of the red nucleus of the domestic pig (Sus scrofa). The Journal of Comparative Neurology 138, 373–389.CrossRefGoogle ScholarPubMed
Palmieri, G, Farina, V, Panu, R, Asole, A, Sanna, L, De Riu, PL, Gabbi, C 1986. Course and termination of the pyramidal tract in the pig. Archives d’Anatomie Microscopique et de Morphologie Expérimentale 75, 167–176.Google ScholarPubMed
Panepinto, LM, Phillips, RW, Wheeler, LR, Will, DH 1978. The Yucatan miniature pig as a laboratory animal. Laboratory Animal Science 28, 308–313.Google ScholarPubMed
Paxinos, G, Watson, C 2006. The rat brain in stereotaxic coordinates. Academic Press, San Diego, CA.Google Scholar
Perlemoine, C, Macia, F, Tison, F, Coman, I, Guehl, D, Burbaud, P, Cuny, E, Baillet, L, Gin, H, Rigalleau, V 2005. Effects of subthalamic nucleus deep brain stimulation and levodopa on energy production rate and substrate oxidation in Parkinson’s disease. British Journal of Nutrition 93, 191–198.CrossRefGoogle ScholarPubMed
Phillips, RW, Panepinto, LM, Spangler, R, Westmoreland, N 1982. Yucatan miniature swine as a model for the study of human diabetes mellitus. Diabetes 31, 30–36.CrossRefGoogle Scholar
Phillips, RJ, Powley, TL 1998. Gastric volume detection after selective vagotomies in rats. American Journal of Physiology 274, R1626–R1638.Google ScholarPubMed
Plogmann, D, Kruska, D 1990. Volumetric comparison of auditory structures in the brains of European wild boars (Sus scrofa) and domestic pigs (Sus scrofa f. dom.). Brain, Behavior and Evolution 35, 146–155.CrossRefGoogle ScholarPubMed
Poceta, JS, Hamlin, MN, Haack, DW, Bohr, DF 1981. Stereotaxic placement of cannulae in cerebral ventricles of the pig. The Anatomical Record 200, 349–356.CrossRefGoogle ScholarPubMed
Ritter, RC 2004. Gastrointestinal mechanisms of satiation for food. Physiology & Behavior 81, 249–273.CrossRefGoogle ScholarPubMed
Rosa-Neto, P, Doudet, DJ, Cumming, P 2004a. Gradients of dopamine D1- and D2/3-binding sites in the basal ganglia of pig and monkey measured by PET. NeuroImage 22, 1076–1083.CrossRefGoogle ScholarPubMed
Rosa-Neto, P, Gjedde, A, Olsen, AK, Jensen, SB, Munk, OL, Watanabe, H, Cumming, P 2004b. MDMA-evoked changes in [11C]raclopride and [11C]NMSP binding in living pig brain. Synapse 53, 222–233.CrossRefGoogle ScholarPubMed
Rosset, A, Spadola, L, Ratib, O 2004. OsiriX: an open-source software for navigating in multidimensional DICOM images. Journal of Digital Imaging 17, 205–216.CrossRefGoogle ScholarPubMed
Sachs, HG, Gekeler, F, Schwahn, H, Jakob, W, Kohler, M, Schulmeyer, F, Marienhagen, J, Brunner, U, Framme, C 2005. Implantation of stimulation electrodes in the subretinal space to demonstrate cortical responses in Yucatan minipig in the course of visual prosthesis development. European Journal of Ophthalmology 15, 493–499.CrossRefGoogle ScholarPubMed
Saito, T, Bjarkam, CR, Nakamura, M, Nemoto, T 1998. Determination of stereotaxic coordinates for the hippocampus in the domestic pig. Journal of Neuroscience Methods 80, 29–36.CrossRefGoogle ScholarPubMed
Sakoh, M, Rohl, L, Gyldensted, C, Gjedde, A, Ostergaard, L 2000a. Cerebral blood flow and blood volume measured by magnetic resonance imaging bolus tracking after acute stroke in pigs: comparison with [(15)O]H(2)O positron emission tomography. Stroke 31, 1958–1964.CrossRefGoogle Scholar
Sakoh, M, Ostergaard, L, Rohl, L, Smith, DF, Simonsen, CZ, Sorensen, JC, Poulsen, PV, Gyldensted, C, Sakaki, S, Gjedde, A 2000b. Relationship between residual cerebral blood flow and oxygen metabolism as predictive of ischemic tissue viability: sequential multitracer positron emission tomography scanning of middle cerebral artery occlusion during the critical first 6 hours after stroke in pigs. Journal of Neurosurgery 93, 647–657.CrossRefGoogle ScholarPubMed
Sakoh, M, Ostergaard, L, Gjedde, A, Rohl, L, Vestergaard-Poulsen, P, Smith, DF, Le Bihan, D, Sakaki, S, Gyldensted, C 2001. Prediction of tissue survival after middle cerebral artery occlusion based on changes in the apparent diffusion of water. Journal of Neurosurgery 95, 450–458.CrossRefGoogle ScholarPubMed
Salinas-Zeballos, ME, Zeballos, GA, Gootman, PM 1986. A stereotaxic atlas of the developing swine (Sus scrofa) forebrain. In Swine in biomedical research (ed. ME Tumbleson), pp. 887–906. Plenum Press, New York, USA.Google Scholar
Sengupta, JN, Gebhart, GF 1994. Gastrointestinal afferent fibers and sensation. In Physiology of the gastrointestinal tract (ed. LR Johnson, DH Alpers, J Christensen, ED Jacobson and JH Walsh), pp. 483–519. Raven Press, New York, USA.Google Scholar
Smith, GPE 1998. Satiation: from gut to brain. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Smith, DF, Poulsen, PH, Ishizu, K, Sakoh, M, Hansen, SB, Gee, AD, Bender, D, Gjedde, A 1998. Quantitative PET analysis of regional cerebral blood flow and glucose and oxygen metabolism in response to fenfluramine in living porcine brain. Journal of Neuroscience Methods 86, 17–23.CrossRefGoogle ScholarPubMed
Solnitzky, J 1938. The thalamic nuclei of Sus scrofa. The Journal of Comparative Neurology 69, 121–169.CrossRefGoogle Scholar
Solnitzky, O 1939. The hypothalamus and subthalamus of Sus scrofa. The Journal of Comparative Neurology 70, 191–229.CrossRefGoogle Scholar
Stephan, H 1951. Vergleichende untersuchungen über den Feinbau des Hirnes von Wild- und Haustieren. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 71, 487–586.Google Scholar
Strain, GM, Tedford, BL, Gill, MS 2006. Brainstem auditory evoked potentials and flash visual evoked potentials in Vietnamese miniature pot-bellied pigs. Research in Veterinary Science 80, 91–95.CrossRefGoogle ScholarPubMed
Sugino, T, Hasegawa, Y, Kurose, Y, Kojima, M, Kangawa, K, Terashima, Y 2004. Effects of ghrelin on food intake and neuroendocrine function in sheep. Animal Reproduction Science 82–83, 183–194.CrossRefGoogle ScholarPubMed
Suk, JY, Thompson, CJ, Labuda, A, Goertzen, AL 2008. Improvement of the spatial resolution of the MicroPET R4 scanner by wobbling the bed. Medical Physics 35, 1223–1231.CrossRefGoogle ScholarPubMed
Szteyn, S, Galert, D, Dynowski, J, Hoczyk, W 1980. The stereotaxic configuration of hypothalamus nerve centres in the pig. Anatomischer Anzeiger 147, 12–32.Google ScholarPubMed
Thorngren-Jerneck, K, Ley, D, Hellstrom-Westas, L, Hernandez-Andrade, E, Lingman, G, Ohlsson, T, Oskarsson, G, Pesonen, E, Sandell, A, Strand, SE, Werner, O, Marsal, K 2001. Reduced postnatal cerebral glucose metabolism measured by PET after asphyxia in near term fetal lambs. Journal of Neuroscience Research 66, 844–850.CrossRefGoogle ScholarPubMed
Vandenbergh, J, Dupont, P, Fischler, B, Bormans, G, Persoons, P, Janssens, J, Tack, J 2005. Regional brain activation during proximal stomach distention in humans: a positron emission tomography study. Gastroenterology 128, 564–573.CrossRefGoogle ScholarPubMed
Watanabe, H, Andersen, F, Simonsen, CZ, Evans, SM, Gjedde, A, Cumming, P 2001. MR-based statistical atlas of the Göttingen minipig brain. NeuroImage 14, 1089–1096.CrossRefGoogle ScholarPubMed
Westerink, BH 1995. Brain microdialysis and its application for the study of animal behaviour. Behavioural Brain Research 70, 103–124.CrossRefGoogle Scholar
Wichmann, T, Delong, MR 2006. Deep brain stimulation for neurologic and neuropsychiatric disorders. Neuron 52, 197–204.CrossRefGoogle ScholarPubMed
Woolsey, CN, Fairman, D 1946. Contralateral, ipsilateral and bilateral representation of cutaneous receptors in somatic areas I and II of the cerebral cortex of pig, sheep and other mammals. Surgery 19, 684–702.Google Scholar
Yelnik, J, Percheron, G 1979. Subthalamic neurons in primates: a quantitative and comparative analysis. Neuroscience 4, 1717–1743.CrossRefGoogle ScholarPubMed
Yoshikawa, T 1968. Atlas of the brains of domestic animals. The brain of the pig. University of Tokyo Press, Tokyo, Japan.Google Scholar
Zieba, DA, Szczesna, M, Klocek-Gorka, B, Molik, E, Misztal, T, Williams, GL, Romanowicz, K, Stepien, E, Keisler, DH, Murawski, M 2008. Seasonal effects of central leptin infusion on secretion of melatonin and prolactin and on SOCS-3 gene expression in ewes. Journal of Endocrinology 198, 147–155.CrossRefGoogle ScholarPubMed