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2013 | 73 | 2 |

Tytuł artykułu

Expression of the calcium-binding proteins in the central, medial and cortical nuclei of the rabbit amygdaloid complex during postnatal development

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
Calbindin-D28k (CB), parvalbumin (PV) and calretinin (CR) are calcium-binding proteins (CaBPs) considered to be markers for certain subpopulations of neurons in the central nervous system. The aim of this study was to describe the pattern of distribution of CB-, PV- and CR-immunoreactive elements in the rabbit corticomedial amygdaloid complex during the postnatal period. The time course of changes in CaBPs expression during maturation of the selected nuclei indicates their diversity. During the first month after birth, CaBPs expression stabilizes earliest in the anterior cortical and then in the medial nuclei. Later, during the second month of postnatal life, the posteromedial and posterolateral cortical nuclei maturate. The central nucleus requires a considerably longer time to reach maturity - about three months are needed to stabilize CaBPs expression in all its subdivisions. This nucleus also shows the most differentiated, time-dependent distribution of CaBPs- immunoreactivity (especially CB), distinct in its divisions. The differences in the CaBPs immunoreactivity confirm previous reports concerning dissimilar origin and development, and also reflect the diversity of connectivity of the amygdaloid body - the collection of nuclei, considered as one functional integrity.

Słowa kluczowe

Wydawca

-

Rocznik

Tom

73

Numer

2

Opis fizyczny

p.260-279,fig.,ref.

Twórcy

autor
  • Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland
autor
  • Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland
  • Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland
autor
  • Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland
  • Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland
autor
  • Department of Anatomy and Neurobiology, Medical University of Gdansk, Gdansk, Poland

Bibliografia

  • Abbott LC, Jacobowitz DM (1999) Developmental expres¬sion of calretinin-immunoreactivity in the thalamic emi¬nence of the fetal mouse. Int J Dev Neurosci 17: 331¬345.
  • Aggleton JP and Saunders RC (2000) The amygdala - what's happened in the last decade? In: The Amygdala. A func¬tional analysis (Aggleton JP, Ed.). Oxford University Press, Oxford, UK. p 1-30.
  • Alheid GF, Heimer L (1988) New perspectives in basal fore- brain organization of special relevance for neuropsychiatry disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27: 1-39.
  • Alheid GF, DeOlmos SJ, Beltramino CA (1995) Amygdala and extended amygdala. In: The Rat Nervous System (Paxinos G, Ed.). Academic Press, San Diego, CA. p. 495-578.
  • Alheid GF (2003) Extended Amygdala and Basal Forebrain.
  • Ann NY Acad Sci 985: 185-205. Amaral DG, Price JL, Pitkanen A, Carmichael ST (1992) Anatomical organisation of the primate amygdaloid com¬plex. In: The Amygdala (Aggleton JP, Ed.). Wiley-Liss, New York, NY. p. 1-66. Andressen C, Blumcke I, Celio MR (1993) Calcium-binding protein: selective markers of nerve cells. Cell Tiss Res 271: 181-208.
  • Ashwell KW, Hardman CD, Paxinos G (2005) Cyto- and chemoarchitecture of the amygdala of a monotreme, Tachyglossus aculeatus (the short-beaked echidna). J Chem Neuroanat 30: 82-104.
  • Barker DA, Dreher B (1998) Spatiotemporal patterns of ontogenetic expression of parvalbumin in the superior col- liculi of rats and rabbits. J Comp Neurol 393: 210-230.
  • Bauman MD, Amaral DG (2005) The distribution of sero¬tonergic fibers in the macaque monkey amygdala: An immunohistochemical study using antisera to 5-hydrok- sytryptamine. Neuroscience 136: 193-203.
  • Bayer SA, Altman J, Russo RJ, Zhang X (1993) Timetables of neurogenesis in the human brain based on experimen¬tally determined patterns in the rat. Neurotoxicology 14: 83-144.
  • Behan M, Haberly LB (1999) Intrinsic and efferent connec¬tions of the endopiriform nucleus in rat. J Comp Neurol 408: 532-548.
  • Berdel B, Morys J (2000) Expression of calbindin-D28k and parvalbumin during development of rat's basolateral amygdaloid complex. Int J Dev Neurosci 18: 501-513.
  • Bernard JF, Alden M, Besson JM (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex - A phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329: 201-229.
  • Brummelte S, Witte V, Teuchert-Noodt G (2007) Postnatal development of GABA and calbindin cells and fibers in the prefrontal cortex and basolateral amygdala of gerbils (Meriones unguiculatus). Int J Dev Neurosci 25: 191¬200.
  • Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, Marty A (2000) Role of the calcium-binding protein par- valbumin in short-term synaptic plasticity. Proc Natl Acad Sci U S A 97: 13372-13377.
  • Camp AJ, Wijesinghe R (2009) Calretinin: modulator of neuronal excitability. Int J Biochem Cell Biol 41: 2118¬2121.
  • Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol 360: 213-245.
  • Carmichael ST, Clugnet MC, Price JL (1994) Central olfac¬tory connections in the macaque monkey. J Comp Neurol 346: 403-434.
  • Cassell MD, Gray TS (1989) Morphology of peptide-immu- noreactive neurons in the rat central nucleus of the amygdala. J Comp Neurol 281: 320-333.
  • Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375-475.
  • Crosby EC, Humphrey T (1941) Studies of the vertebrate telencephalon II. The nuclear pattern of the anterior olfac¬tory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man. J Comp Neurol 74: 309-352.
  • Davern PJ, Head GA (2011) Role of the medial amygdala in mediating responses to aversive stimuli leading to hyper¬tension. Clin Exp Pharmacol Physiol 38: 136-143.
  • Davis M (1992) The role of the amygdala in fear and anxi¬ety. Annu Rev Neurosci 15: 353-375.
  • Davis M (2000) The role of the amygdala in conditioned and unconditioned fear and anxiety. In: The Amygdala, Vol. 2. (Aggleton JP, Ed.). Oxford University Press, Oxford,UK. p 213-287.
  • Dayas CV, Buller KM, Day TA (1999) Neuroendocrine responses to an emotional stressor: evidence for involve¬ment of the medial but not the central amygdala. Eur J Neurosci 11: 2312-2322.
  • de Olmos J, Alheid GF, Beltramino CA (1985) Amygdala. In: The Rat Nervous System (Paxinos G, Ed.). Academic Press, Sydney, AU. p. 223-334.
  • Dong HW, Petrovich GD, Swanson LW (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Rev 38: 192-246.
  • Famiglietti EV, Sundquist SJ (2010) Development of excit¬atory and inhibitory neurotransmitters in transitory cho- linergic neurons, starburst amacrine cells, and GABAergic amacrine cells of rabbit retina, with implications for pre- visual and visual development of retinal ganglion cells. Vis Neurosci 27: 19-42.
  • Fox CA (1940) Certain basal telencephalic centers in the cat. J Comp Neurol 72: 1-62.
  • Frassoni C, Arcelli P, Selvaggio M, Spreafico R (1998) Calretinin immunoreactivity in the developing thalamus of the rat: A marker of early generated thalamic cells. Neuroscience 83: 1203-1214.
  • Frassoni C, Amadeo A, Ortino B, Jaranowska A, Spreafico R (2000) Organization of radial and non-radial glia in the developing rat thalamus. J Comp Neurol 428: 527-542.
  • Girgis M, Shih-Chang W (1981) Stereotaxic Atlas of the Rabbit Brain. Warren H. Green, Inc. ,St. Louis, MO.
  • Gomez DM, Newman SW (1991) Medial nucleus of the amygdala in the adult syrian hamster - A quantitative Golgi analysis of gonadal hormonal regulation of neu¬ronal morphology. Anat Rec 231: 498-509.
  • Guirado S, Real MA, Davila JC (2008) Distinct immunohis- tochemically defined areas in the medial amygdala in the developing and adult mouse. Brain Res Bull 75: 214¬217.
  • Hall J, Parkinson JA, Connor TM, Dickinson A, Everitt BJ (2001) Involvement of the central nucleus of the amygda¬la and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur J Neurosci 13: 1984-1992.
  • Halpern M (1987) The organization and function of the vomeronasal system. Annu Rev Neurosci 10: 325-362.
  • Herdade KC, Strauss CV, Zangrossi Júnior H, Viana MB (2006) Effects of medial amygdala inactivation on a panic-related behavior. Behav Brain Res 172: 316-323.
  • Hewitson L, Lopresti BJ, Stott C, Mason NS, Tomko J (2010) Influence of pediatric vaccines on amygdala growth and opioid ligand binding in rhesus macaque infants: A pilot study. Acta Neurobiol Exp (Wars) 70: 147-164.
  • Hof PR, Glezer II, Condé F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM (1999) Cellular distribution of the calcium binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16: 77-116.
  • Hogan D, Berman NEJ (1993) Transient expression of cal- bindin-D28k immunoreactivity in layer V pyramidal neurons during postnatal development of kitten cortical areas. Dev Brain Res 74: 177-192.
  • Humphrey T (1936) The telencephalon of the bat. I. The non-cortical nuclear masses and certain pertinent fiber connections. J Comp Neurol 65: 603-711.
  • Humphrey T (1968) The development of the human amygdala during early embryonic life. J Comp Neurol 132: 135-166.
  • Humphrey T (1972) The development of the human amygdaloid complex. In: The Neurobiology of the Amygdala (Eleftherion BE, Ed.). Plenum Press, New York, NY. p 21-77.
  • Ito T, Ando H, Handa H (2011) Teratogenic effects of thali¬domide: molecular mechanisms. Cell Mol Life Sci 68: 1569-1579.
  • Jagalska-Majewska H, Dziewiatkowski J, Wojcik S, Luczynska A, Kurlapska R, Morys J (2001) The amygdaloid complex of the rabbit - morphological and histochemical study. Folia Morphol 60: 259-280.
  • Jolkkonen E, Pitkanen A (1998) Intrinsic connections of the rat amygdaloid complex: Projections originating in the central nucleus. J Comp Neurol 395: 53-72.
  • Jones EG, Lensky KM, Chan VH (2001) Delineation of thalamic nuclei immunoreactive for calcium-binding pro¬teins and around the posterior pole of the ventral poste¬rior complex. Thalamus Rel Syst 1: 213-224.
  • Kapp BS, Schwaber JS, Driscoll PA (1985) Frontal cortex projections to the amygdaloid central nucleus in the rab¬bit. Neuroscience 15: 327-346.
  • Kemppainen S, Pitkanen A (2000) Distribution of parvalbu- min, calretinin, and calbindin-D28k immunoreactivity in the rat amygdaloid complex and colocalization with gamma- aminobutyric acid. J Comp Neurol 426: 441-467.
  • Kevetter GA, Winans SS (1981a) Connections of the corti¬comedial amygdala in the golden hamster. I. Efferents of the "ventromedial amygdala". J Comp Neurol 197: 81-98.
  • Kevetter GA, Winans SS (1981b) Connections of the cortico- medial amygdala in the Golden hamster: II. Efferents to the "Olfactory Amygdala". J Comp Neurol 197: 99-111.
  • Komuro H, Rakic P (1996) Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17: 275-285.
  • Krettek JE, Price JL (1978a) A description of the amygdaloid complex in the rat and cat with observations on intra- amygdaloid axonal connections. J Comp Neurol 178: 255-280.
  • Krettek JE, Price JL (1978b) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178: 225¬254.
  • LeDoux JE (2000) Emotion circuits in the brain. Ann Rev Neurosci 23: 155-184.
  • LeDoux JE, Farb CR (1991) Neurons of the acoustic thala¬mus that project to the amygdala contain glutamate. Neurosci Lett 134: 145-149.
  • Legaz I, Olmos L, Real MA, Guirado S, Davila JC, Medina L (2005) Development of neurons and fibers containing calcium binding proteins in the pallial amygdala of mouse, with special emphasis on those of the basolat- eral amygdalar complex. J Comp Neurol 488: 492¬513.
  • Martin SJ, Grimwood PD, Morris RGM (2000) Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711.
  • Martina M, Royer S, Paré D (1999) Physiological properties of central medial and central lateral amygdala neurons. J Neurophysiol 82: 1843-1854.
  • Martinez-Marcos A, Halpern M (1999) Differential projec¬tions from the anterior and posterior divisions of the accessory olfactory bulb to the medial amygdala in the opossum, Monodelphis domestica. Eur J Neurosci 11: 3789-3799.
  • Mascagni F, McDonald AJ, Coleman JR (1993) Corticoamygdaloid and corticocortical projections of the rat temporal cortex: Aphaseolus vulgaris leucoagglutinin study. Neuroscience 57: 697-715.
  • McDonald AJ (1994) Calretinin immunoreactive neurons in the basolateral amygdala of the rat and monkey. Brain Res 667: 238-242.
  • McDonald AJ (1997) Calbindin-D28k immunoreactivity in the rat amygdala. J Comp Neurol 383: 231-244.
  • McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55: 257-332.
  • McDonald AJ, Jackson TR (1987) Amygdaloid connections with posterior insular and temporal cortical areas in the rat. J Comp Neurol 262: 59-77.
  • McDonald AJ, Mascagni F (1996) Cortico-cortical and cor- tico-amygdaloid projections of the rat occipital cortex: A Phaseolus vulgaris leucoagglutinin study. Neuroscience 71: 37-54.
  • McDonald AJ, Betette RL (2001) Parvalbumin-containing neurons in the rat basolateral amygdala: Morphology and co-localization of calbindin-D28k. Neuroscience 102: 413¬425.
  • McDonald AJ, Mascagni F (2001) Colocalization of calci¬um-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105: 681-693.
  • Moon JS, Kim JJ, Chang IY, Chung YY, Jun JY, You HJ, Yoon SP (2002) Postnatal development parvalbumin and calbindin D-28k immunoreactivities in the canine anterior cingulate cortex: transient expression in layer V pyrami¬dal cells. Int J Dev Neurosci 20: 511-519.
  • Morys J, Berdel B, Jagalska-Majewska H, Luczynska A (1999a) The basolateral amygdaloid complex - its devel¬opment, morphology and functions. Folia Morphol (Wars) 58: 29-46.
  • Morys J, Berdel B, Kowianski P, Majak K, Tarnawski M, Wisniewski HM (1999b) Relationship of calcium-binding proteins containing neurons and projective neurons in the rat basolateral amygdala. Neurosci Lett 259: 91-94.
  • Muller JF, Mascagni F, McDonald AJ (2005) Coupled net¬works of parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Neurosci 25: 7366-7376.
  • Newman SW (1999) The medial extended amygdala in male reproductive behavior - A node in the mammalian social behavior network. Ann N Y Acad Sci 877: 242-257.
  • Newman SW (2002) Pheromonal signals access the medial extended amygdala: One node in a proposed social behavior network. In: Mammalian Hormone-Behavior System (Pfaff D, Arnold A, Etgen A, Fahrbach SE, Rubin R, Eds). Academic Press, New York, Ny. p 17-32.
  • Nitsch R, Bergmann I, Kuppers K, Mueller G, Frotscher M (1990) Late appearance of parvalbumin-immunoreactivi- ty in the development of GABAergic neurons in the rat hippocampus. Neurosci Lett 118: 147-150.
  • Novella S, Hines T (2011) Autism and the amygdala: com¬mentary on Hewitson and coauthors (2010) Acta Neurobiol Exp (Wars) 71: 178-179.
  • Paredes J, Winters RW, Schneiderman N, McCabe PM (2000) Afferents to the central nucleus of the amygdala and functional subdivisions of the periaqueductal gray: neuroanatomical substrates for affective behavior. Brain Res 887: 157-173.
  • Parent A, Fortin M, Cote PY, Cicchetti F (1996) Calcium- binding proteins in primate basal ganglia. Neurosci Res 25: 309-334.
  • Petrovich GD, Swanson LW (1997) Projections from the lateral part of the central amygdalar nucleus to the postu¬lated fear conditioning circuit. Brain Res 763: 247-254.
  • Petrovich GD, Canteras NS, Swanson LW (2001) Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Rev 38: 247-289.
  • Pitkanen A (2000) Connectivity of the rat amygdaloid com¬plex. In: The Amygdala: A functional analysis (Aggleton JP, Ed.). Oxford University Press, Oxford, UK. p. 31-115.
  • Pitkanen A, Amaral DG (1993a) Distribution of calbindin- D(28K) immunoreactivity in the monkey temporal lobe: The amygdaloid complex. J Comp Neurol 331: 199-224.
  • Pitkanen A, Amaral DG (1993b) Distribution of parvalbu- min-immunoreactive cells and fibers in the monkey tem¬poral lobe: The amygdaloid complex. J Comp Neurol 331: 14-36.
  • Pitkanen A, Kemppainen S (2002) Comparison of the distri¬bution of calcium-binding proteins and intrinsic connec¬tivity in the lateral nucleus of the rat, monkey, and human amygdala. Pharmacol Biochem Behav 71: 369-397.
  • Pitkanen A, Stefanacci L, Farb CR, Go G-G, LeDoux JE, Amaral DG (1995) Intrinsic connections of the rat amygdaloid complex: Projections originating in the lat¬eral nucleus. J Comp Neurol 356: 288-310.
  • Pitkanen A, Savander V, LeDoux JE (1997) Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 20: 517-523.
  • Price JL, Russchen FT, Amaral DG (1987) The limbic region. II: the amygdaloid complex. In: Handbook of Chemical Neuroanatomy, Vol. 5. Integrated Systems of the CNS (Bjorklund A, Hokfelt T, Swanson LW, Eds). Elsevier, Amsterdam, NL. p. 279-388.
  • Price JL, Slotnick BM, Revial MF (1991) Olfactory projec¬tions to the hypothalamus. J Comp Neurol 306: 447-461.
  • Real MA, Pineda D, Davila JC, Guirado S (2008) Development and adult organization of the lateral part of the bed nucleus of the stria terminalis in the chicken. Brain Res Bull 75: 410-413.
  • Sah P, Faber ES, Lopez DA, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83: 803-834.
  • Salomé N, Viltart O, Leman S, Sequeira H (2001) Activation of ventrolateral medullary neurons projecting to spinal autonomic areas after chemical stimulation of the central nucleus of amygdala: a neuroanatomical study in the rat. Brain Res 890: 287-295.
  • Schierle GS, Gander JC, D'Orlando C, Celio MR, Weisenhorn DM (1997) Calretinin-immunoreactivity during postnatal development of the rat isocortex: A qualitative and quan¬titative study. Cereb Cortex 7: 130-142.
  • Schwaber JS, Kapp BS, Higgins GA, Rapp PR (1982) Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J Neurosci 2:1424-1438.
  • Seo-Hiraiwa ML, Seto-Ohshima A, Kato K (1995) The sur¬face evoked potential and parvalbumin-immunoreactivity in the somatosensory cortex of the developing rat. Dev Psychobiol 28: 337-351.
  • Setzer M, Ulfig N (1999) Differential expression of calbin- din and calretinin in the human fetal amygdala. Microsc Res Tech 46: 1-17.
  • Shek JW, Wen GY, Wisniewski HM (1986) Atlas of the Rabbit Brain and Spinal Cord. Karger, Basel, CH.
  • Shi CJ, Cassell MD (1998) Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399: 440-468.
  • Sidorowicz M, Dziewiatkowski J, Morys J, Berdel B, Maciejewska B, Sloniewski P, Zegarska Z. (1996) Calcium binding proteins in the development of central nucleus of amygdaloid body - a morphometric and immunohistochemical study. Folia Morphol (Warsz) 55: 437-439.
  • Solbach S, Celio MR (1991) Ontogeny of the calcium bind¬ing protein parvalbumin in the rat nervous system. Anat Embryol (Berl) 184: 103-124.
  • Sorvari H, Soininen H, Paljärvi L, Karkola K, Pitkänen A (1995) Distribution of parvalbumin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 360: 185-212.
  • Sorvari H, Soininen H, Pitkänen A (1996a) Calbindin- D28K-immunoreactive cells and fibres in the human amygdaloid complex. Neuroscience 75: 421-443.
  • Sorvari H, Soininen H, Pitkänen A (1996b) Calretinin- immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 369: 188-208.
  • Spitzer NC (1994) Spontaneous Ca2+ spikes and waves in embryonic neurons: signaling systems for differentiation. Trends Neurosci 17: 115-118.
  • Stefanacci L, Amaral DG (2002) Some observations on cor¬tical inputs to the Macaque monkey amygdala: An antero¬grade tracing study. J Comp Neurol 451: 301-323.
  • Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886: 113-164.
  • Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21: 323-331.
  • Uchida Y (1950) A contribution to the comparative anatomy of the amygdaloid nuclei in mammals, especially in rodents. Part II: guinea pig, rabbit and squirrel. Folia Psychiat Neurol Jap 4: 91-107.
  • Urban I, Richard P (1972) A Stereotaxic Atlas of the New Zealand Rabbit's Brain. Charles C. Thomas Publisher LTD, Springfield, IL.
  • Veening JG, Swanson LW, Sawczenko PE (1984) The orga¬nization of projections from the central nucleus of the amygdala to brainstem sites involved in central auto- nomic regulation: A combined retrograde transport-im- munohistochemical study. Brain Res 303: 337-357.
  • Veinante P, Freund-Mercier MJ (1998) Intrinsic and extrin¬sic connections of the rat central extended amygdala: an in vivo electrophysiological study of the central amygdaloid nucleus. Brain Res 794: 188-198.
  • Wells PG, Bhuller Y, Chen CS, Jeng W, Kasapinovic S, Kennedy JC, Kim PM, Laposa RR, McCallum GP, Nicol CJ, Parman T, Wiley MJ, Wong AW (2005) Molecular and biochemical mechanisms in teratogenesis involving reactive oxygen spe¬cies. Toxicol Appl Pharmacol 207 (2 Suppl): 354-366.
  • Wolterbeek A, Waalkens-Berendsen I (2011) Postnatal physical development in juvenile New-Zealand White rabbits. Reprod Toxicol 32: 178-179.
  • Wójcik S, Dziewiatkowski J, Spodnik E, Ludkiewicz B, Kowiański P, Spodnik JH, Morys J (2004a) Distribution of immunoreactivity of calcium-binding proteins in the rabbit piriform cortex. Folia Neuropathol 42: 209-220.
  • Wójcik S, Dziewiatkowski J, Spodnik E, Ludkiewicz B, Domaradzka-Pytel B, Kowiański P, Moryś J (2004b) Analysis of calcium binding protein immunoreactivity in the claustrum and the endopiriform nucleus of the rabbit. Acta Neurobiol Exp (Wars) 64: 449-460.
  • Wójcik S, Spodnik E, Spodnik JH, Dziewiatkowski J, Moryś J (2007) Distribution of neuronal nitric oxide synthase (nNOS)-immunoreactive elements in the rabbit piriform cortex. Folia Morphol (Warsz) 66: 296-302.
  • Yasui Y, Breder CD, Saper CB, Cechetto DF (1991) Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol 303: 355-374.

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