Abstract
We have previously shown that the morphological compartmentalization of the elasmobranch olfactory bulb is accompanied by a topographical arrangement of the primary olfactory projections onto the bulb. If this spatial arrangement is significant for the processing of the information, one would expect it to be preserved in the secondary olfactory centers of the telencephalon. In this paper, we describe the elasmobranch secondary projections from the olfactory bulb to the telencephalon, focusing on their spatial arrangements within the forebrain. Results show that the olfactory input onto the telencephalon are segregated. The medial olfactory tract projects rostrally onto the superficial layer of the dorsal pallium and onto the lateral pallium. The lateral olfactory tract projects caudally onto the lateral pallium, the striatum and the area superficialis basalis. Thus, the secondary olfactory projections are segregated within the telencephalon, with an overlapping of the secondary fibers in the main projection area, the lateral pallium.
Similar content being viewed by others
References
Adrian ED (1950) Sensory discrimination with some recent evidence from the olfactory organ. Br Med Bull 6:330–333
Ariens-Kappers CU, Huber GC, Crosby EC (1936) The comparative anatomy of the nervous system of vertebrates, including man. Macmillan, New York
Aronson LR (1963) The central nervous system of sharks and bony fishes with special reference to sensory and integrative mechanisms. In: Gilbert PW (ed) Sharks and survival. Heath, Boston, MA, pp 165–241
Astic L, Saucier D, Holley A (1987) Topographical relationship between olfactory receptor cells and glomerular foci in the rat olfactory bulb. Brain Res 424:144–152
Backström K (1924) Contribution to the forebrain morphology in selachians. Acta Zool 5:123–240
Bass AH (1981) Olfactory bulb efferents in the channel catfish, Ictalurus punctatus. J Morphol 169:91–111
Brückmoser P, Dieringer N (1973) Evoked potentials in the primary and secondary olfactory projections areas of the forebrain in Elasmobranchia. J Comp Physiol 87:65–74
Carr CE, Maler L, Sas E (1982) Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211:139–153
Catarelli M, Astic L, Kauer JS (1988) Metabolic mapping of 2-deoxyglucose uptake in the rat piriform cortex using computerized image processing. Brain Res 442:180–184
Compagno LJV (1988) Sharks of the order Carcharhiniforms. Princeton University Press, Princeton
Davis RE, Chase R, Morris J, Kaufman B (1981) Telencephalon of the teleost Macropodus: experimental localization of secondary olfactory areas and of components of the lateral forebrain bundle. Behav Neur Biol 33:257–279
Døving KB, Selset R (1980) Behavioral patterns in the cord released by electrical stimulation of the olfactory tract bundlets. Science 207:559–560
Dryer L, Graziadei PPC (1993) A pilot study of morphological compartmentalization and heterogeneity in the elasmobranch olfactory bulb. Anat Embryol 188:41–51
Dryer L, Graziadei PPC (1994) Mitral cell dendrites: a comparative approach. Anat Embryol 189:91–106
Ebbesson SOE (1972) New insights into the organization of the shark brain. Comp Biochem Physiol A 42:121–129
Ebbesson SOE (1980) On the organization of the telencephalon in elasmobranchs. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. New York, Plenum Press, pp 1–16
Ebbesson SOE, Heimer L (1970) Projections from the olfactory tract fibers in the nurse shark (Ginglymostoma cirratum). Brain Res 17:47–55
Ebbesson SOE, Meyer DL, Scheich H (1981) Connections of the olfactory bulb in the pirhana (Serrasalmus nattereri). Cell Tissue Res 216:167–180
Finger TE (1975) The distribution of the olfactory tract in the bullhead catfish, Ictalurus nebulosus. J Comp Neurol 161:125–141
Freeman WJ (1974) Topographic organization of primary olfactory nerve in cat and rabbit as shown by evoked potentials. Electroencephalogr Clin Neurophysiol 36:33–45
Fujita I, Satou M, Ueda K (1984) A field-potential study of centripetal and centrifugal connections of the olfactory bulb in the carp, Cyprinus carpio (L). Brain Res 321:33–44
Fujita I, Satou M, Ueda K (1988) Morphology of physiologically identified mitral cells in the carp olfactory bulb: a light microscopic study after intracellular staining with horseradish peroxidase. J Comp Neurol 267:253–268
Greer CA, Stewart WB, Kauer JS, Shepherd GM (1981) Topographical and laminar localization of 2-deoxyglucose uptake in rat olfactory bulb induced by electrical stimulation of olfactory nerves. Brain Res 217:279–293
Haberly EB (1990) Olfactory cortex. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford University Press, New York, pp 317–345
Haberly LB, Price JL (1977) The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res 129:152–157
Heiligenberg W, Dye J (1982) Labelling of electroreceptor afferents in a gymnotic fish by intracellular injection of HRP: the mystery of multiple maps. J Comp Physiol 148:287–296
Heimer L (1968) Synaptic distribution of centripetal and centrifugal nerve fibers in the olfactory system of the rat. An experimental anatomical study. J Anat 103:413–432
Holmgren N (1922) Points of view concerning forebrain morphology in lower vertebrates. J Comp Neurol 34:391–459
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol (Lond) 160:106–154
Ichikawa M (1975) The central projections of the olfactory tract in the goldfish, Carassius auratus. J Fac Sci Tokyo Univ, Sec IV, 13:257–263
Ichikawa M, Ueda K (1978) Electron microscopic study of the terminal regions of the olfactory tract fibers in the goldfish telencephalic hemispheres. J Fac Sci Tokyo Univ, Sec IV, 14:127–134
Ichikawa M, Ueda K (1979) Electron microscopic study of the termination of the centrifugal fibers in the goldfish olfactory bulb. Cell Tissue Res 197:257–262
Ito H (1975) Normal and experimental studies on synaptic patterns in the carp telencephalon, with special references to the secondary olfactory termination. J Hirnforsch 14:237–253
Jastreboff PJ, Pedersen PE, Greer CA, Stewart WB, Kauer JS, Benson TE, Shepherd GM (1984) Specific olfactory receptor populations projecting to identified glomeruli in the rat olfactory bulb. Proc Natl Acad Sci USA 81:5250–5254
Johnston JB (1911) The telencephalon of selachians. J Comp Neurol 21:1–113
Kaas JH, Nelson RJ, Sur M, Lin CS, Merzenich MM (1979) Multiple representations of the body within the primary somatosensory cortex of primates. Science 204:521–523
Kemali M, Guglielmotti V (1987) A horseradish peroxidase study of the olfactory system of the frog, Rana esculenta. J Comp Neurol 263:400–417
Lancet D, Greer CA, Kauer JS, Shepherd GM (1982) Mapping of odor-related neuronal activity in the olfactory bulb by high-resolution 2-deoxyglucose autoradiography. Proc Natl Acad Sci USA 79:670–674
Land LJ, Shepherd GM (1974) Autoradiographic analysis of olfactory receptor projections. Brain Res 70:506–510
Le Gros Clark WE (1951) The projections of the olfactory epithelium on the olfactory bulb in the rabbit. J Neurol Neurosurg Psychiatry 14:1–10
Levine RL, Dethier S (1985) The connections between the olfactory bulb and the brain in the goldfish. J Comp Neurol 237:427–444
Lohman AHM, Mentik GM (1969) The lateral olfactory tract, the anterior commissure, and the cells of the olfactory bulb. Brain Res 12:396–413
Lund JS (1988) Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci 11:253–288
Manley GA, Koppl C, Konishi M (1988) A neural map of interaural intensity differences in the brain stem of the barn owl. J Neurosci 8:2665–2676
Masino T, Grobstein P (1990) Tectal connectivity in the frog Rana pipiens: tectotegmental projections and a general analysis of topographic organization. J Comp Neurol 291:103–127
Merzenich MM, Reid MD (1974) Representation of the cochlea within the inferior colliculus of the cat. Brain Res 77:397–415
Murakami T, Morita Y, Ito H (1933) Extrinsic and intrinsic fiber connections of the telencephalon in a teleost, Sebasticus marmoratus. J Comp Neurol 216:115–131
Nieuwenhuys R (1967) Comparative anatomy of olfactory centers and tracts. Progr Brain Res 23:1–63
Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am Zool 17:411–429
Northcutt RG (1978) Brain organization in the cartilaginous fishes. In: Hodgson ES, Mathewson RF (eds): Sensory biology of sharks, skates, and rays. Office to Naval Research, Arlington, VA, pp 117–193
Northcutt RG (1981) Evolution of the telencephalon in non-mammals. Annu Rev Neurosci 4:301–305
Northcutt RG (1985) Efferent projections of the olfactory bulb in the Pacific hagfish. Am Zool 25:106A
Northcutt RG, Pudrowski RL (1988) Projections of the olfactory bulb and nervus terminalis in the Silver lamprey. Brain Behav Evol 32:96–107
Oka Y (1980) The origin of the centrifugal fibers to the olfactory bulb in the goldfish, Carassius auratus: an experimental study using the fluorescent dye primuline as a retrograde tracer. Brain Res 185:215–225
Penfield W, Rasmussen T (1950) The cerebral cortex of man: a clinical study of localization of function. Macmillan, New York
Polenova OA, Vesselkin NP (1993) Olfactory and nonolfactory projections in the River lamprey (Lampetra fluviatilis) telencephalon. J Hirnforsch 34:261–279
Price JL (1987) The central olfactory and accessory olfactory systems. In: Finger TE, Silver WL (eds) Neurobiology of taste and smell. Wiley, New York, pp 179–203
Price JL, Powell TPS (1971) Certain observations on the olfactory pathway. J Anat 110:105–126
Rooney D, Døving KB, Ravaille-Veron M, Szabo T (1992) The central connections of the olfactory bulbs in Cod, Gadus Morhua L. J Hirnforsch 33:63–75
Satou M, Ichikawa M, Ueda K, Tagaki SF (1979) Topographical relation between olfactory bulb and olfactory tracts in the carp. Brain Res 173:142–146
Satou M, Fujita I, Ichikawa M, Yamaguchi K, Ueda K (1983) Field potential and intracellular potential studies of the olfactory bulb in the carp: evidence for a functional separation and the olfactory bulb into lateral and medial subdivisions. J Comp Physiol 152:319–333
Scalia F, Ebbesson SOE (1971) The central projections of the olfactory bulb in a teleost (Gymnothorax funebris). Brain Behav Evol 4:376–399
Schoenfeld TA, Marchand JE, Macrides F (1985) Topographical organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J Comp Neurol 235:503–518
Schwob JE, Price JL (1984) The development of lamination of afferent fibers to the olfactory cortex in rats, with additional observations in the adult. J Comp Neurol 223:203–222
Sheldon RE (1912) The sense of smell in selachians. J Exp Zool 10:51–61
Sicard G, Royet JP, Jourdan F (1989) A comparative study of the 2-deoxyglucose patterns of glomerular activation in the olfactory bulb of C57BL/6J and AKR/J mice. Brain Res 481:325–334
Skeen LC, Hall WC (1977) Efferent projections of the main and accessory olfactory bulb in the tree shrew (Tupaia glis). J Comp Neurol 172:1–36
Smeets WJAJ (1983) The secondary olfactory connections in two Chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 218:334–344
Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes. Springer, Berlin Heidelberg New York, pp 123–148
Switzer RC, Olmos J de, Heimer L (1985) Olfactory system. In: Paxinos G (ed) The rat nervous system: forebrain and midbrain. Academic Press, Sidney, pp 1–36
Von Bartheld CS, Meyer DL, Fiebig E, Ebbesson SOE (1984) Central connections of the olfactory bulb in the goldfish, Carrasius auratus. Cell Tissue Res 238:475–487
White EL (1965) Olfactory bulb projections in the rat. Anat Rec 152:465–480
Wicht H, Northcutt RG (1993) Secondary olfactory projections and pallial topography in the Pacific hagfish, Eptapterus stouti. J Comp Neurol 337:529–542
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Dryer, L., Graziadei, P.P.C. Projections of the olfactory bulb in an elasmobranch fish, Sphyrna tiburo: segregation of inputs in the telencephalon. Anat Embryol 190, 563–572 (1994). https://doi.org/10.1007/BF00190106
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00190106