Stimulus-Specific Habituation in Toads: 2DG Studies and Lesion Experiments

  • Thomas Finkenstädt


The innate releasing mechanisms of prey-catching in toads can be modified by experience. The present study sheds light on neural substrates involved in stimulus-specific long-term habituation (non-associative learning). Applying the 14C2-deoxyglucose (2DG) technique, the regional distribution of cerebral glucose utilization was compared between (i) toads after stimulus-specific long-term habituation of orienting toward a repeatedly presented prey dummy (“habituation group”) and (ii) toads readily orienting toward the same prey stimulus (“naive group”). In the habituation group, the caudal ventral medial pallium (vMP) (so-called primordium hippocampi), a portion of the preoptic area (PO), and the dorsal hypothalamus (dHYP) showed statistically significant increases in 2DG-uptake; decreases were observed in the anterior thalamic (A) nucleus, the medioventral layers of the optic tectum (vOT), a portion of the tegmental reticular formation (RET), the striatum (STR), and the ventral cerebellum (vCB). The results suggest that stimulus-specific long-term habituation of prey-catching involves structures of the stimulus-response mediating circuit (e.g., vOT), extrinsic structures belonging to a modulatory circuit (e.g., vMP, RET), and relays connecting both circuits (e.g., PO/dHYP, A). According to Sokolov’s hypothesis it is assumed that habituation leads to stimulus-specific after-effects in the modulatory system which accumulate with repetitive presentation of prey and suppress the response toward prey with reference to specific cues. Bilateral vMP-lesions strongly delay habituation without impairing innate prey recognition. Various brain structures (e.g., vMP, vOT, RET) showed opposite changes in 2DG-uptake during habituation and arousal. The underlying brain circuitries are discussed.


Optic Tectum Medial Septum Anterior Thalamic Nucleus Bufo Bufo Naive Group 
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  1. Altman J, Brunner RL, Bayer SA (1973) The hippocampus and behavioural maturation. Behav Biol 8: 557–596PubMedCrossRefGoogle Scholar
  2. Birukow G, Meng M (1955) Eine neue Methode zur Prüfung des Gesichtssinnes bei Amphibien. Naturwissenschaften 49: 652–653CrossRefGoogle Scholar
  3. Brodai A (1969) Neurological anatomy in relation to clinical medicine. Oxford Univ Press, London Bruner J, Tauc L (1966) Habituation at the synaptic level in Aplysia. Nature 210: 37–39Google Scholar
  4. Campbell BA, Ballantine P, Lynch G (1971) Hippocampal control of behavioral arousal: duration of lesion effects and possible interactions with recovery after frontal cortical damage. Exp Neurol 33(1): 159–170Google Scholar
  5. Chevalier G, Vacher S, Deniau JM (1984) Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behavior. ExpBrain Res 53: 320–326Google Scholar
  6. Chin JH, Killam EK, Killam KF (1965) Factors affecting sensory input in the cat: modification of evoked auditory potentials by reticular formation. Electroenceph Clin Neurophysiol18: 567–574Google Scholar
  7. Diebschlag E (1935) Zur Kenntnis der Großhirnfunktionen einiger Urodelen und Anuren. Z Vergl Physiol 21: 343–394Google Scholar
  8. Douglas RJ, Pribram KH (1966) Learning and limbic lesions. Neuropsychologia 5: 197–220CrossRefGoogle Scholar
  9. Eikmanns KI-1 (1955) Verhaltensphysiologische Untersuchungen über den Beutefang und das Bewegungssehen der Erdkröte (Bufo bufo L). Z Tieipsychol 12: 229–253CrossRefGoogle Scholar
  10. Ewert J-P (1967a) Untersuchungen über die Anteile zentralnervöser Aktionen an der taxispezifischen Ermüdung beim Beutefang der Erdkröte (Bufo bufo L). Z Vergl Physiol 57: 263–298CrossRefGoogle Scholar
  11. Ewert J-P (1967b) Der Einfluß von Störreizen auf die Antwortbereitschaft bei der Richtbewegung der Erdkröte (Bufo bufo L). Z Tiespsychol 24: 208–312Google Scholar
  12. Ewert J-P (1969) Quantitative Analyse von Reiz-Reaktions-Beziehungen bei visuellem Auslösen der Beutefang-Wendereaktion der Erdkröte (Bufo bufo L). Pflügers Arch 308: 225–243PubMedCrossRefGoogle Scholar
  13. Ewert J-P (1974) The neural basis of visually guided behavior. Sci Amer 230: 34–42Google Scholar
  14. Ewert J-P (1980) Neuroethology. An introduction to the neurophysiological fundamentals of behavior. Springer-Verlag, Berlin Heidelberg New YorkGoogle Scholar
  15. Ewert J-P (1984) Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New York, pp 247–416Google Scholar
  16. Ewert J-P (1987a) Neuroethology: toward a functional analysis of stimulus-response mediating and modulating neural circuitries. In: Ellen P, Thinus- Blanc C (eds) Cognitive processes and spatial orientation in animal and man, Vol I. Martinus Nijhoff, Dordrecht, pp 177–200Google Scholar
  17. Ewert J-P (1987b) Neuroethology of releasing mechanisms: prey-catching in toads. Behav Brain Sci 10: 337–405CrossRefGoogle Scholar
  18. Ewert J-P, Birukow G (1965) Über den Einfluß des Zentralnervensystems auf die Ermüdbarkeit der Richtbewegung im Beuteschema der Erdkröte Bufo bufo (L). Naturwissenschaften 52: 68–69CrossRefGoogle Scholar
  19. Ewert J-P, Finkenstädt T (1987) Modulation of tectal functions by prosencephalic loops in amphibians. A commentary. Behav Brain Sci 10: 122–123CrossRefGoogle Scholar
  20. Ewert J-P, Ingle DJ (1971) Excitatory effects following habituation of prey-catching activity in frogs and toads. J Comp Physiol Psycho! 77: 369–374CrossRefGoogle Scholar
  21. Ewert J-P, Kehl W (1978) Configurational prey selection by individual experience in the toad Bufo bufo. J Comp Physiol 126: 105–114CrossRefGoogle Scholar
  22. Ewert J-P, Rehn B (1969) Quantitative Analyse der Reiz-Reaktionsbeziehungen bei visuellem Auslösen des Fluchtverhaltens der Wechselkröte (Bufo vi n rdi s L). Behaviour 35: 212–234CrossRefGoogle Scholar
  23. Finkenstädt T (1987) Verschaltung Interaktion und Funktion visuell beeinflußbarer Hirngebiete bei Amphibien. Habil Thesis, Univ of KasselGoogle Scholar
  24. Finkenstädt T, Ewert J-P (1983) Visual pattern discrimination through interactions of neural networks: a combined electrical brain stimulation, brain lesion, and extracellular recording study in Salamandra salamandra. J Comp Physiol 153: 99–110CrossRefGoogle Scholar
  25. Finkenstädt T, Ewert J-P (1985) Glucose utilization in the toad’s brain during anesthesia and stimulation of the ascending reticular arousal system. Natulwissenschaften72: 161–162Google Scholar
  26. Finkenstädt T, Ewert J-P (1988a) Effects of visual associative conditioning on behavior and cerebral metabolic activity in toads. Naturwissenschaften 75: 95–97PubMedCrossRefGoogle Scholar
  27. Finkenstädt T, Ewert J-P (1988b) Stimulus-specific long-term habituation of visually guided orienting behavior toward prey in toads: a 14C–2DG study. J Comp Physiol 163: 1–11CrossRefGoogle Scholar
  28. Finkenstädt T, Ebbesson SOE, Ewert J-P (1983) Projections to the midbrain tectum in Salamandra salamandra L Cell Tiss Res 234: 39–55Google Scholar
  29. Finkenstädt T, Adler NT, Allen TO, Ebbesson SOE, Ewert J-P (1985) Mapping of brain activity in mesencephalic and diencephalic structures of toads during presentation of visual key stimuli: A computer assisted analysis of (14C)2DG autoradiographs. J Comp Physiol 156: 433–445CrossRefGoogle Scholar
  30. Finkenstädt T, Adler NT, Allen TO, Ewert J-P (1986) Regional distribution of glucose utilization in the telencephalon of toads in response to configurational visual stimuli: a 14C–2DG study. J Comp Physiol 158: 457–467CrossRefGoogle Scholar
  31. Foreman N, Stevens R (1987) Relationships between the superior colliculus and hippocampus: neural and behavioural considerations. Behav Brain Sci 10: 101–152CrossRefGoogle Scholar
  32. Gallistel CR, Piner CT, Allen TO, Adler NT, Yadin E, Negin M (1982) Computer assisted analysis of 2-DG autoradiographs. NeurosciBiobehavRev 6: 409–422Google Scholar
  33. Gonzalez-Lima F (1986) Activation of substantia gelatinosa by midbrain reticular stimulation demonstrated with 2-deoxyglucose in the rat spinal cord. Neuroscr Lett 65: 326–330CrossRefGoogle Scholar
  34. Gonzalez-Lima F, Scheich H (1985) Ascending reticular activating system in the rat: a 2-deoxyglucose study. Brain Res 344: 70–88PubMedCrossRefGoogle Scholar
  35. Groves PM, Thompson RF (1970) Habituation: a dual process theory. Psych Rev 77: 419–450CrossRefGoogle Scholar
  36. Grasser O-J, Grasser-Cornehls U (1976) Neurophysiology of the anuran visual system. In: Llini s R, Precht W (eds) Frog neurobiology. Springer-Verlag, Berlin Heidelberg New York, pp 298–385Google Scholar
  37. Hernandez-Peon R (1961) Reticular mechanisms of sensory control. In: Rosenblith WA (ed) Sensory communication. Wiley, New York, pp 497–520Google Scholar
  38. Herrick CJ (1933) The amphibian forebrain. VIII: Cerebral hemispheres and palliai primordia. J Comp Neurol 58: 737–759CrossRefGoogle Scholar
  39. Hore J, Vilis T (1980) Arm movement performance during reversible basal ganglia lesions in the monkey. Fxp Brain Res 39: 217–228Google Scholar
  40. Horn G (1967) Neuronal mechanisms of habituation. Nature 215: 707–711PubMedCrossRefGoogle Scholar
  41. Horn E, Greiner B, Horn I (1979) The effect of ACTH on habituation of the turning reaction in the toad Bufo bufo L. J Comp Physiol 131: 129–135CrossRefGoogle Scholar
  42. Jarrard LE (1973) The hippocampus and motivation. Psycho! Bull 79: 1–11CrossRefGoogle Scholar
  43. Juliano SL, Whitsel BL (1987) A combined 2-deoxyglucose and neurophysiological study of primate somatosensory cortex. J Comp Neural 263: 514–525CrossRefGoogle Scholar
  44. Kandel E (1976) Cellular basis of behavior: an introduction to behavioral neurobiology. Freeman, New YorkGoogle Scholar
  45. Krasne FB, Kandel ER, Truman JW (1979) Simple systems revisited. Neurosci Res Prog Bull 17 (4): 529–538Google Scholar
  46. Laming PR, McKee M (1981) Deficits in habituation of cardiac arousal responses incurred by telencephalic ablation in Goldfish (Carassius auratus) and their relation to other telencephalic functions. J Comp Physiol Psycho! 95 3: 460–467CrossRefGoogle Scholar
  47. Laming PR, Ennis P (1982) Habituation of fright and arousal responses in the teleosts Carassius auratus and Rutilus rutilus. J Comp Physiol Psycho! 96 3: 460–466CrossRefGoogle Scholar
  48. Lara R, Arbib MA (1985) A model of the neural mechanisms responsible for pattern recognition and stimulus specific habituation in toads. Bio! Cybern 51: 223–237CrossRefGoogle Scholar
  49. Lettvin JY, Maturana HR, Pitts WH, McCulloch WS (1961) Two remarks on the visual system of the frog. In: Rosenblith WA (ed) Sensory communication. MIT Press, Cambridge MA, pp 757–776Google Scholar
  50. Llinâs R, Precht W (1969) Inhibitory vestibular efferents system and its relation to the cerebellum in the frog. amp;p Brain Res 9: 19–29Google Scholar
  51. Masino T, Grobstein P (1986) The organization of tectal projections to the ventral midbrain in Rana pipiens. Soc Neurosci Abstr 84: 11Google Scholar
  52. Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroenceph Clin Neurophysiol 1: 455–473PubMedGoogle Scholar
  53. Nauta WJH (1963) Central nervous organization and the endocrine motor system. In: Nalbandov AV (ed) Advances in neuroendocrinology. Univ Illinois Press, Urbano, pp 5–21Google Scholar
  54. Neary TJ, Northcutt RG (1983) Nuclear organization of the bullfrog diencephalon. J Comp Neurol 213: 262–278PubMedCrossRefGoogle Scholar
  55. Nieuwenhuys R, Opdam P (1976) Structure of the brain stem. In: Llinâs R, Precht W (eds) Frog neurobiology. Springer-Verlag, Berlin Heidelberg New York, pp 811–855CrossRefGoogle Scholar
  56. Northcutt RG, Kicliter E (1980) Organization of the amphibian telencephalon. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. Plenum Press, New York, pp 203–255CrossRefGoogle Scholar
  57. Patton P, Grobstein P (1986) Possible striatal involvement in prey orienting behavior in the frog. Soc Neurosci Abstr 10 (1): 61Google Scholar
  58. Potter HD (1972) Terminal arborizations of retinotectal axons in the bullfrog. J Comp Neural 144: 269–283CrossRefGoogle Scholar
  59. Ramm P, Frost BJ (1983) Regional metabolic activity in the rat brain during sleep-wake activity. Sleep 6: 196–216PubMedGoogle Scholar
  60. Reiner A, Brauth SE, Karten HJ (1984) Evolution of the amniote basal ganglia. TINS 9: 320–325Google Scholar
  61. Ryan AF, Sharp FR (1982) Localization of (3H)2-deoxyglucose at the cellular level using freeze-dried tissue and dry-looped emulsion. Brain Res 252: 177–180PubMedCrossRefGoogle Scholar
  62. Sachs L (1978) Statistische Methoden. Springer-Verlag, Berlin Heidelberg New YorkGoogle Scholar
  63. Satou M, Ewert J-P (1985) The antidromic activation of tectal neurons by electrical stimuli applied to the caudal medulla oblongata in the toad Bufo bufo (L). J Comp Physio! 157: 739–748CrossRefGoogle Scholar
  64. Segundo JP, Arana R, French JD (1955) Behavioral arousal by stimulation of the brain in the monkey. J Neurosurgl 2: 601–613CrossRefGoogle Scholar
  65. Sharp FR, Ryan AF (1984) Regional (14C)2-deoxyglucose uptake during forelimb movements evoked by rat motor cortex stimulation: pons, cerebellum, medulla, spinal cord, and muscle. J Comp Neural 224: 286–306CrossRefGoogle Scholar
  66. Sokoloff L (1984) Modeling metabolic processes in the brain in vivo. Ann Neural Supp! 15: 1–11CrossRefGoogle Scholar
  67. Sokoloff L, Reivich M, Kennedy C, DesRosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The (14C)-deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure and normal values in the conscious and anesthetized albino rat. J Neurochem 28: 897–916PubMedCrossRefGoogle Scholar
  68. Sokolov EN (1960) In: Brazier MAB (ed) The central nervous system and behaviour. Josiah Macy Jun. Foundation, New YorkGoogle Scholar
  69. Sokolov EN (1975) Neuronal mechanisms of the orienting reflex. In: Sokolov EN, Vinogradova O (eds) Neuronal mechanisms of the orienting reflex. Lawrence Erlbaum/Hillsdale, New York, pp 217–235Google Scholar
  70. Székely G, Iazâr G (1976) Cellular and synaptic architecture of the optic tectum. In: Llinâs R, Precht W (eds) Frog neurobiology. Springer-Verlag, Berlin Heidelberg New York, pp 407–434CrossRefGoogle Scholar
  71. Theurich M, Müller CM, Scheich H (1984) 2-deoxyglucose accumulation parallels extracellularly recorded spike activity in the avian auditory neostriatrum. Brain Res 322: 157–161Google Scholar
  72. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neural substrates of behavior. Psych Rev 73: 16–43CrossRefGoogle Scholar
  73. Trepakov VV (1974) Postsynaptic inhibition in the frog’s primordial hippocampus. Neurofiziologia 5: 583–592Google Scholar
  74. Vinogradova O (1970) Registration of information in the limbic system. In: Horn G, Hinde RA (eds) Short term changes in neural activity and behavior. Cambridge University Press, Cambridge, pp 95–140Google Scholar
  75. Vinogradova O (1975) Hippocampus and the orienting reflex. In: Sokolov EN, Vinogradova O (eds) Neuronal mechanisms of the orienting reflex. Lawrence Erlbaum/Hillsdale, New York, pp 128–154Google Scholar
  76. Wilczynski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: an HRP study. J Comp Neurol 173: 219–229CrossRefGoogle Scholar
  77. Wilczynski W, Northcutt RG (1983a) Connections of the bullfrog striatum: afferent organization. J Comp Neural 214: 321–332CrossRefGoogle Scholar
  78. Wilczynski W, Northcutt RG (1983b) Connections of the bullfrog striatum: efferent projections. J Comp Neurol 214: 333–342PubMedCrossRefGoogle Scholar
  79. Zimmermann E, Rahmann H (1987) Acoustic communication in the poison-arrow frog Phyllobates tricolor advertisement calls and their effects on behavior and metabolic brain activity of recipients. J Comp Physiol 160: 693–702CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1989

Authors and Affiliations

  • Thomas Finkenstädt
    • 1
  1. 1.Abteilung Neuroethologie, Fachbereich Biologie/ChemieUniversität KasselKasselFR Germany

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