Habituation: Events in the history of its characterization and linkage to synaptic depression. A new proposed kinetic criterion for its identification

Progress in Neurobiology

Volumn 53, Issue 1, 1997, Pages 45-66

  Christoffersen, G R J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; NORADRENALIN; OPIATE; PROTEIN; PUROMYCIN;

DIENCEPHALON; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; EXCITATORY POSTSYNAPTIC POTENTIAL; HABITUATION; HELIX POMATIA; HUMAN; KINETICS; LEARNING; NEUROCHEMISTRY; NOMENCLATURE; NONHUMAN; NYSTAGMUS; PRIORITY JOURNAL; REFLEX; REVIEW; SYNAPSE; TELENCEPHALON;

ANIMALS; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; KINETICS; MODELS, NEUROLOGICAL; SYNAPSES;

EID: 0030843110     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(97)00031-2     Document Type: Review

References (138)

1. Abels, H. (1906) Über Nachempfindung im Gebiete der kinästhetischen und statischen Sinnes. Ein Beitrag zur Lehre von Bewegungsschwindel (Drehschwindel). Psychol. und Physiol. der Sinnesorgane. I. Abteilung. Zeitschrift für Psychologie 43, 268-289 and 374-422.
2. Ammassari-Teule, M., Fagioli, S. and Rossi-Arnaud, C. (1994) Radial maze performance and open-field behaviours in aged C57BL/6 mice: further evidence for preserved cognitive abilities during senescence. Physiol. Behav. 55, 341-345.
3. Appleton, T. and Wilkens, J. L. (1990) Habituation, sensitization and the effect of serotonin on the eyestalk withdrawal reflex of Cancer magister. Comp. Biochem. Physiol. 97A, 159-163.
4. Aviation Medicine in the A. E. F. War Department (1920) Washington, DC. Cited by Mowrer (1934).
5. Bailey, C. H., Castellucci, V. F., Koester, J. and Chen, M. (1953) Behavioural changes in ageing Aplysia: a model system for studying the cellular basis of age-impaired learning, memory and arousal. Behav. Neural Biol. 38, 70-81.
6. Bailey, C. H. and Chen, M. (1983) Morphological basis of long-term habituation and sensitization in Aplysia. Science 220, 91-93.
7. Bailey, C. H. and Chen, M. (1988a) Morphological basis of short-term habituation in Aplysia. J. Neurosci. 8, 2452-2459.
8. Bailey, C. H. and Chen, M. (1988b) Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc. natn. Acad. Sci. U.S.A. 85, 9356-9359.
9. Bárány, R. (1907) Weitere Untersuchungen über den vom Vestibularapparat des Ohres reflektorisch ausgelösten rhythmischen Nystagmus und seine Begleiterscheinungen. Monatsschr. f. Ohrenhk XLI, 477-526.
10. Barrass, R. (1961) A quantitative study of the behaviour of the male Mormoniella vitripennis (Walker) (Hymenoptera, Pleromalidae) towards two constant stimulus situations. Behaviour 18, 288-312.
11. Beck, C. D. O. and Rankin, C. H. (1993) Effects of aging in the nematode Caenorhabditis elegans. Behav. Proc. 28, 145-164.
12. Beritoff, J. (1926) Über die individuell erworbene Tätigkeit des Zentralnervensystems bei Tauben. Pflüg. Arch. ges. Physiol. Mensch. Tiere 213, 370-406.
13. Bicker, G. and Haehnlein, I. (1994) Long-term habituation of an appetitive reflex in the honeybee. NeuroReport 6, 54-56.
14. Brodfuehrer, P. D., Debski, E. A., O'Gara, B. A. and Friesen, W. O. (1995) Neural control of leech swimming. J. Neurobiol. 27, 403-418.
15. Bruner, J. and Kehoe, J. (1970) Long-term decrements in the efficacy of synaptic transmission in molluscs and crustaceans. In: Short-term Changes in Neural Activity and Behaviour, pp. 323-359. Eds G. Horn and R. A. Hinde. Cambridge University Press: U.K.
16. Byrne, J., Castellucci, V. and Kandel, E. R. (1974) Receptive fields and response properties of mechanoreceptor neurons innervating siphon and mantle shelf in Aplysia. J. Neurophysiol. 37, 1041-1064.
17. Callec, J. J., Guillet, J. C., Pichon, Y. and Boistel, J. (1971) Further studies on synaptic transmission in insects. II: relations between sensory information and its synaptic integration at the level of a single giant axon in the cockroach. J. Expl Biol. 55, 123-149.
18. Carew, T. J. and Kandel, E. R. (1973) Acquisition and retention of long-term habituation in Aplysia. Science 182, 1158-1160.
19. Carew, T. J., Pinsker, H. M. and Kandel, E. R. (1972) Long term habituation of a defensive withdrawal reflex in Aplysia. Science 175, 451-454.
20. Castellucci, T. J. and Kandel, E. R. (1974) A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. natn. Acad. Sci. U.S.A. 71, 5004-5008.
21. Castellucci, V. F., Pinsker, H., Kupfermann, I. and Kandel, E. R. (1970) Neuronal mechanisms of habituation and dishabituation of the gill withdrawal reflex in Aplysia. Science 167, 1745-1748.
22. Cheever, L. and Koshland, D. E. Jr (1992) Retention of habituation in PC12 cells. Proc. natn. Acad. Sci. U.S.A. 89, 10084-10088.
23. Cheever, L. and Koshland, D. E. Jr (1994) Habituation of neurosecretory responses to extracellular ATP in PC12 cells. J. Neurosci. 14, 4831-4838.
24. Chow, K. L. and Leiman, A. L. (1971) The photo-sensitive organs of crayfish and brightness learning. Behav. Biol. 7, 25-35.
25. Christoffersen, G. R. J. (1992a) The kinetics of homosynaptic short-term depression in cell RPa3 of Helix pomatia depends upon the level of activation prior to depression. Comp. Biochem. Physiol. 101A, 221-227.
26. Christoffersen, G. R. J. (1992b) Habituation of the tentacle reflex of Helix pomatia is cancelled at specific stimulus intervals present during spatial orientation. Proc. 5th Conf. Neurobiol. Learning and Memory, p. 35. University of California at Irvine.
27. Christoffersen, G. R. J. (1992c) Anomalous frequency dependency of reflex habituation and synaptic depression in the tentacle of Helix pomatia. Eur. J. Neurosci. Suppl. 5, 73.
28. Christoffersen, G. R. J., Frederiksen, K., Johansen, J., Kristensen, B. I. and Simonsen, L. (1980) Behavioural modification of the optic tentacle of Helix pomatia; effect of puromycin, activity of S-100. Comp. Biochem. Physiol. 68A, 611-624.
29. Christoffersen, G. R. J. and Juel, C. (1979) Synaptic depression in Helix pomania I: a presynaptic model. Comp. Biochem. Physiol. 62A, 611-619.
30. Christoffersen, G. R. J. and Nielsen, L. E. (1991) Properties of the transition from short-term to long-term depression in neurons of Helix pomatia. Comp. Biochem. Physiol. 100A, 407-412.
31. Christoffersen, G. R. J. and Schilhab, T. S. S. (1996) Synaptic long-term depression alters recovery from, and frequency dependency of, short-term depression in Helix pomatia. Neuroscience 73, 1009-1016.
32. Clark, R. B. (1966) The integrative action of a worm's brain. Symp. Soc. Expl Biol. 20, 345-379.
33. Clayton, F. L. and Hinde, R. A. (1968) The habituation and recovery of aggressive display in Bella splendens. Behaviour 30, 96-106.
34. Cleary, L. J., Byrne, J. H. and Frost, W. N. (1995) Role of interneurons in defensive withdrawal reflexes in Aplysia. Learn. Memory 2, 133-151.
35. Coombs, C. H. (1938) Adaptation of the galvanic response to auditory stimulation. J. Expl Biol. 22, 244-268.
36. Csanyi, V. (1985) Ethological analysis of predator avoidance by the paradise fish (Macropodus opercularis L.) 1. Recognition and learning of predators. Behaviour 92, 227-240.
37. Csanyi, V., Csizmadia, G. and Miklosi, A. (1989) Long-term memory and recognition of another species in the paradise fish. Anim. Behav. 37, 908-911.
38. D'Alessio, G., Di Donato, A., Jaffé, K., Maldonado, H. and Zabala, N. A. (1982) Arginine and memory consolidation in praying mantis. J. Comp. Physiol. 147A, 231-235.
39. Davis, R. C. (1934) Modification of the galvanic skin reflex by daily repetition of a stimulus. J. Expl Psychol. XVII, 504-535.
40. Davis, M., Gendelman, D. S., Tischler, M. D. and Gendelman, P. M. (1982) A primary acoustic startle curcuit: lesion and stimulation studies. J. Neurosci. 2, 791-805.
41. Delorenzi, A., Pedreira, M. E., Romano, A., Pirola, C. J., Nahmod, V. E. and Maldonado, H. (1995) Acute administration of angiotensin II improves long-term habituation in the crab Chasmagnathus. Neurosci. Lett. 196, 193-196.
42. Dimant, B. and Maldonado, H. (1992) Habituation and associative learning during explorative behaviour of the crab Chasmagnathus. J. Comp. Physiol. 170, 749-759.
43. Dodge, R. (1923) Habituation to rotation. J. Expl Psychol. 6, 1-35.
44. Ebbinghaus, H. (1885) Über das Gedächtnis. Leipzig: Dunker.
45. Ennaceur, A. and Delacour, J. (1987) Effect of combined or separate administration of piracetam and choline on learning and memory in the rat. Psychopharmacology 92, 58-67.
46. Farel, P. B. (1971) Long-lasting habituation in spinal frogs. Brain Res. 33, 405-417.
47. Farel, P. B., Glanzman, D. L. and Thompson, R. F. (1973) Habituation of a monosynaptic response in vertebrate central nervous system: Lateral column-motorneuron pathway in isolated frog spinal cord. J. Neurophysiol. 36, 1117-1130.
48. Fisher, L. (1917) Vertigo: its causes and method of diagnosis. Am. J. Surg. XXXI, 67-70.
49. Gingrich, K. J. and Byrne, J. H. (1985) Simulation of synaptic depression, posttetanic potentiation and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J. Neurophysiol. 53, 652-669.
50. Glaser, E. M. and Griffin, J. P. (1962) Influence of the cerebral cortex on habituation. J. Physiol. 160, 429-445.
51. Glaser, E. M. and Whittow, G C. (1957) Retention in a warm environment of adaptation to localised cooling. J. Physiol. 136, 98-111.
52. Griffin, J. P. (1963) The role of the frontal cortex upon habituation in man. Clin. Sci. 24, 127-134.
53. Griffin, J. P. (1970) Neurophysiological studies into habituation. In: Short-term Changes in Neural Activity and Behaviour, pp. 141-179. Eds G. Horn and R. A. Hindepp. Cambridge University Press: U.K.
54. Griffin, J. P. and Pearson, J. A. (1967) Habituation of the flexor reflex in the rat. J. Physiol. 190, 3-5.
55. Griffin, J. P. and Pearson, J. A. (1968a) The effect of lesions of the frontal areas of the cerebral cortex on habituation of the flexor withdrawal response in the rat. Brain Res. 8, 177-180.
56. Griffin, J. P. and Pearson, J. A. (1968b) The effect of bladder extension on habituation of the flexor withdrawal reflex in the decerebrate cat. Brain Res. 8, 185-192.
57. Griffith, C. R. (1920a) The organic effects of repeated bodily rotation. J. Expl Psychol. III, 15-46.
58. Griffith, C. R. (1920b) The effect upon the white rat of continued bodily rotation. Am. Natur. 54, 524-534.
59. Groves, P. M. and Thompson, R. F. (1970) Habituation: a dual-process theory. Psychol. Rev. 77, 419-450.
60. Guttich, A. (1914) Beitrag zur Physiologie des Vestibularapparates. Passow-Schaf. Beitr. Anat. Physiol. VII, 1-18.
61. Gwilliam, G. F. (1969) Electrical responses to photic stimulation in the eyes and nervous system of nereid polychaetes. Biol. Bull. 136, 385-397.
62. Hagbarth, K. E. and Kugelberg, E. (1958) Plasticity of the human skin reflex. Brain 81, 305-318.
63. Harris, J. D. (1943) Habituatory response decrement in the intact organism. Psychol. Bull. 40, 385-422.
64. Hernandez-Peon, R., Jouvet, M. and Scherrer, H. (1957) Auditory potentials at the cochlear nucleus during acoustic habituation. Acta Neurol. Latinoam. 3, 144-156.
65. Hinde, R. A. (1954) Factors governing the changes in strength of a partially inborn response, as shown by the mobbing behaviour of the chaffinch (Fringilla coelebs). II. The waning of the response. Proc. R. Soc. Lond. (B) 142, 331-358.
66. Hinde, R. A. (1970) Behavioural habituation. In: Short-term Changes in Neural Activity and Behaviour, pp. 3-40. Eds G. Horn and R. A. Hinde. Cambridge University Press: U.K.
67. Hochner, B., Braha, O., Klein, M. and Kandel, E. R. (1986a) Distinct processes in presynaptic facilitation contribute to sensitization and dishabituation in Aplysia: possible involvement of C kinase in dishabituation. Soc. Neurosci. Abstr. 12, 1340.
68. Hochner, B., Klein, M., Schacher, S. and Kandel, E. R. (1986b) Additional component in the cellular mechanism of presynaptic facilitation contributes to behavioural dishabituation in Aplysia. Proc. natn. Acad. Sci. U.S.A. 83, 8794-8798.
69. Hood, J. D. and Pfaltz, C. R. (1954) Observations upon the effects of repeated stimulation upon rotational and caloric nystagmus. J. Physiol. 124, 130-144.
70. Horridge, G. (1959) Analysis of the rapid response of Nereis and Harmonthoe (Annelida). Proc. R. Soc. (B) 150, 245-262.
71. Huber, F. (1965) Brain controlled behaviour in Orthopterans. In: The Physiology of the Insect Central Nervous System, pp. 79-112. Eds J. E. Treherne and J. W. Beament. Academic Press: NY.
72. Humphrey, G. (1933) The Nature of Learning in its Relation to the Living System. Kegan, Trench, Trubner: London.
73. Huntingford, F. A. and Coulter, R. M. (1989) Habituation of predator inspection in the three-spined stickleback, Gasterosteus aculeatus L.. J. Fish Biol. 35, 153-154.
74. Johnson, M. C. and Wuensch, K. L. (1994) An investigation of habituation in the jellyfish Aurelia aurita. Behav. Neural Biol. 61, 54-59.
75. Juel, C. and Christoffersen, G. R. J. (1979) Synaptic depression in Helix pomatia: II. Temperature and ion dependency. Comp. Biochem. Physiol. 62A, 621-626.
76. Kandel, E. R. (1976) Cellular Basis of Behaviour. An Introduction to Behavioural Neurobiology. W. H. Freeman and Co.: San Francisco.
77. Karni, A., Meyer, G., Jezzard, P., Adams, M. M., Turner, R. and Ungerleider, L. G. (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155-158.
78. Kimmel, H. D. and Goldstein, A. J. (1967) Retention of habituation of the GSR to visual and auditory stimulation. J. Expl Psychol. 73, 401-404.
79. King, B. G. (1926) The influence of repeated rotations on decerebrate and on blinded squabs. J. Comp. Psychol. 6, 399-421.
80. 2+ current. J. Expl Biol. 89, 117-157.
81. Kozak, W., McFarlane, M. B. and Westerman, R. (1962) Long lasting reversible changes in the reflex responses of chronic spinal cats to touch, heat and cold. Nature 193, 171-173.
82. Krasne, F. B. (1969) Excitation and habituation of the crayfish escape reflex: the depolarizing response in lateral giant fibers of the isolated abdomen. J. Expl Biol. 50, 29-46.
83. Krasne, F. B. and Teshiba, T. M. (1995) Habituation of an invertebrate escape reflex due to modulation by higher centers rather than local events. Proc. natn. Acad. Sci. U.S.A. 92, 3362-3366.
84. Krasne, F. B. and Woodsmall, K. S. (1969) Waning of the crayfish escape response as a result of repeated stimulation. Anim. Behav. 17, 416-424.
85. Kuczka, H. (1956) Verhaltenphysiologische Untersuchungen über die Wishhandlung der Erdkröte (Bufu bufo L.). Z. Tierpsychol. 13, 185-207.
86. Kuenzer, P. (1958) Verhaltenphysiologische Untersuchungen über das Zucken des Regenwurms. Z. Tierpsychol. 13, 185-207.
87. Kupfermann, I., Castelluci, V., Pinsker, H. and Kandel, E. R. (1970) Neuronal correlates of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167, 1743-1745.
88. Laming, P. R. and Ennis, P. (1982) Habituation of fright and arousal responses in the teleosts Carassius auratus and Rutilus rutilus. J. Comp. Physiol. Psychol. 96, 460-466.
89. Leaton, R. N., Casella, J. V. and Borszcz, G. S. (1985) Short-term and long-term habituation of the acoustic startle response in chronic decerebrate rats. Behav. Neurosci. 99, 901-912.
90. Lehner, G. F. J. (1941) A study of the extinction of unconditioned reflexes. J. Expl Psychol. 29, 435-455.
91. Lumpkin, R. C. (1927) Post-rotation nystagmus in the rabbit with head fixed and head free. J. Comp. Physiol. VII, 181-185.
92. Macphail, E. M. (1993) The Neuroscience of Animal Intelligence. Columbia University Press: NY.
93. Maldonado, H., Romano, A. and Lozada, M. (1989) Opioid action on response level to a danger stimulus in the crab (Chasmagnathus granulatus). Behav. Neurosci. 103, 1139-1143.
94. Manual of the Medical Research Laboratory (1920) War Department, Washington, DC. Cited by Mowrer (1934).
95. Marcus, E. A., Nolan, T. G., Rankin, C. H. and Carew, T. J. (1988) Behavioural dissociation of dishabituation, sensitization and inhibition in Aplysia. Science 241, 210-213.
96. Martin, P. T. and Koshland, D. E. (1992) Regulation of neurosecretory habituation in PC12 cells: parallel pathways used by cAMP and calcium. Proc. natn. Acad. Sci. U.S.A. 89, 10257-10261.
97. Maxwell, S. S., Burke, V. L. and Reston, C. (1922) The effect of repeated rotation on the duration of after-nystagmus in the rabbit. Am. J. Physiol. LVIII, 432-438.
98. Mogensen, J. (1990) Influences of the rearing conditions on functional properties of the rat's prefrontal system. Behav. Brain Res. 42, 135-142.
99. Mogensen, J. and Holm, S. (1994) The prefrontal cortex and variants of sequential behaviour: indications of functional differentiation between subdivisions of the rat's prefrontal cortex. Behav. Brain. Res. 63, 89-100.
100. Mowrer, O. H. (1934) The modification of vestibular nystagmus by means of repeated elicitation. Comp. Psychol. Monogr. IX, 1-48.
101. Nesmeianova, T. N. (1957) The inhibition of the motor reflex in spinal dogs under conditions of chronic experimentation. Sechen. Physiol. J. U.S.S.R. 43, 281-288.
102. Parsons, R. P. and Segar, L. H. (1918) Barany chair tests and flying ability. J. Am. Med. Assoc. 70, 1064-1065.
103. Pavlov, I. P. (1927) Conditioned Reflexes. Oxford University Press: U.K.
104. Pavlov, I. P. (1928) Lectures on Conditioned Reflexes. International Publishers: NY.
105. Peckham, G. W. and Peckham, E. G. (1887) Some observations on the mental powers of spiders. J. Morphol. 1, 383-419.
106. Pieron, H. (1913) Recherches experimentales sur les phénomènes de memoire. Ann. Psychol. 19, 91-193.
107. Pilz, G. F. (1926) On the relation of the after-nystagmus to rotation-nystagmus. Am. J. Physiol. LXXVII, 428-458.
108. Pinsker, H., Kupfermann, I., Castelluci, V. and Kandel, E. R. (1970) Habituation and dishabituation of the gill withdrawal reflex in Aplysia. Science 167, 1740-1742.
109. Prosser, C. L. and Hunter, W. S. (1936) The extinction of startle responses and spinal reflexes in the white rat. Am. J. Physiol. 117, 609-618.
110. Rankin, C. H., Beck, C. D. O. and Chiba, C. M. (1990) Caenorhabditis elegans: a new model system for the study of learning and memory. Behav. Brain Res. 37, 89-92.
111. Rankin, C. H. and Carew, T. J. (1988) Dishabituation and senshization emerge as separate processes during development in Aplysia. J. Neurosci. 8, 197-211.
112. Rayport, S. G. and Camardo, J. S. (1984) Differential emergence of cellular mechanisms mediating habituation and sensitization in the developing Aplysia nervous system. J. Neurosci. 4, 2528-2532.
113. Rayport, S. G. and Schacher, S. (1986) Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization. J. Neurosci. 6, 759-763.
114. Riedel, G. (1994) Computer-assisted shock-reinforced Y-maze training: a method for studying spatial alternation behaviour. NeuroReport 5, 2061-2064.
115. Roberts, M. B. V. (1962) The giant fibre reflex of the earthworm, Lumbricus terrestris. II. Fatigue. J. Expl Biol. 39, 229-237.
116. Ruppert, J. (1906) Untersuchungen über den Drehnystagmus. Zentr. Blatt inn. Med. XXVII, 465-478.
117. Russell, E. M. (1967) Changes on the behaviour of Lebistes reticulatus upon a repeated shadow stimulus. Anim. Behav. 15, 574-585.
118. Schilhab, T. S. S. and Christoffersen, G. R. J. (1996) Role of protein synthesis in the transition from synaptic short-term to long-term depression in neurons of Helix pomatia. Neuroscience 73, 999-1007.
119. Schlapfer, W. T., Woodson, P. B. J., Tremblay, J. P. and Barondes, S. H. (1974) Depression and frequency facilitation at a synapse in Aplysia californica: evidence for regulation by availability of transmitter. Brain Res. 76, 267-280.
120. Sharpless, S. and Jasper, H. (1956) Habituation of the arousal reaction. Brain 79, 665-680.
121. Sherrington, C. S. (1906). The Integrative Action of the Nervous System. Charles Scribner's Sons: NY.
122. Sokolov, E. N. (1955) The higher nervous activity and the problem of perception. Proc. XIX Intl Congr. Psychol., Montreal.
123. Sokolov, E. N. (1963) Higher nervous functions: the orienting reflex. Annu. Rev. Physiol. 25, 545-580.
124. Spencer, W. A., Thompson, R. F. and Neilson, D. R. (1966) Response decrement of the flexion reflex in the acute spinal cat and transient restoration by strong stimuli. J. Neurophysiol. 29, 221-239.
125. Thompson, R. F. and Spencer, W. A. (1966) Habituation: a model phenomenon for the study of neuronal substrates of behaviour. Psychol. Rev. 73, 16-43.
126. Thorpe, W. H. (1950) The concepts of learning and their relation to those of instinct. Physiological Mechanisms in Animal Behaviour Symposium. Soc. Expl Biol. 4, 387-408.
127. Tomsic, D., Massoni, V. and Maldonado, H. (1993) Habituation to a danger stimulus in two semiterrestrial crabs: ontogenic, ecological and opioid modulation correlates. J. Comp. Physiol. 173A, 621-633.
128. Walter, W. G., Cooper, R., Aldridge, V. J., McCallum, W. C. and Winter, A. L. (1964) Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature 203, 380-384.
129. Wickelgren, B. G. (1967) Habituation of spinal motorneurones. J. Neurophysiol. 30, 1404-1438.
130. Wicks, S. R. and Rankin, C. K. (1995) Integration of mechanosensory stimuli in Caenorhabditis elegans. J. Neurosci. 15, 2434-2444.
131. Wintermute, G. P. (1909) The test for involvement of the labyrinth in suppurative middle ear processes. Calif. State J. Med. VII, 97-101.
132. Wood, D. C. (1970a) Parametric studies of the response decrement produced by mechanical stimuli in the protozoan, Stentor coeruleus. J. Neurobiol. 1, 345-360.
133. Wood, D. C. (1970b) Electrophysiological correlates of the response decrement produced by mechanical stimuli of the protozoan. Stentor coeruleus. J. Neurobiol. 2, 1-11.
134. Woodson, P. B. J., Schlapfer, W. T., Tremblay, J. P. and Barondes, S. H. (1976) Synaptic depression at a synapse in Aplysia californica: analysis in terms of a material flow model of neurotransmitter. Brain Res. 109, 41-59.
135. Woodworth,. R. S. and Schlosberg, H. (1964) Experimental Psychology, pp. 786-794. Holt, Rinehart and Winston: NY.
136. Zilber-Gachelin, N. F. and Chartier, M. P. (1973a) Modification of the motor reflex responses due to repetition of the peripheral stimulus in the cockroach. I: habituation at the level of an isolated abdominal ganglion. J. Expl Biol. 59, 359-381.
137. Zilber-Gachelin, N. F. and Chartier, M. P. (1973b) Modification of the motor reflex responses due to repetition of the peripheral stimulus in the cockroach. II: conditions of activation of the motorneurons. J. Expl Biol. 59, 383-403.
138. Zucker, R. S. (1972) Crayfish escape behaviour and central synapses. II. Physiological mechanisms underlying behavioural habituation. J. Neurophysiol. 35, 621-637.