Summary
Recently, a neural model of visual pattern discrimination for stimulus-specific habituation was developed, based on previous behavioral studies which demonstrated that toads exhibit a dishabituation hierarchy for different worm-like stimuli. The model suggests that visual objects are represented by temporal coding and predicts that the dishabituation hierarchy changes when the stimulus/background contrast direction is reversed or the stimulus size is varied. The behavioral experiments reported in this paper were designed to test these predictions, (1) For a pair of stimuli from the contrast reversal prediction, the experimental results validated the theory. (2) For a pair of stimuli from the size reduction prediction, the experimental results failed to validate the theory. Further experiments concerning size effects suggest that configurai visual pattern discrimination in toads exhibits size invariance. (3) Inspired by the Groves-Thompson account of habituation, we found that dishabituation by a second stimulus has a separate process from habituation to a first stimulus. This paper serves as an example of a fruitful dialogue between experimentation and modeling, crucial for understanding brain functions.
Similar content being viewed by others
Abbreviations
- a-h :
-
worm-like stimulus patterns
- AT :
-
anterior thalamus
- ERF :
-
excitatory receptive field
- IRF :
-
inhibitory receptive field
- RF :
-
receptive field
- R2 to R4 :
-
retinal ganglion cell types
- vMP :
-
posterior ventromedial pallium
References
Arbib MA (1989) The metaphorical brain 2: neural networks and beyond. Wiley Interscience, New York Chichester Brisbane Toronto Singapore
Birukow G (1955) Angeborene und erworbene Anteile relativ einfacher Verhaltenseinheiten. Verh Deutsch Zool Ges 1955:32–47
Birukow G, Meng M (1955) Eine neue Methode zur Prüfung des Gesichtssinnes bei Amphibien. Naturwissenschaften 42:652–653
Boice R, Quanty CB, Williams RC (1974) Competition and possible dominance in turtles, toads, and frogs. J Comp Physiol Psychol 86:1116–1131
Burghagen H, Ewert J-P (1982) Question of “head preference” in response to worm-like dummies during prey-capture of toads Bufo bufo, Behav Processes 7:295–306
Carew TJ, Castellucci VF, Kandel ER (1971) An analysis of dishabituation and sensitization of the gill-withdrawal reflex in Aplysia. Int J Neurosci 2:79–98
Cerella J (1975) Studies of pattern perception in pigeons. Ph.D. Dissertation, Harvard University, Cambridge Mass
Eikmanns KH (1955) Verhaltensphysiologische Untersuchungen über den Beutefang und das Bewegungssehen der Erdkröte (Bufo bufo L). Z Tierpsychol 12:229–253
Ewert J-P (1967) Der Einfluß von Störreizen auf die Antwortbereitschaft bei der Richtbewegung der Erdkröte (Bufo bufo L). Z Tierpsychol 24:298–312
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 London, pp 246–416
Ewert J-P (1987) Neuroethology of releasing mechanism: preycatching in toads. Behav Brain Sci 10:337–405
Ewert J-P (1992) Neuroethology of an object features relating algorithm and its modification by learning. Rev Neurosci (in press)
Ewert J-P, Hock FJ (1972) Movement sensitive neurons in the toad's retina. Exp Brain Res 16:41–59
Ewert J-P, Ingle DJ (1971) Excitatory effects following habituation of prey-catching activity in frogs and toads. J Comp Physiol Psychol 77:369–374
Ewert J-P, Kehl W (1978) Configurational prey-selection by individual experience in the toad Bufo bufo. J Comp Physiol 126:105–114
Finkenstädt T (1989) Visual associative learning: searching for behaviorally relevant brain structures in toads: In: Ewert J-P, Arbib MA (eds) Visuomotor coordination: amphibians, comparisons, models, and robots. Plenum Press, New York London, pp 799–832
Finkenstädt T, Ewert J-P (1988a) Stimulus-specific long-term habituation of visually guided orienting behavior toward prey in toads: a 14C-2DG study. J Comp Physiol A 163:1–11
Finkenstädt T, Ewert J-P (1988b) Effects of visual associative conditioning on behavior and cerebral metabolic activity in toads. Naturwissenschaften 75:85–97
Fukushima K (1988) Neocognitron: a hierarchical neural network capable of visual pattern recognition. Neural Networks 1:119–130
Gellerman LW (1933) Form discrimination in chimpanzees and two-year-old children: 1. Form (triangularity) per se. J Genet Psychol 42:2–27
Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77:419–450
Harvey CB, Moore M, Lindsay L (1981) Passive-avoidance learning in bullfrogs, grass frogs, and toads. Psychol Rep 49:1003–1006
Hateren JH van, Srinivasan MV, Wait PB (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 167:649–654
Herrnstein RJ, Loveland BH (1964) Complex visual concept in the pigeon. Science 146:549–551
Ingle D (1968) Visual releasers of prey-catching behavior in frogs and toads. Brain Behav Evol 1:500–518
Ingle D (1971) Vision: The experimental analysis of visual behavior. In: Hoar WS, Randall DJ (eds) Fish Physiology, Vol. V. Academic Press, New York London, pp 59–71
Ingle D (1978) Mechanisms of shape-recognition among vertebrates. In: Held R, Leibowitz HW, Teuber H-L (eds) Perception (Handbook of sensory physiology, Vol. VIII). Springer, Berlin Heidelberg New York, pp 259–287
Ingle DJ, McKinley D (1978) Effects of stimulus configuration on elicited prey catching by the marine toad (Bufo marinus). Anim Behav 26:885–891
Jones WA, Falkenberg VP (1980) Test for effects of visual and position cues on T-maze learning in toads. Percept Motor Skills 50:455–460
Kandel E (1976) Cellular basis of behavior: an introduction to behavioral neurobiology. Freeman Comp, San Francisco
Karplus I, Algom D, Samuel D (1981) Acquisition and retention of dark avoidance by the toads, Xenopus laevis (Dudin). Anim Learning Behav 9:45–59
Merkel-Harff C, Ewert J-P (1991) Learning-related modulation of toad's responses to prey by neural loops involving the forebrain. In: Arbib MA, Ewert J-P (eds) Visual structures and integrated functions. Research notes in neural computing, Vo13. Springer, Berlin Heidelberg New York, pp 417–426
Pache J (1932) Formensehen bei Fröschen. Z Vergl Physiol 17:423–463
Schleidt W (1962) Die historische Entwicklung der Begriffe “angeborenes auslösendes Schema” und “angeborener Auslösemechanismus” in der Ethologie. Z Tierpsychol 19:697–722
Schmajuk NA, Segura ET (1980) Behavioral changes along escape learning in toads. Acta Physiol Lat Am 30:211–215
Schmajuk NA, Segura ET, Reboreda JC (1980) Appetitive conditioning and discriminatory learning in toads. Behav Neural Biol 28:392–397
Smith KU (1934) Visual discrimination in the cat: II. A further study of the capacity of the cat for visual figure discrimination. J Genet Psychol 45:336–357
Sokolov E (1975) Neuronal mechanisms of the orienting reflex. In: Sokolov E, Vinogradova O (eds) Neuronal mechanisms of the orienting reflex. Lawrence Erlbaum Hillsdale, New York, 217–235
Sutherland NS (1969) Shape discrimination in rat, octopus, and goldfish: a comparative study. J Comp Physiol Psychol 67:160–176
Sutherland NS, Carr AE (1968) Shape discrimination by rats: squares and rectangles. Brit J Psychol 55:39–48
Tinbergen N (1951) The study of instinct. Clarendon Press, Oxford
Thompson PA, Boice R (1975) Attempts to train frogs: review and experiments. J Biol Psychol 17:3–13
Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43
Thorpe WH (1963) Learning and instinct in animals. Harvard University Press, Cambridge Mass
Tsai HJ, Ewert J-P (1987) Edge preference of retinal and tectal neurons in common toads (Bufo bufo) in response to worm-like moving stripes: the question of behaviorally relevant position indicators. J Comp Physiol A 161:295–304
Wang DL (1991) Neural networks for temporal order learning and stimulus specific habituation. Ph.D. Dissertation, Univ Southern California
Wang DL, Arbib MA (1991) How does the toad's visual system discriminate different worm-like stimuli? Biol Cybern 64:251–261
Wang DL, Hsu CC (1990) SLONN: a simulation language for modeling of neural networks. Simulation 55:69–83
Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology, vol VII/6C). Springer, Berlin Heidelberg New York, pp 287–616
Wells MJ (1978) Octopus: physiology and behavior of an advanced invertebrate. Chapman and Hall, London
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wang, D., Ewert, JP. Configurational pattern discrimination responsible for dishabituation in common toads Bufo bufo (L.): Behavioral tests of the predictions of a neural model. J Comp Physiol A 170, 317–325 (1992). https://doi.org/10.1007/BF00191420
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00191420