Abstract
Conditioned responses often reflect knowledge about the timing of a US. This knowledge is manifested in the dependance of response topography on the CS-US interval employed in training. A neural network model and set of learning rules capable of simulating temporally adaptive features of conditioned responses is reviewed, and simulations are presented. In addition, we present a neural network implementation of the model which is designed to reconcile empirical studies of long-term synaptic depression in the cerebellum with neurobiological evidence from studies of the classically conditioned nictitating membrane response of the rabbit.
Similar content being viewed by others
References
Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61
Alkon DL (1984) Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226:1037–1045
Berthier NE, Moore JW (1986) Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp Brain Res 63:341–350
Berthier NE, Desmond JE, Moore JW (1987) Brain stem control of the nictitating membrane response. In: Gormezano I, Prokasy WF, Thompson RF (eds) Classical conditioning. III. Lawrence Erlbaum, Hillsdale, NJ, pp 275–286
Berthier NE, Barto AG, Moore JW (1988) Linear systems analysis of cerebellar deep nuclei cells during performance of classical conditioned eyeblink. Soc Neurosci (abstr) 14:1239
Boncau CA (1958) The interstimulus interval and the latency of the conditioned eyelid response. J Exp Psychol 56:464–472
Braitcnberg V (1967) Is the cerebellar cortex a biological clock in the millisecond range? In: Fox CA, Snider RS (eds) Progress in brain research, vol 25. The cerebellum. Elsevier, New York, pp 334–346
Brand S, Dahl AL, Mugnaini E (1976) The length of parallel fibers in the cat cerebellar cortex. An experimental light and electron microscope study. Exp Brain Res 26:39–58
Clark GA, McCormick DA, Lavond DG, Thompson RF (1984)Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal responses. Brain Res 291:125–136
Coss RG, Perkel DH (1985) The function of dendritic spines: a review of theoretical issues. Behav Neur Biol 44:151–185
Crepel F, Krupa M (1988) Activation of protein kinase C induces a long-term depression of glutamate sensitivity of cerebellar Purkinje cells. An in vitro study. Brain Res 458:397–401
Desmond JE (1988) Temporally adaptive conditioned responses: representation of the stimulus trace in neural-network models. Computer and Information Science Technical Report 88–80, University of Massachusetts, Amherst
Desmond JE, Moore JW (1982) A brain stem region essential for the classically conditioned but not unconditioned nictitating membrane response. Physiol Behav 28:1029–1033
Desmond JE, Moore JW (1986) Dorsolateral pontine tegmentum and the classically conditioned nictitating membrane response: analysis of CR-related activity. Exp Brain Res 65:59–74
Desmond JE, Moore JW (1987) Red nucleus single-unit activity during the classically conditioned rabbit nictitating membrane response. Soc Neurosci (abstr) 13:841
Desmond JE, Moore JW (1988) Adaptive timing in neural networks: the conditioned response. Biol Cybern 58:405–415
Dietrichs E, Walberg F (1983) Cerebellar cortical afferents from the red nucleus in the cat. Exp Brain Res 50:353–358
Donegan NH, Lowery RW, Thompson RF (1983) Effects of lesioning cerebellar nuclei on conditioned leg-flexion responses. Soc Neurosci (abstr) 9:331
Fujita M (1982) Adaptive filter model of the cerebellum. Biol Cybern 45:195–206
Gingrich KJ, Byrne JH (1987) Single-cell neuronal model for associative learning. J Neurophys 57:1705–1715
Gormezano I, Moore JW (1969) Classical conditioning. In: Marx MH (ed) Learning: processes. Collier-Macmillan, London
Gormezano I, Kehoe EJ, Marshall BS (1983) Twenty years of classical conditioning with the rabbit. Prog Psychobiol Physiol Psychol 10:197–275
Grossberg S, Schmajuk NA (1989) Neural dynamics of adaptive timing and temporal discrimination during associative learning. Neural Networks 2:79–102
Haines DE (1988) Evidence of intracerebellar collateralization of nucleocortical cell processes in a prosimian primate (Galago): a fluorescence retrograde study. J Comp Neurol 275:441–451
Hardiman MJ, Glickstein M, Yeo CH (1988) Kainic acid lesions of the cerebellar cortex abolish the classically conditioned nictitating membrane response of the rabbit. Soc Neurosci (abstr) 14:784
Harvey JA, Winsky L, Schindler CW, McMaster SE, Welsh JP (1988) Asymmetric uptake of 2-deoxy-D-[14G] glucose in the dorsal cochlear nucleus during Pavlovian conditioning in the rabbit. Brain Res 449:213–224
Huang CM, Liu G, Huang R (1982) Projections from the cochlear nucleus to the cerebellum. Brain Res 244:1–8
Hull CL (1932) The goal gradient hypothesis and maze learning. Psychol Rev 39:25–43
Ito M (1984) The cerebellum and neural control. Raven Press, New York
Ito M (1989) Long-term depression. Ann Rev Neurosci 12:85–102
Ito M, Sakurai M, Tongroach P (1982) Climbing fibre-induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol (London) 324:113–134
Kamin LJ (1968) Attention-like processes in classical conditioning. In: Prokasy WF (ed) Classical conditioning: a symposium. Appleton, New York, pp 118–147
Kano M, Kato M (1987) Quisqualate receptors are specifically involved in cerebellar synaptic plasticity. Nature 325:276–279
Kano M, Kato M (1988) Modes of induction of long-term depression at parallel fibre-Purkinje cells synapses in rabbit erebellar cortex. Neurosci Res 5:544–556
Kelly TM, McAlduff JD, Bloedel JR (1988) Presence of eyeblink conditioning in decerebrate and decerebellate rabbit. Soc Neurosci (abstr) 14:169
Kimmel HD (1965) Instrumental inhibitory factors in classical conditioning. In: Prokasy WF (ed) Classical conditioning. Appleton-Century-Crofts, New York, pp 148–171
Klopf AH (1988) A neuronal model of classical conditioning. Psychobiology 16:85–125
Lavond DG, Steinmetz JE, Yokaitis MH, Thompson RF (1987)Reacquisition of classical conditioning after removal of cerebellar cortex. Exp Brain Res 67:569–593
Leonard DW, Theios J (1967) Effect of CS-US interval shift on classical conditioning of the nictitating membrane in the rabbit. J Comp Physiol Psychol 63:355–358
Levey AB, Martin I (1968) Shape of the conditioned eyelid response. Psychol Rev 75:398–408
Llinas R, Hillman DE (1969) Physiological and morphological organization of the cerebellar circuits in various vertebrates. In: Llinas R (ed) Neurobiology of cerebellar evolution and development. American Medical Association, Chicago, pp 43–73
Llinas R, Muhlethaler M (1988) Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol (London) 404:251–258
Logan FA (1956) A micromolar approach to behavior theory. Psychol Rev 65:63–73
Marchant HG, Moore JW (1973) Blocking of the rabbit's conditioned nictitating membrane response in Kamin's twostage paradigm. J Exp Psychol 101:155–158
Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437–470
Martin I, Levey AB (1965) Efficiency of the conditioned eyelid response. Science 150:781–783
Menne D (1985) Theoretical limits of time resolution in narrow band neurons. In: Michelsen A (ed) Time resolution in auditory systems. Proceedings of the 11th Danavox symposium on hearing. Springer, Berlin, Heidelberg New York, pp 96–107
Millenson JR, Kehoe EJ, Gormezano I (1977) Classical conditioning of the rabbit's nictitating membrane response under fixed and mixed CS-US intervals. Learn Motiv 8:351–366
Moore JW (1979) Brain processes and conditioning. In: Dickinson A, Boakes RA (eds) Mechanisms of learning and motivation: a memorial volume to Jerzy Konorski. Erlbaum, Hillsdale, NJ, pp 111–142
Moore JW, Berthier NE (1987) Purkinje cell activity and the conditioned nictitating membrane response. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and neuronal plasticity. Plenum Press, New York, pp 339–352
Moore JW, Blazis DEJ (1989) Conditioning and the cerebellum. In: Arbib MA, Amari S (eds) Dynamic interactions in neural networks: Models and data. Springer, New York Berlin Heidelberg, pp 261–277
Moore JW, Stickney KJ (1985) Antiassociations: conditioned inhibition in attentional-associative networks. In: Miller RR, Spear NE (eds) Information processes in animals: conditioned inhibition. Erlbaum, Hillsdale, NJ, pp 209–222
Moore JW, Desmond JE, Berthier NE, Blazis DEJ, Sutton RS, Barto AG (1986) Simulation of the classically conditioned nictitating membrane response by a neuron-like adaptive element: response topography, neuronal firing, and interstimulus intervals. Behav Brain Res 21:143–154
Nelson B, Barmack NH, Mugnaini E (1984) A GABAergic cerebello-olivary projection in the rat. Soc Neurosci (abstr) 10:539
Norman RF, Buchwald JS, Villablanca JR (1977) Classical conditioning with auditory discrimination of the eye blink in decerebrate cats. Science 196:551–553
Nowak AJ, Gormezano I (1988) Reflex modification (RM) and classical conditioning of the rabbit's nictitating membrane response (NMR) to electrical stimulation of brain stem structures as an unconditioned stimulus (UCS). Soc Neurosci (abstr) 14:3
Polenchar BE, Patterson MM (1984) Cerebellar deep nuclei lesions abolish or impair an instrumental avoidance response in rabbit. Soc Neurosci (abstr) 10:123
Port RL, Mikhail AA, Patterson MM (1985) Differential effects of hippocampectomy on classically conditioned rabbit nictitating membrane response related to interstimulus interval. Behav Neurosci 99:200–208
Ross WN, Werman R (1987) Mapping calcium transients in the dendrites of Purkinje cells from the guinea-pig cerebellum in vitro. J Physiol (London) 389:319–336
Sakurai M (1987) Synaptic modification of parallel fiberPurkinje cell transmission in in vitro guinea-pig cerebellar slices. J Physiol (London) 394:463–480
Scheibel ME, Scheibel AB (1985) Structural substrates for integrative patterns in the brain stem reticular core. In: Jasper H, Proctor LD, Knighton RS, Noshay WS, Costello RT (eds) Reticular formation of the brain. Little, Brown, Boston, pp 31–55
Scheibel ME, Scheibel AB (1967) Anatomical basis of attention mechanisms in vertebrate brains. In: Quarton GC, Melnechuk T, Schmitt FO (eds) The neurosciences. A study program. The Rockefeller University Press, New York, pp 577–602
Schmajuk NA, Moore JW (1988) The hippocampus and the classically conditioned nictitating membrane response: a real-time attentional-associative model. Psychobiology 16:20–35
Schmajuk NA, Moore JW (1989) Simulation of the classically conditioned nictitating membrane response by an attentional-associative network: response topography, neuronal firing, and the effects of hippocampal lesions and simulation. Behav Brain Res 32:173–189
Schreurs BG (1988) Stimulation of the spinal trigeminal nucleus supports classical conditioning of the rabbit's nictitating membrane response. Behav Neurosci 102:163–172
Sears RJ, Baker JS, Frey PW (1979) The eye blink as a timelocked response: implications for serial and second-order conditioning. J Exp Psychol: Anim Behav Proc 5:43–64
Sutton RS, Barto AG (1981) Toward a modern theory of adaptive networks: expectation and prediction. Psychol Rev 88:135–170
Tank DW, Sugimori M, Connor JA, Llinas RR (1988) Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242:773–777
Tesauro G (1986) Simple neural models of classical conditioning. Biol Cybern 55:187–200
Thompson RF (1986) The neurobiology of learning and memory. Science 233:941–947
Thompson RF, Donegan NH, Clark GA, Lavond DG, Lincoln JS, Madden J, Mamounas LA, Mauk MD, McCormick DA (1987) Neuronal substrates of discrete conditioned reflexes, conditioned fear states, and their interactions in the rabbit. In: Gormezano I, Prokasy WF, Thompson RF (eds) Classical conditioning. III. Erlbaum, Hillsdale, NJ, pp 371–400
Weiss C, Tocco G, Thompson JK, Thompson RF (1988) Anatomical analysis of cerebellar-olivary projections in the rabbit. Soc Neurosci (abstr) 14:493
Wells GR, Hardiman MJ, Yeo CH (1989) Visual projections to the pontine nuclei in rabbit: Orthograde and retrograde tracing studies with WGA-HRP. J Comp Neurol 279:629–652
Yeo CB (1987) Cerebellum and classical conditioning. In: Glickstein M, Yeo C, Stein J (eds) Cerebellum and neuronal plasticity. Plenum Press, New York, pp 321–338
Yeo CH, Hardiman MJ (1988) Loss of conditioned responses following cerebellar cortical lesions is not a performance deficit. Soc Neurosci (abstr) 14:3
Zipser D (1986) A model of hippocampal learning during classical conditioning. Behav Neurosci 100:764–776
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Moore, J.W., Desmond, J.E. & Berthier, N.E. Adaptively timed conditioned responses and the cerebellum: A neural network approach. Biol. Cybern. 62, 17–28 (1989). https://doi.org/10.1007/BF00217657
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00217657