A test of Hebb's postulate at identified synapses which mediate classical conditioning in Aplysia

In 1949, D. O. Hebb proposed a novel mechanism for producing changes in the strength of synapses that could account for associative learning. According to Hebb , the strength of a synapse might increase when the use of that synapse contributes to the generation of action potentials in a postsynaptic neuron. Thus, an essential feature of this postulate is that action potentials must occur in both a postsynaptic cell and a presynaptic cell for associative synaptic changes to occur. We have directly tested Hebb 's postulate in Aplysia at identified synapses which are known to exhibit a temporally specific increase in efficacy during a cellular analogue of differential conditioning. We find that the mechanism postulated by Hebb is neither necessary nor sufficient to produce the associative change in synaptic strength that underlies conditioning in Aplysia. In contrast, impulse activity in the presynaptic cell must be paired with facilitatory input, supporting the hypothesis that the temporal specificity of classical conditioning in Aplysia can be accounted for by activity-dependent amplification of presynaptic facilitation.

[1]  Elmer S. West From the U. S. A. , 1965 .

[2]  E. Kandel,et al.  Mechanism of heterosynaptic facilitation in the giant cell of the abdominal ganglion of Aplysia depilans. , 1965, The Journal of physiology.

[3]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[4]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[5]  D. Cohen The Neural Pathways and Informational Flow Mediating a Conditioned Autonomic Response , 1974 .

[6]  E. Kandel,et al.  Two functional effects of decreased conductance EPSP's: synaptic augmentation and increased electrotonic coupling. , 1976, Science.

[7]  F. F. Weight,et al.  Synaptic transmission: long-lasting potentiation by a postsynaptic mechanism. , 1976, Science.

[8]  Conditioning of cortical neurons in cats with antidromic activation as the unconditioned stimulus. , 1977, Journal of comparative and physiological psychology.

[9]  G. Hoyle,et al.  Neural events underlying learning in insects: changes in pacemaker , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  E. Kandel,et al.  Presynaptic modulation of voltage-dependent Ca2+ current: mechanism for behavioral sensitization in Aplysia californica. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[11]  C. D. Woody,et al.  Effects of acetylcholine and cyclic GMP on input resistance of cortical neurons in awake cats , 1978, Brain Research.

[12]  W. Davis,et al.  Neural correlate of behavioral plasticity in command neurons of Pleurobranchaea. , 1978, Science.

[13]  D. L. Alkon,et al.  Membrane depolarization accumulates during acquisition of an associative behavioral change. , 1980, Science.

[14]  G. Hoyle Learning, using natural reinforcements, in insect preparations that permit cellular neuronal analysis. , 1980, Journal of neurobiology.

[15]  E. Kandel,et al.  Intracellular injection of t he catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[16]  D. Alkon,et al.  Associative Behavioral Modification in Hermissenda: Cellular Correlates , 1980, Science.

[17]  A. Gelperin,et al.  Rapid taste-aversion learning by an isolated molluscan central nervous system. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[18]  E. Kandel,et al.  Classical conditioning in a simple withdrawal reflex in Aplysia californica , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  W. Singer,et al.  The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb synapses. , 1981, The Journal of physiology.

[20]  A. Baranyi,et al.  Synaptic facilitation requires paired activation of convergent pathways in the neocortex , 1981, Nature.

[21]  N. Tsukahara,et al.  Classical conditioning mediated by the red nucleus in the cat. , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  A. Gelperin,et al.  One-trial associative learning modifies food odor preferences of a terrestrial mollusc. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. Alkon,et al.  Primary changes of membrane currents during retention of associative learning. , 1982, Science.

[24]  G. A. Clark,et al.  Initial localization of the memory trace for a basic form of learning. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[25]  E R Kandel,et al.  Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[26]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. Ito Cerebellar control of the vestibulo-ocular reflex--around the flocculus hypothesis. , 1982, Annual review of neuroscience.

[28]  E. Kandel,et al.  A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. , 1983, Science.

[29]  E. Kandel,et al.  Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. , 1983, Journal of neurophysiology.

[30]  E. Kandel,et al.  Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica. , 1983, Science.

[31]  M. Brostrom,et al.  Associative Conditioning of Single Sensory Neurons Suggests a Cellular Mechanism for Learning , 2022 .