Abstract
We developed a multicompartmental Hodgkin-Huxley model of the Hermissenda type-B photoreceptor and used it to address the relative contributions of reductions of two K+ currents, I a and I C, to changes in cellular excitability and synaptic strength that occur in these cells after associative learning. We found that reductions of gC, the peak conductance of I C, substantially increased the firing frequency of the type-B cell during the plateau phase of a simulated light response, whereas reductions of gA had only a modest contribution to the plateau frequency. This can be understood at least in part by the contributions of these currents to the light-induced (nonspiking) generator potential, the plateau of which was enhanced by gC reductions, but not by gA reductions. In contrast, however, reductions of gA broadened the type-B cell action potential, increased Ca2+ influx, and increased the size of the postsynaptic potential produced in a type-A cell, whereas similar reductions of gC had only negligible contributions to these measures. These results suggest that reductions of I A and I C play important but different roles in type-B cell plasticity.
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References
Acosta-Urquidi J, Crow T (1993) Differential modulation of voltage-dependent currents in Hermissenda type B photoreceptors by serotonin. Journal of Neurophysiology 20:541–548.
Acosta-Urquidi J, Crow T (1995) Characterization of voltage-activated currents in Hermissenda type B-photoreceptors. Journal of Neuroscience 15:319–332.
Akaike T, Alkon DL (1980) Sensory convergence on central visual neurons in Hermissenda. Journal of Neurophysiology 44:501–513.
Alkon DL, Fuortes MGF (1972) Responses of photoreceptors in Hermissenda. Journal of General Phsyiology 60:631–649.
Alkon DL, Lederhendler II, Shoukimas JJ (1982a) Primary changes of membrane currents during retention of associative learning. Science (Washington, DC) 215:693–695.
Alkon DL, Shoukimas JJ, Heldman E (1982b) Calcium-mediated decrease of a voltage-dependent potassium current. Biophysical Journal 40:245–250.
Alkon DL (1983) Intersensory convergence: A prerequisite for primary membrane changes of molluscan associative conditioning. In: Multimodal Convergences in Sensory Systems. Verlag, Stuttgart, pp. 355–368.
Alkon DL, Farley J, Sakakibara M, Hay B (1984) Voltage-dependent calcium and calcium-activated potassium currents of a molluscan photoreceptor. Biophysical Journal 46:605–614.
Alkon DL, Sakakibara M, Forman R, Harrigan J, Lederhendler I, Farley J (1985) Reduction of two voltage-dependent K+ currents mediates retention of a learned association. Behavioral and Neural Biology 44:278–300.
Alkon DL, Sanchez-Andres JV, Ito E, Oka K, Yoshioka T, Collin C (1992) Long-term transformation of an inhibitory into an excitatory GABAergic synaptic response. Proceedings of the National Academy of Sciences 89:11862–11866.
Barrett EP, Barrett JN (1976) Separation of two voltage-sensitive potassium currents, and demonstration of tetrodotoxin-resistant calcium current in frog motoneurones. Journal of Physiology 255:737–774.
Baxter DA, Byrne JH (1990) Differential effects of cAMP and serotonin on membrane current, action potential duration, and excitability in somata of pleural sensory neurons of Aplysia. Journal of Neurophysiology 64:978–990.
Braha O, Dale N, Hochner B, Klein M, Abrams TW, Kandel ER (1990) Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons. Proceedings of the National Academy of Sciences 87:2040–2044.
Byrne JH, Zwartjes R, Homayouni R, Critz SD, Eskin A (1993) Roles of second messenger pathways in neuronal plasticity and in learning and memory. In: S Shenolikar, AC Nairn, eds. Advances in Second Messenger and Phosphoprotein Research, Vol. 27. Raven Press, New York, pp. 47–108.
Canavier CC, Clark JW, Byrne JH (1991) Simulation of the bursting activity of neuron R15 in Aplysia: Role of ionic currents, calcium balance, and modulatory transmitters. Journal of Neurophysiology 66:2107–2124.
Clark GA, Schuman EM (1992) Snails' tails: Initial comparisons of synaptic plasticity underlying learning in Hermissenda and Aplysia. In: L Squire, N Butters, eds. Neuropsychology of Memory (2nd ed.). Guilford Press, New York, pp. 588–602.
Collin C, Ikeno H, Harrigan JF, Lederhendler I, Alkon DL (1988) Sequential modification of membrane currents with classical conditioning. Biophysical Journal 54:955–960.
Connor JA, Stevens CF (1971a) Inward and delayed outward membrane currents in isolated neural somata under voltage clamp. Journal of Physiology 213:1–19.
Connor JA, Stevens CF (1971b) Prediction of repetitive firing behavior from voltage clamp data on an isolated neurone soma. Journal of Physiology 213:31–53.
Connor JA, Stevens CF (1971c) Voltage clamp studies of a transient outward membrane current in gastropod neural somata. Journal of Physiology 213:21–30.
Crow T, Akon DL (1978) Retention of an associative behavioral change in Hermissenda. Science 209:1239.
Crow T, Alkon DL (1980) Neural correlates of a long-term associative behavioral modification in Hermissenda crassicornis (Abstract). Society for Neuroscience Abstracts 39:596.
Crow T (1983) Modification of B-photoreceptor adaptation predicts differential light responding following conditioning in Hermissenda (Abstract). Society for Neuroscience Abstracts 9:167.
Crow T, Offenbach N (1983) Modification of the initiation of locomotion in Hermissenda. Brain Research 271:301–310.
Crow T (1985) Conditioned modification of phototactic behavior in Hermissenda, II. Differential adaptation of B-photoreceptors. Journal of Neuroscience 5:215–223.
Crow T, Forrester J (1991) Light paired with serotonin in vivo produces both short- and long-term enhancement of generator potentials of identified B-photoreceptors in Hermissenda. Journal of Neuroscience 11:608–617.
Farley J (1987) Contingency learning and causal detection in Hermissenda: I. Behavior. Behavioral Neuroscience 101:13–27.
Farley J (1988) Associative training results in persistent reductions in a calcium-activated potassium current in Hermissenda type B photoreceptors. Behavioral Neuroscience 102:784–802.
Farley J, Alkon DL (1982) Associative neural and behavioral change in Hermissenda: Consequences of nervous system orientation for light and pairing specificity. Journal of Neurophysiology 48:785–807.
Farley J, Richards WG, Grover LM (1990) Associative learning causes changes intrinsic to Hermissenda type A photoreceptors. Behavioral Neuroscience 104:135–152.
Fost JW, Clark GA (1993) Computational analysis of contributions of K+ currents to learning-dependent changes in Hermissenda type-B photoreceptors (Abstract). Society for Neuroscience Abstracts 19:580.
Fost JW, Clark GA (1996) Modeling Hermissenda: II. Effects of variations in type-B cell excitability, synaptic strength, and connectivity. Journal of Computational Neuroscience 3.
Frysztak RJ, Crow T (1994) Enhancement of type B and type A photoreceptor inhibitory synaptic connections in conditioned Hermissenda. Journal of Neuroscience 14:1245–1250.
Goh Y, Alkon DL (1984) Sensory, interneuronal, and motor interactions within Hermissenda visual pathway. Journal of Neurophysiology 52:156–169.
Goh Y, Lederhendler I, Alkon DL (1985) Input and output changes of an identified neural pathway and correlated with associative learning in Hermissenda. Journal of Neuroscience 5:536–543.
Hochner B, Klein M, Schacher S, Kandel ER (1986) A novel component in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proceedings of the National Academy of Sciences 83:8794–8798.
Hochner B, Kandel ER (1992) Modulation of a transient K+ current in the pleural sensory neurons of Aplysia by serotonin and cAMP: Implications for spike broadening. Proceedings of the National Academy of Sciences 89:11476–11480.
Hodgkin A, Huxley A (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology 117:500–544.
Hodgson TM, Crow T (1991) Characterization of 4 light-responsive putative motor neurons in the pedal ganglia of Hermissenda crassicornis. Brain Research 557:255–264.
Klein M, Camardo J, Kandel ER (1982) Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proceedings of the National Academy of Sciences 79:5713–5717.
Lederhendler II, Gart S, Alkon DL (1986) Classical conditioning of Hermissenda: Origin of a new response. Journal of Neuroscience 6:1325–1331.
Lederhendler II, Collin C, Alkon DL (1990) Sequential changes of potassium currents in Hermissenda type B photoreceptor during early stages of classical conditioning. Neuroscience Letters 110:28–33.
Matzel LD, Lederhendler II, Alkon DL (1990a) Regulation of a short-term associative memory by calcium-dependent protein kinase. Journal of Neuroscience 10:2300–2307.
Matzel LD, Schreurs BG, Alkon DL (1990b) Pavlovian conditioning of distinct components of Hermissenda's response to rotation. Behavioral and Neural Biology 54:131–145.
Matzel LD, Collin C, Alkon DL (1992) Biophysical and behavioral correlates of memory storage, degradation, and reactivation. Behavioral Neuroscience 106:954–963.
McCormick DA, Huguenard J, Stowenbridge BW (1990) Determination of state-dependent processing in thalamus by single neuron properties and neuromodulators. In: T McKenna, J David, SF Zornetzer, eds. Single Neuron Computation. Academic Press, San Diego, pp. 259–290.
Pennefeather P, Lancaster B, Adams PR, Nicoll RA (1985) Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cells. Proceedings of the National Academy of Sciences 82:3040–3044.
Richards WG, Farley J, Alkon DL (1984) Extinction of associative learning in Hermissenda: Behavior and neural correlates. Behavioral and Brain Research 14:161–170.
Rogawski M (1985) The A-current: How ubiquitous a feature of excitable cells is it? Trends in the Neurosciences 8:214–219.
Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25:729–749.
Sakakibara M, Ikeno H, Usui S, Alkon DL (1990) Model of Hermissenda type-B photoreceptor based on principal soma currents. In: Vision, Memory, and the Temporal Lobe. Elsevier, New York, pp. 421–426.
Sakakibara M, Ikeno H, Usui S, Collin C, Alkon DL (1993) Reconstruction of ionic currents in a molluscan photoreceptor. Biophysical Journal 65:519–527.
Schultz L, Clark GA (1995) GABA-induced facilitation at type B to A photoreceptor synapses in Hermissenda (Abstracts). Society for Neuroscience Abstracts 21:1619.
Schuman EM, Clark GA (1994) Synaptic facilitation at connections of Hermissenda type B photoreceptors. Journal of Neuroscience 14:1613–1622.
Shimahara T (1983) Presynaptic modulation of transmitter release by the early outward potassium current in Aplysia. Brain Research 263:51–56.
Walsh JP, Byrne JH (1989) Modulation of a steady-state Ca2+-activated, K+ current in tail sensory neurons of Aplysia: Role of serotonin and cAMP. Journal of Neurophysiology 60:32–44.
Werness SA, Fay SD, Blackwell KT, Vogl TP, Alkon DL (1992) Associative learning in a network model of Hermissenda crassicornis: I. Theory. Biological Cybernetics 68:125–133.
West A, Barnes E, Alkon DL (1982) Primary changes of voltage responses during retention of associative learning. Journal of Neurophysiology 48:1243–1255.
Yamada W, Koch C, Adams P (1989) Multiple channels and calcium dynamics. In: C Koch, I Segev, eds. Methods in Neuronal Modeling. MIT Press, Cambridge, MA.
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Fost, J.W., Clark, G.A. Modeling Hermissenda: I. Differential contributions of I A and I C to type-B cell plasticity. J Comput Neurosci 3, 137–153 (1996). https://doi.org/10.1007/BF00160809
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DOI: https://doi.org/10.1007/BF00160809