nach oben

Journal of Computational Neuroscience

Erschienen in:

01.08.2011

A computer model of unitary responses from associational/commissural and perforant path synapses in hippocampal CA3 pyramidal cells

verfasst von: John L. Baker, Tamara Perez-Rosello, Michele Migliore, Germán Barrionuevo, Giorgio A. Ascoli

Erschienen in: Journal of Computational Neuroscience | Ausgabe 1/2011

Einloggen

Aktivieren Sie unsere intelligente Suche, um passende Fachinhalte oder Patente zu finden.

search-config

KI-gestützte Suche

Aus

Abstract

Despite the central position of CA3 pyramidal cells in the hippocampal circuit, the experimental investigation of their synaptic properties has been limited. Recent slice experiments from adult rats characterized AMPA and NMDA receptor unitary synaptic responses in CA3b pyramidal cells. Here, excitatory synaptic activation is modeled to infer biophysical parameters, aid analysis interpretation, explore mechanisms, and formulate predictions by contrasting simulated somatic recordings with experimental data. Reconstructed CA3b pyramidal cells from the public repository NeuroMorpho.Org were used to allow for cell-specific morphological variation. For each cell, synaptic responses were simulated for perforant pathway and associational/commissural synapses. Means and variability for peak amplitude, time-to-peak, and half-height width in these responses were compared with equivalent statistics from experimental recordings. Synaptic responses mediated by AMPA receptors are best fit with properties typical of previously characterized glutamatergic receptors where perforant path synapses have conductances twice that of associational/commissural synapses (0.9 vs. 0.5 nS) and more rapid peak times (1.0 vs. 3.3 ms). Reanalysis of passive-cell experimental traces using the model shows no evidence of a CA1-like increase of associational/commissural AMPA receptor conductance with increasing distance from the soma. Synaptic responses mediated by NMDA receptors are best fit with rapid kinetics, suggestive of NR2A subunits as expected in mature animals. Predictions were made for passive-cell current clamp recordings, combined AMPA and NMDA receptor responses, and local dendritic depolarization in response to unitary stimulations. Models of synaptic responses in active cells suggest altered axial resistivity and the presence of synaptically activated potassium channels in spines.

Vorheriger Artikel Control of firing patterns by two transient potassium currents: leading spike, latency, bistability

Sie haben noch keine Lizenz? Dann Informieren Sie sich jetzt über unsere Produkte:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

über 102.000 Bücher
über 537 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Finance + Banking
Management + Führung
Marketing + Vertrieb
Maschinenbau + Werkstoffe
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Jetzt informieren

Springer Professional "Wirtschaft"

Online-Abonnement

Mit Springer Professional "Wirtschaft" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 340 Zeitschriften

aus folgenden Fachgebieten:

Bauwesen + Immobilien
Business IT + Informatik
Finance + Banking
Management + Führung
Marketing + Vertrieb
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Jetzt informieren

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 390 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Maschinenbau + Werkstoffe

Jetzt Wissensvorsprung sichern!

Jetzt informieren

Amaral, D. G., Ishizuka, N., & Claiborne, B. (1990). Neurons, numbers and the hippocampal network. Progress in Brain Research, 83, 1–11.PubMedCrossRef

Amaral, D. G., & Witter, M. P. (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31, 571–591.PubMedCrossRef

Andrásfalvy, B. K., & Magee, J. C. (2001). Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. The Journal of Neuroscience, 21, 9151–9159.PubMed

Ascoli, G. A., Donohue, D. E., & Halavi, M. (2007). NeuroMorpho.Org: a central resource for neuronal morphologies. Journal of Neuroscience, 27, 9247–9251.PubMedCrossRef

Baker, J. L., & Olds, J. L. (2007). Theta phase precession emerges from a hybrid computational model of a CA3 place cell. Cognitive Neurodynamics, 1, 237–248.PubMedCrossRef

Bekkers, J. M., & Stevens, C. F. (1996). Cable properties of cultured hippocampal neurons determined from sucrose-evoked miniature EPSCs. Journal of Neurophysiology, 75, 1250–1255.PubMed

Berzhanskaya, J., Urban, N. N., & Barrionuevo, G. (1998). Electrophysiological and pharmacological characterization of the direct perforant path input to hippocampal area CA3. Journal of Neurophysiology, 79, 2111–2118.PubMed

Bloodgood, B. L., & Sabatini, B. L. (2007). Nonlinear regulation of unitary synaptic signals by CaV_2.3 voltage-sensitive calcium channels located in dendritic spines. Neuron, 53, 249–260.PubMedCrossRef

Cais, O., Sedlacek, M., Horak, M., Dittert, I., & Vyklicky, L., Jr. (2008). Temperature dependence of NR1/NR2B NMDA receptor channels. Neuroscience, 151, 428–438.PubMedCrossRef

Carnevale, N. T., & Hines, M. L. (2005). The NEURON book. New York: Cambridge University Press.

Chen, N., Ren, J., Raymond, L. A., & Murphy, T. H. (2001). Changes in agonist concentration dependence that are a function of duration of exposure suggest N-methyl-d-aspartate receptor nonsaturation during synaptic stimulation. Molecular Pharmacology, 59, 212–219.PubMed

Colquhoun, D., Jonas, P., & Sakmann, B. (1992). Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. Journal de Physiologie, 458, 261–287.

Cull-Candy, S., Brickley, S., & Farrant, M. (2001). NMDA receptor subunits: diversity, development and disease. Current Opinion in Neurobiology, 11, 327–335.PubMedCrossRef

Dalby, N. O., & Mody, I. (2003). Activation of NMDA receptors in rat dentate gyrus granule cells by spontaneous and evoked transmitter release. Journal of Neurophysiology, 90, 786–797.PubMedCrossRef

Dayan, P., & Abbott, L. (2001). Theoretical neuroscience. Cambridge: MIT.

Debanne, D., Guérineau, N. C., Gähwiler, B. H., & Thompson, S. M. (1995). Physiology and pharmacology of unitary synaptic connections between pairs of cells in areas CA3 and CA1 of rat hippocampal slice cultures. Journal of Neurophysiology, 73, 1282–1294.PubMed

Debanne, D., Gähwiler, B. H., & Thompson, S. M. (1998). Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. Journal de Physiologie, 507, 237–247.CrossRef

Debanne, D., Gähwiler, B. H., & Thompson, S. M. (1999). Heterogeneity of synaptic plasticity at unitary CA3-CA1 and CA3-CA3 connections in rat hippocampal slice cultures. The Journal of Neuroscience, 19, 10664–10671.PubMed

Destexhe, A., Mainen, Z. F., & Sejnowski, T. J. (1998). Kinetic models of synaptic transmission. In C. Koch & I. Segev (Eds.), Methods in neuronal modeling: From ions to networks (2nd ed., pp. 1–15). Cambridge: MIT.

Diamond, J. S. (2001). Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. The Journal of Neuroscience, 21, 8328–8338.PubMed

Do, V. H., Martinez, C. O., Martinez, J. L., Jr., & Derrick, B. E. (2002). Long-term potentiation in direct perforant path projections to the hippocampal CA3 region in vivo. Journal of Neurophysiology, 87, 669–678.PubMed

Erreger, K., Dravid, S. M., Banke, T. G., Wyllie, D. J. A., & Traynelis, S. F. (2005). Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. Journal de Physiologie, 563, 345–358.CrossRef

Feldmeyer, D., Lübke, J., Silver, R. A., & Sakmann, B. (2002). Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. Journal de Physiologie, 538, 803–822.CrossRef

Geiger, J. R., Lübke, J., Roth, A., Frotscher, M., & Jonas, P. (1997). Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron, 18, 1009–1023.PubMedCrossRef

Gentet, L. J., Stuart, G. J., & Clements, J. D. (2000). Direct measurement of specific membrane capacitance in neurons. Biophysical Journal, 79, 314–320.PubMedCrossRef

Golding, N. L., Mickus, T. J., Katz, Y., Kath, W. L., & Spruston, N. (2005). Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. Journal de Physiologie, 568, 69–82.CrossRef

Hemond, P., Epstein, D., Boley, A., Migliore, M., Ascoli, G. A., & Jaffe, D. B. (2008). Distinct classes of pyramidal cells exhibit mutually exclusive firing patterns in hippocampal area CA3b. Hippocampus, 18, 411–424.PubMedCrossRef

Hemond, P., Migliore, M., Ascoli, G. A., & Jaffe, D. B. (2009). The membrane response of CA3b pyramidal neurons near rest: heterogeneity of passive properties and the contribution of hyperpolarization-activated currents. Neuroscience, 160, 359–370.PubMedCrossRef

Henze, D., Cameron, W. E., & Barrionuevo, G. (1996). Dendritic morphology and its effects on the amplitude and rise-time of synaptic signals in hippocampal CA3 pyramidal cells. The Journal of Comparative Neurology, 369, 331–344.PubMedCrossRef

Hines, M. L., Morse, T., Migliore, M., Carnevale, N. T., & Shepherd, G. M. (2004). ModelDB: a database to support computational neuroscience. Journal of Computational Neuroscience, 17, 7–11.PubMedCrossRef

Hjorth-Simonsen, A. (1973). Some intrinsic connections of the hippocampus in the rat: an experimental analysis. The Journal of Comparative Neurology, 147, 145–161.PubMedCrossRef

Holmes, W. R., Ambros-Ingerson, J., & Grover, L. M. (2006). Fitting experimental data to models that use morphological data from public databases. Journal of Computational Neuroscience, 20, 349–365.PubMedCrossRef

Iansek, R., & Redman, S. J. (1973). The amplitude, time course, and charge of unitary excitatory post-synaptic potentials evoked in spinal motoneurone dendrites. Journal de Physiologie, 234, 665–688.

Ishizuka, N., Cowan, W. M., & Amaral, D. G. (1995). A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. The Journal of Comparative Neurology, 362, 17–45.PubMedCrossRef

Jaffe, D. B., & Carnevale, N. T. (1999). Passive normalization of synaptic integration influenced by dendritic architecture. Journal of Neurophysiology, 82, 3268–3285.PubMed

Jahr, C. E., & Stevens, C. F. (1990). Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. The Journal of Neuroscience, 10, 3178–3182.PubMed

Jonas, P., & Sakmann, B. (1992). Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. Journal de Physiologie, 455, 143–171.

Jonas, P., Major, G., & Sakmann, B. (1993). Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. Journal de Physiologie, 472, 615–663.

Káli, S., & Dayan, P. (2000). The involvement of recurrent connections in area CA3 in establishing the properties of place fields: a model. The Journal of Neuroscience, 20, 7463–7477.PubMed

Khazipov, R., Ragozzino, D., & Bregestovski, P. (1995). Kinetics and Mg²⁺ block of N-methyl-d-aspartate receptor channels during postnatal development of hippocampal CA3 pyramidal neurons. Neuroscience, 69, 1057–1065.PubMedCrossRef

Lazarewicz, M. T., Migliore, M., & Ascoli, G. A. (2002). A new bursting model of CA3 pyramidal cell physiology suggests multiple locations for spike initiation. Biosystems, 67, 129–137.PubMedCrossRef

Magee, J. C., & Cook, E. P. (2000). Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nature Neuroscience, 3, 895–903.PubMedCrossRef

Major, G., Larkman, A. U., Jonas, P., Sakmann, B., & Jack, J. J. B. (1994). Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. The Journal of Neuroscience, 14, 4613–4638.PubMed

Marr, D. (1971). Simple memory: a theory for archicortex. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 262, 23–81.PubMedCrossRef

Matsuda, S., Kobayashi, Y., & Ishizuka, N. (2004). A quantitative analysis of the laminar distribution of synaptic boutons in field CA3 of the rat hippocampus. Neuroscience Research, 49, 241–252.PubMedCrossRef

McMahon, D. B., & Barrionuevo, G. (2002). Short- and long-term plasticity of the perforant path synapse in hippocampal area CA3. Journal of Neurophysiology, 88, 528–533.PubMed

Megías, M., Emri, Z., Freund, T. F., & Gulyás, A. I. (2001). Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience, 102, 527–540.PubMedCrossRef

Migliore, M., Hoffman, D. A., Magee, J. C., & Johnston, D. (1999). Role of an A-type K⁺ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. Journal of Computational Neuroscience, 7, 5–15.PubMedCrossRef

Miles, R., & Wong, R. K. S. (1986). Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. Journal de Physiologie, 373, 397–418.

Miller, R. G., Jr. (1998). Beyond ANOVA: Basics of applied statistics. New York: Chapman & Hall/CRC.

Nicholson, D., Katz, Y., Trana, R., Kath, W. L., Spruston, N., & Geinisman, Y. (2006). Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron, 50, 431–442.PubMedCrossRef

Palmer, L. M., & Stuart, G. J. (2009). Membrane potential changes in dendritic spines during action potentials and synaptic inputs. The Journal of Neuroscience, 29, 6897–6903.PubMedCrossRef

Perez-Rosello, T., Baker, J. L., Ferrante, M., Iyengar, S., Ascoli, G. A., Barrionuevo, G. (2010). Passive and active shaping of unitary responses from associational/commissural and perforant path synapses in hippocampal CA3 pyramidal cells. Journal of Computational Neuroscience (in press).

R Development Core Team (2009). R: A language and environment for statistical computing [Online]. R Foundation for Statistical Computing. http://www.R-project.org. Accessed October 19, 2009.

Rall, W., Burke, R. E., Smith, T. G., Nelson, P. G., & Frank, K. (1967). Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. Journal of Neurophysiology, 30, 1169–1193.PubMed

Ramón y Cajal, S. (1995). Histology of the nervous system of man and vertebrates. Translation from the French edition by Swanson N, Swanson LW. New York: Oxford University Press.

Rolls, E. T. (1996). A theory of hippocampal function in memory. Hippocampus, 6, 601–620.PubMedCrossRef

Roth, A., & Häusser, M. (2001). Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. Journal de Physiologie, 535, 445–472.CrossRef

Samsonovich, A., & McNaughton, B. L. (1997). Path integration and cognitive mapping in a continuous attractor neural network model. The Journal of Neuroscience, 17, 5900–5920.PubMed

Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 20, 11–21.CrossRef

Smith, M. A., Ellis-Davies, G. C. R., & Magee, J. C. (2003). Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons. Journal de Physiologie, 548, 245–258.CrossRef

Spruston, N., & Johnston, D. (1992). Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. Journal of Neurophysiology, 67, 508–529.PubMed

Spruston, N., Jonas, P., & Sakmann, B. (1995). Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. Journal de Physiologie, 482, 325–352.

Svoboda, K., Tank, D. W., & Denk, W. (1996). Direct measurement of coupling between dendritic spines and shafts. Science, 272, 716–719.PubMedCrossRef

Swanson, L. W., Wyss, J. M., & Cowan, W. M. (1978). An autoradiographic study of the organization of intrahippocampal association pathways in the rat. The Journal of Comparative Neurology, 181, 681–715.PubMedCrossRef

Turner, D. A., Li, X. G., Pyapali, G. K., Ylinen, A., & Buzsáki, G. (1995). Morphometric and electrical properties of reconstructed hippocampal CA3 neurons recorded in vivo. The Journal of Comparative Neurology, 356, 580–594.PubMedCrossRef

Vicini, S., Wang, J. F., Li, J. H., Zhu, W. J., Wang, Y. H., Luo, J. H., et al. (1998). Functional and pharmacological differences between recombinant N-methyl-d-aspartate receptors. Journal of Neurophysiology, 79, 555–566.PubMed

Wallenstein, G. V., & Hasselmo, M. E. (1997). GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. Journal of Neurophysiology, 78, 393–408.PubMed

Williams, S. H., & Johnston, D. (1991). Kinetic properties of two anatomically distinct excitatory synapses in hippocampal CA3 pyramidal neurons. Journal of Neurophysiology, 66, 1010–1020.PubMed

Titel: A computer model of unitary responses from associational/commissural and perforant path synapses in hippocampal CA3 pyramidal cells
verfasst von: John L. Baker
Tamara Perez-Rosello
Michele Migliore
Germán Barrionuevo
Giorgio A. Ascoli
Publikationsdatum: 01.08.2011
Verlag: Springer US
Erschienen in: Journal of Computational Neuroscience / Ausgabe 1/2011
Print ISSN: 0929-5313
Elektronische ISSN: 1573-6873
DOI: https://doi.org/10.1007/s10827-010-0304-x

Springer Professional

Abstract

Bitte loggen Sie sich ein, um Zugang zu Ihrer Lizenz zu erhalten.

Sie haben noch keine Lizenz? Dann Informieren Sie sich jetzt über unsere Produkte:

Springer Professional "Wirtschaft+Technik"

Springer Professional "Wirtschaft"

Springer Professional "Technik"

Weitere Artikel der Ausgabe 1/2011

Role of active dendritic conductances in subthreshold input integration

Control of firing patterns by two transient potassium currents: leading spike, latency, bistability

Firing responses of bursting neurons with delayed feedback

The impacts of geometry and binding on CaMKII diffusion and retention in dendritic spines

Non-weak inhibition and phase resetting at negative values of phase in cells with fast-slow dynamics at hyperpolarized potentials

An inter-segmental network model and its use in elucidating gait-switches in the stick insect