Skip to main content
Log in

After-hyperpolarization currents and acetylcholine control sigmoid transfer functions in a spiking cortical model

Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Recurrent networks are ubiquitous in the brain, where they enable a diverse set of transformations during perception, cognition, emotion, and action. It has been known since the 1970’s how, in rate-based recurrent on-center off-surround networks, the choice of feedback signal function can control the transformation of input patterns into activity patterns that are stored in short term memory. A sigmoid signal function may, in particular, control a quenching threshold below which inputs are suppressed as noise and above which they may be contrast enhanced before the resulting activity pattern is stored. The threshold and slope of the sigmoid signal function determine the degree of noise suppression and of contrast enhancement. This article analyses how sigmoid signal functions and their shape may be determined in biophysically realistic spiking neurons. Combinations of fast, medium, and slow after-hyperpolarization (AHP) currents, and their modulation by acetylcholine (ACh), can control sigmoid signal threshold and slope. Instead of a simple gain in excitability that was previously attributed to ACh, cholinergic modulation may cause translation of the sigmoid threshold. This property clarifies how activation of ACh by basal forebrain circuits, notably the nucleus basalis of Meynert, may alter the vigilance of category learning circuits, and thus their sensitivity to predictive mismatches, thereby controlling whether learned categories code concrete or abstract information, as predicted by Adaptive Resonance Theory.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abel, H. J., Lee, J. C. F., Callaway, J. C., & Foehring, R. C. (2004). Relationships between intracellular calcium and afterhyperpolarizations in neocortical pyramidal neurons. Journal of Neurophysiology, 91(1), 324–335.

    Article  PubMed  CAS  Google Scholar 

  • Akins, P. T., Surmeier, D. J., & Kitai, S. T. (1990). Muscarinic modulation of a transient k + conductance in rat neostriatal neurons. Nature, 344, 240–242.

    Article  PubMed  CAS  Google Scholar 

  • Anwar, H., Hong, S., & De Schutter, E. (2010). Controlling ca(2+)-activated K (+) channels with models of Ca (2+) buffering in purkinje cells. Cerebellum. England: London.

    Google Scholar 

  • Arnold, H. M., Burk, J. A., Hodgson, E. M., Sarter, M., & Bruno, J. P. (2002). Differential cortical acetylcholine release in rats performing a sustained attention task versus behavioral control tasks that do not explicitly tax attention. Neuroscience, 114(2), 451–460.

    Article  PubMed  CAS  Google Scholar 

  • Atri, A., Sherman, S., Norman, K. A., Kirchhoff, B. A., Nicolas, M. M., Greicius, M. D., et al. (2004). Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behavioral Neuroscience, 118(1), 223–236.

    Article  PubMed  CAS  Google Scholar 

  • Ballaz, S. J. (2009). Differential novelty detection in rats selectively bred for novelty-seeking behavior. Neuroscience Letters, 461(1), 45–48.

    Article  PubMed  CAS  Google Scholar 

  • Barkai, E., & Hasselmo, M. E. (1994). Modulation of the input/output function of rat piriform cortex pyramidal cells. Journal of Neurophysiology, 72(2), 644–658.

    PubMed  CAS  Google Scholar 

  • Bordey, A., Sontheimer, H., & Trouslard, J. (2000). Muscarinic activation of BK channels induces membrane oscillations in glioma cells and leads to inhibition of cell migration. Journal of Membrane Biology, 176(1), 31–40.

    Article  PubMed  CAS  Google Scholar 

  • Bosking, W. H., Zhang, Y., Schofield, B., & Fitzpatrick, D. (1997). Orientation selectivity and the arrangement of horizontal connections in the tree shrew striate cortex. Journal of Neuroscience, 7, 2112–2127.

    Google Scholar 

  • Botly, L. C., & De Rosa, E. (2007). Cholinergic influences on feature binding. Behavioral Neuroscience, 121(2), 264–276.

    Article  PubMed  Google Scholar 

  • Botly, L. C., & De Rosa, E. (2009). Cholinergic deafferentation of the neocortex using 192 igg-saporin impairs feature binding in rats. Journal of Neuroscience, 29(13), 4120–4130.

    Article  PubMed  CAS  Google Scholar 

  • Brown, A. M., Schwindt, P. C., & Crill, W. E. (1993). Voltage dependence and activation kinetics of pharmacologically defined components of the high-threshold calcium current in rat neocortical neurons. Journal of Neurophysiology, 70(4), 1530–1543.

    PubMed  CAS  Google Scholar 

  • Bullier, J., McCourt, M. E., & Henry, G. H. (1988). Physiological studies on the feedback connection to the striate cortex from cortical areas 18 and 19 of the cat. Experimental Brain Research, 70, 90–98.

    CAS  Google Scholar 

  • Bullock, D., & Grossberg, S. (1988). Neural dynamics of planned arm movements: Emergent invariants and speed-accuracy properties during trajectory formation. Psychological Review, 95, 49–90.

    Article  PubMed  CAS  Google Scholar 

  • Bullock, D., Cisek, P., & Grossberg, S. (1998). Cortical networks for control of voluntary arm movements under variable force conditions. Cerebral Cortex, 8, 48–62.

    Article  PubMed  CAS  Google Scholar 

  • Canavier, C. C., Oprisan, S. A., Callaway, J. C., Ji, H., & Shepard, P. D. (2007). Computational model predicts a role for ERG current in repolarizing plateau potentials in dopamine neurons: implications for modulation of neuronal activity. Journal of Neurophysiology, 98(5), 3006–3022.

    Article  PubMed  Google Scholar 

  • Cantrell, A. R., & Catterall, W. A. (2001). Neuromodulation of Na+ channels: an unexpected form of cellular plasticity. Nature Review Neuroscience, 2, 397–407.

    Article  CAS  Google Scholar 

  • Carpenter, G. A., & Grossberg, S. (1987). A massively parallel architecture for a self-organizing neural pattern recognition machine. Computer Vision, Graphics, and Image Processing, 37, 54–115.

    Article  Google Scholar 

  • Carpenter, G. A., & Grossberg, S. (1991). Pattern recognition by self-organizing neural Networks. Cambridge: MIT Press.

    Google Scholar 

  • Carter, A. J., O’Connor, W. T., Carter, M. J., & Ungerstedt, U. (1995). Caffeine enhances acetylcholine release in the hippocampus in vivo by a selective interaction with adenosine a1 receptors. Journal of Pharmacology and Experimental Therapeutics, 273(2), 637–642.

    PubMed  CAS  Google Scholar 

  • Chisum, H. J., Mooser, F., & Fitzpatrick, D. (2003). Emergent properties of Layer 2/3 neurons reflect the collinear arrangement of horizontal connections in tree shrew visual cortex. Journal of Neuroscience, 23, 2947–2960.

    PubMed  CAS  Google Scholar 

  • Cox, D. H., Cui, J., & Aldrich, R. W. (1997). Allosteric gating of a large conductance ca-activated K+ channel. Journal of General Physiology, 110(3), 257–281.

    Article  PubMed  CAS  Google Scholar 

  • Crouzier, D., Baubichon, D., Bourbon, F., & Testylier, G. (2006). Acetylcholine release, EEG spectral analysis, sleep staging and body temperature studies: a multiparametric approach on freely moving rats. Journal of Neuroscience Methods, 151(2), 159–167.

    Article  PubMed  CAS  Google Scholar 

  • Delcour, A. H., Lipscombe, D., & Tsien, R. W. (1993). Multiple modes of n-type calcium differences in gating kinetics channel activity distinguished by differences in gating kinetics. Journal of Neuroscience, 13(1), 181–194.

    PubMed  CAS  Google Scholar 

  • Descarries, L., & Umbriaco, D. (1995). Ultrastructural basis of monoamine and acetylcholine function in cns. Seminars in Neuroscience, 7(5), 309–318.

    Article  CAS  Google Scholar 

  • Desimone, R. (1998). Visual attention mediated by biased competition in extrastriate visual cortex. Philosophical Transactions of Royal Socociety B, 353, 1245–1255.

    Article  CAS  Google Scholar 

  • Destexhe, A., Mainen, Z. F., & Sejnowski, T. J. (1994a). Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. Journal of Computational Neuroscience, 1(3), 195–230.

    Article  PubMed  CAS  Google Scholar 

  • Destexhe, A., Mainen, Z. F., & Sejnowski, T. J. (1994b). An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Computation, 6(1), 14–18.

    Article  Google Scholar 

  • Ellias, S., & Grossberg, S. (1975). Pattern formation, contrast control, and oscillations in the short term memory of shunting on-center off-surround networks. Biological Cybernetics, 20, 69–98.

    Article  Google Scholar 

  • Elman, J. L. (1991). Distributed representations, simple recurrent networks, and grammatical structure. Machine Learning, 7(2–3), 195–225.

    Google Scholar 

  • Engel, A. K., Fries, P., & Singer, W. (2001). Dynamic predictions: oscillations and synchrony in top-down processing. Nature Reviews Neuroscience, 2, 704–716.

    Article  PubMed  CAS  Google Scholar 

  • Fellous, J.-M. M., Rudolph, M., Destexhe, A., & Sejnowski, T. J. (2003). Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience, 122(3), 811–829.

    Article  PubMed  CAS  Google Scholar 

  • Freeman, W. J. (1979). Nonlinear gain mediating cortical stimulus-response relations. Biological Cybernetics, 33(4), 237–247.

    Article  PubMed  CAS  Google Scholar 

  • Fries, P., Reynolds, J. H., Rorie, A. E., & Desimone, R. (2001). Modulation of oscillatory neuronal synchronization by selective visual attention. Science, 291, 1560–1563.

    Article  PubMed  CAS  Google Scholar 

  • Gao, E., & Suga, N. (1998). Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proceedings of the National Academy of Sciences of the United States of America, 95, 12663–12670.

    Article  PubMed  CAS  Google Scholar 

  • Giocomo, L., & Hasselmo, M. (2007). Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Molecular Neurobiology, 36(2), 184–200.

    Article  PubMed  CAS  Google Scholar 

  • Goldman, D. E. (1943). Potential, impedance, and rectification in membranes. The Journal of General Physiology, 27, 37–60.

    Article  PubMed  CAS  Google Scholar 

  • Grossberg, S. (1973). Contour enhancement, short-term memory, and constancies in reverberating neural networks. Studies in Applied Mathematics, 52, 213–257.

    Google Scholar 

  • Grossberg, S. (1980). How does a brain build a cognitive code? Psychological Review, 87, 1–51.

    Article  PubMed  CAS  Google Scholar 

  • Grossberg, S. (1999). How does the cerebral cortex work? Learning, attention, and grouping by the laminar circuits of visual cortex. Spatial Vision, 12, 163–186.

    Article  PubMed  CAS  Google Scholar 

  • Grossberg, S. (2003). How does the cerebral cortex work? Development, learning, attention, and 3D vision by laminar circuits of visual cortex. Behavioral and Cognitive Neuroscience Reviews, 2, 47–76.

    Article  PubMed  Google Scholar 

  • Grossberg, S., & Levine, D. (1975). Some developmental and attentional biases in the contrast enhancement and short term memory of recurrent neural networks. Journal of Theoretical Biology, 53(2), 341–380.

    Article  PubMed  CAS  Google Scholar 

  • Grossberg, S., & Versace, M. (2008). Spikes, synchrony, and attentive learning by laminar thalamocortical circuits. Brain Research, 1218, 278–312.

    Article  PubMed  CAS  Google Scholar 

  • Hata, T., Kumai, K., & Okaichi, H. (2007). Hippocampal acetylcholine efflux increases during negative patterning and elemental discrimination in rats. Neuroscience Letters, 418(2), 127–132.

    Article  PubMed  CAS  Google Scholar 

  • Hestrin, S., & Armstrong, W. E. (1996). Morphology and physiology of cortical neurons in layer i. Journal of Neuroscience, 16(17), 5290–5300.

    PubMed  CAS  Google Scholar 

  • Hicks, G. A., & Marrion, N. V. (1998). Ca2+ −dependent inactivation of large conductance Ca2+ −activated K+ (BK) channels in rat hippocampal neurones produced by pore block from an associated particle. The Journal of Physiology, 508(3), 721–734.

    Article  PubMed  CAS  Google Scholar 

  • Hirschberg, B., Maylie, J., Adelman, J. P., & Marrion, N. V. (1998). Gating of recombinant small-conductance Ca-activated K + channels by calcium. Journal of General Physiology, 111(4), 565–581.

    Article  PubMed  CAS  Google Scholar 

  • Hodgkin, A. L., & Huxley, A. F. (1952). Currents carried by sodium and potassium ions through the membrane of the giant axon of loligo. The Journal of Physiology, 116(4), 449–472.

    PubMed  CAS  Google Scholar 

  • Hodgkin, A. L., & Katz, B. (1949). The effect of sodium ions on the electrical activity of the giant axon of the squid. The Journal of Physiology, 108, 37–77.

    PubMed  CAS  Google Scholar 

  • Hotson, J. R., & Prince, D. A. (1980). A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. Journal of Neurophysiology, 43(2), 409–419.

    PubMed  CAS  Google Scholar 

  • Hsieh, C. Y., Cruikshank, S. J., & Metherate, R. (2000). Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Research, 880(1–2), 51–64.

    Article  PubMed  CAS  Google Scholar 

  • Karmarkar, U. R., & Buonomano, D. V. (2006). Different forms of homeostatic plasticity are engaged with distinct temporal profiles. The European journal of neuroscience, 23(6), 1575–1584.

    Article  PubMed  Google Scholar 

  • Kilgard, M. P., & Merzenich, M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science, 279(5357), 1714–1718.

    Article  PubMed  CAS  Google Scholar 

  • King, J. D., & Meriney, S. D. (2005). Proportion of N-type calcium current activated by action potential stimuli. Journal of Neurophysiology, 94(6), 3762–3770.

    Article  PubMed  CAS  Google Scholar 

  • Klink, R., & Alonso, A. (1997). Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. Journal of Neurophysiology, 77(4), 1813–1828.

    PubMed  CAS  Google Scholar 

  • Köhn, J., & Wörgötter, F. (1998). Employing the zeta-transform to optimize the calculation of the synaptic conductance of NMDA and other synaptic channels in network simulations. Neural Computation, 10(7), 1639–1651.

    Article  PubMed  Google Scholar 

  • Kong, W.-J. J., Guo, C.-K. K., Zhang, S., Hao, J., Wang, Y.-J. J., & Li, Z.-W. W. (2005). The properties of ach-induced BK currents in guinea pig type ii vestibular hair cells. Hearing Research, 209(1–2), 1–9.

    Article  PubMed  CAS  Google Scholar 

  • Kong, W.-J. J., Guo, C.-K. K., Zhang, X.-W. W., Chen, X., Zhang, S., Li, G.-Q. Q., et al. (2007). The coupling of acetylcholine-induced BK channel and calcium channel in guinea pig saccular type ii vestibular hair cells. Brain Research, 1129(1), 110–115.

    Article  PubMed  CAS  Google Scholar 

  • Köppen, A., Klein, J., Schmidt, B. H., van der Staay, F. J., & Löffelholz, K. (1996). Effects of nicotinamide on central cholinergic transmission and on spatial learning in rats. Pharmacology, Biochemistry, and Behavior, 53(4), 783–790.

    Article  PubMed  Google Scholar 

  • Kraus, N., McGee, T., Littman, T., Nicol, T., & King, C. (1994). Nonprimary auditory thalamic representation of acoustic change. Jounral of Neurophysiology, 72, 1270–1277.

    CAS  Google Scholar 

  • Krause, M., & Pedarzani, P. (2000). A protein phosphatase is involved in the cholinergic suppression of the Ca(2+)-activated K(+) current sI(AHP) in hippocampal pyramidal neurons. Neuropharmacology, 39(7), 1274–1283.

    Article  PubMed  CAS  Google Scholar 

  • Krupa, D. J., Ghazanfar, A. A., & Nicolelis, M. A. L. (1999). Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proceedings of the National Academy of Sciences of the United States of America, 96, 8200–8205.

    Article  PubMed  CAS  Google Scholar 

  • Kurokawa, M., Shiozaki, S., Nonaka, H., Kase, H., Nakamura, J., & Kuwana, Y. (1996). In vivo regulation of acetylcholine release via adenosine a1 receptor in rat cerebral cortex. Neuroscience Letters, 209(3), 181–184.

    Article  PubMed  CAS  Google Scholar 

  • Lancaster, B., & Adams, P. R. (1986). Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. Journal of Neurophysiology, 55(6), 1268–1282.

    PubMed  CAS  Google Scholar 

  • Lee, J. C. F., Callaway, J. C., & Foehring, R. C. (2005). Effects of temperature on calcium transients and ca2+ −dependent afterhyperpolarizations in neocortical pyramidal neurons. Journal of Neurophysiology, 93(4), 2012–2020.

    Article  PubMed  CAS  Google Scholar 

  • Levitt, J. B., Yoshioka, T., & Lund, J. S. (1994). Intrinsic cortical connections in macaque visual area V2: evidence for interaction between different functional streams. The Journal of Comparative Neurology, 342, 551–570.

    Article  PubMed  CAS  Google Scholar 

  • Lima, P. A., & Marrion, N. V. (2007). Mechanisms underlying activation of the slow ahp in rat hippocampal neurons. Brain Research, 1150, 74–82.

    Article  PubMed  CAS  Google Scholar 

  • Loane, D. J., Lima, P. A., & Marrion, N. V. (2007). Co-assembly of N-type Ca2+ and BK channels underlies functional coupling in rat brain. Journal of Cell Science, 120(Pt 6), 985–995.

    Article  PubMed  CAS  Google Scholar 

  • Lorenzon, N. M., & Foehring, R. C. (1992). Relationship Between Repetitive Firing and Afterhyperpolarizations in Human Neocortical Neurons. Journal of Neurophysiology, 67(2), 350–363.

    PubMed  CAS  Google Scholar 

  • Lorenzon, N. M., & Foehring, R. C. (1995). Characterization of pharmacologically identified voltage-gated calcium channel currents in acutely isolated rat neocortical neurons. Journal of Neurophysiology, 73(4), 1430–1442.

    PubMed  CAS  Google Scholar 

  • Luvisetto, S., Fellin, T., Spagnolo, M., Hivert, B., Brust, P. F., Harpold, M. M., et al. (2004). Modal gating of human CaV2.1 (P/Q-type) calcium channels: I. the slow and the fast gating modes and their modulation by beta subunits. Journal of General Physiology, 124(5), 445–61.

    Article  PubMed  CAS  Google Scholar 

  • Markram, H., Lübke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic aps and epsps. Science, 275(5297), 213–215.

    Article  PubMed  CAS  Google Scholar 

  • Marrosu, F., Portas, C., Mascia, M., Casu, M., Fa, M., Giagheddu, M., et al. (1995). Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Research, 671(2), 329–332.

    Article  PubMed  CAS  Google Scholar 

  • Matthews, E. A., Linardakis, J. M., & Disterhoft, J. F. (2009). The fast and slow afterhyperpolarizations are differentially modulated in hippocampal neurons by aging and learning. Journal of Neuroscience, 29(15), 4750–4755.

    Article  PubMed  CAS  Google Scholar 

  • McCormick, D. A., & Williamson, A. (1989). Convergence and divergence of neurotransmitter action in human cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America, 86(20), 8098–8102.

    Article  PubMed  CAS  Google Scholar 

  • Mechawar, N., Watkins, K. C., & Descarries, L. (2002). Ultrastructural features of the acetylcholine innervation in the developing parietal cortex of rat. The Journal of Comparative Neurology, 443(3), 250–258.

    Article  PubMed  CAS  Google Scholar 

  • Mitchell, J., Sundberg, K., & Reynolds, J. (2007). Differential attention-dependent response modulation across cell classes in macaque visual area v4. Neuron, 55(1), 131–141.

    Article  PubMed  CAS  Google Scholar 

  • Morishima, M., & Kawaguchi, Y. (2006). Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. The Journal of Neuroscience, 26(16), 4394–4405.

    Article  PubMed  CAS  Google Scholar 

  • Muller, W., Petrozzino, J. J., Griffith, L. C., Danho, W., & Connor, J. A. (1992). Specific involvement of ca(2+)-calmodulin kinase II in cholinergic modulation of neuronal responsiveness. Journal of Neurophysiology, 68(6), 2264–2269.

    PubMed  CAS  Google Scholar 

  • Nakajima, Y., Nakajima, S., Leonard, R. J., & Yamaguchi, K. (1986). Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proceedings of the National Academy of Sciences of the United States of America, 83(9), 3022–3026.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, C. L., Sarter, M., & Bruno, J. P. (2005). Prefrontal cortical modulation of acetylcholine release in posterior parietal cortex. Neuroscience, 132(2), 347–359.

    Article  PubMed  CAS  Google Scholar 

  • Pandya, P. K., Moucha, R., Engineer, N. D., Rathbun, D. L., Vazquez, J., & Kilgard, M. P. (2005). Asynchronous inputs alter excitability, spike timing, and topography in primary auditory cortex. Hearing Research, 203(1–2), 10–20.

    Article  PubMed  Google Scholar 

  • Parikh, V., & Sarter, M. (2006). Cortical choline transporter function measured in vivo using choline-sensitive microelectrodes: clearance of endogenous and exogenous choline and effects of removal of cholinergic terminals. Journal of Neurochemistry, 97(2), 488–503.

    Article  PubMed  CAS  Google Scholar 

  • Parikh, V., Kozak, R., Martinez, V., & Sarter, M. (2007). Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron, 56(1), 141–154.

    Article  PubMed  CAS  Google Scholar 

  • Pedarzani, P., & Storm, J. F. (1996). Evidence that ca/calmodulin-dependent protein kinase mediates the modulation of the Ca2+ −dependent K+ current, Iahp, by acetylcholine, but not by glutamate, in hippocampal neurons. Pflügers Archival European Journal of Physiology, 431(5), 723–728.

    CAS  Google Scholar 

  • Pineda, J. C., Waters, R. S., & Foehring, R. C. (1998). Specificity in the interaction of HVA Ca2+ channel types with Ca2+ −dependent AHPs and firing behavior in neocortical pyramidal neurons. Journal of Neurophysiology, 79(5), 2522–2534.

    PubMed  CAS  Google Scholar 

  • Pollen, D. A. (1999). On the neural correlates of visual perception. Cerebral Cortex, 9, 4–19.

    Article  PubMed  CAS  Google Scholar 

  • Povysheva, N. V., Gonzalez-Burgos, G., Zaitsev, A. V., Kroner, S., Barrionuevo, G., Lewis, D. A., et al. (2006). Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cerebral Cortex, 16(4), 541–552.

    Article  PubMed  CAS  Google Scholar 

  • Power, J. M., & Sah, P. (2008). Competition between calcium-activated k+ channels determines cholinergic action on firing properties of basolateral amygdala projection neurons. Journal of Neuroscience, 28(12), 3209–3220.

    Article  PubMed  CAS  Google Scholar 

  • Prakriya, M., & Lingle, C. J. (1999). BK channel activation by brief depolarizations requires Ca2+ influx through L- and Q-type Ca2+ channels in rat chromaffin cells. Journal of Neurophysiology, 81(5), 2267–2278.

    PubMed  CAS  Google Scholar 

  • Prakriya, M., Solaro, C. R., & Lingle, C. J. (1996). [Ca2+]i elevations detected by BK channels during Ca2+ influx and muscarine-mediated release of Ca2+ from intracellular stores in rat chromaffin cells. Journal of Neuroscience, 16(14), 4344–4359.

    PubMed  CAS  Google Scholar 

  • Prinz, A. A., Billimoria, C. P., & Marder, E. (2003). Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. Journal of Neurophysiology, 90, 3998–4015.

    Article  PubMed  Google Scholar 

  • Ramanathan, D., Tuszynski, M. H., & Conner, J. M. (2009). The basal forebrain cholinergic system is required specifically for behaviorally mediated cortical map plasticity. Journal of Neuroscience, 29(18), 5992–6000.

    Article  PubMed  CAS  Google Scholar 

  • Rasch, B. H., Born, J., & Gais, S. (2006). Combined blockade of cholinergic receptors shifts the brain from stimulus encoding to memory consolidation. Journal of Cognitive Neuroscience, 18(5), 793–802.

    Article  PubMed  Google Scholar 

  • Rhodes, P. A., & Gray, C. M. (1994). Simulations of intrinsically bursting neocortical pyramidal neurons. Neural Computation, 6(6), 1086–1110.

    Article  Google Scholar 

  • Saar, D., & Barkai, E. (2003). Long-term modifications in intrinsic neuronal properties and rule learning in rats. European Journal of Neuroscience, 17, 2727–2734.

    Article  PubMed  Google Scholar 

  • Saar, D., Grossman, Y., & Barkai, E. (2001). Long-lasting cholinergic modulation underlies rule learning in rats. Journal of Neuroscience, 21, 1385–1392.

    PubMed  CAS  Google Scholar 

  • Sah, P. (1996). Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends in Neuroscience, 19(4), 150–154.

    Article  CAS  Google Scholar 

  • Santini, E., Quirk, G. J., & Porter, J. T. (2008). Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. Journal of Neuroscience, 28(15), 4028–4036.

    Article  PubMed  CAS  Google Scholar 

  • Sarter, M., Hasselmo, M. E., Bruno, J. P., & Givens, B. (2005). Unraveling the attentional functions of cortical cholinergic inputs: Interactions between signal-driven and cognitive modulation of signal detection. Brain Research Reviews, 48, 98–111.

    Article  PubMed  CAS  Google Scholar 

  • Sarter, M., Parikh, V., & Howe, W. M. (2009). Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nature Reviews Neuroscience, 10(5), 383–390.

    Article  PubMed  CAS  Google Scholar 

  • Satake, T., Mitani, H., Nakagome, K., & Kaneko, K. (2008). Individual and additive effects of neuromodulators on the slow components of afterhyperpolarization currents in layer v pyramidal cells of the rat medial prefrontal cortex. Brain Research, 1229, 47–60.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, K. E., Goebel, R., Löwel, S., & Singer, W. (1997). The perceptual grouping criterion of colinearity is reflected by anisotropies of connections in the primary visual cortex. European Journal of Neuroscience, 9, 1083–1089.

    Article  PubMed  CAS  Google Scholar 

  • Schreiber, M., & Salkoff, L. (1997). A novel calcium-sensing domain in the BK channel. Biophysical Journal, 73(3), 1355–1363.

    Article  PubMed  CAS  Google Scholar 

  • Schwindt, P. C., Spain, W. J., Foehring, R. C., Stafstrom, C. E., Chubb, M. C., & Crill, W. E. (1988a). Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. Journal of Neurophysiology, 59, 424–449.

    PubMed  CAS  Google Scholar 

  • Schwindt, P. C., Spain, W. J., Foehring, R. C., Stafstrom, C. E., Chubb, M. C., & Crill, W. E. (1988b). Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in excitability changes. Journal of Neurophysiology, 59, 450–467.

    PubMed  CAS  Google Scholar 

  • Shapiro, M. S., Roche, J. P., Kaftan, E. J., Cruzblanca, H., Mackie, K., & Hille, B. (2000). Reconstitution of muscarinic modulation of the KCNQ2/KCNQ3 K(+) channels that underlie the neuronal M current. Journal of Neuroscience, 20(5), 1710–1721.

    PubMed  CAS  Google Scholar 

  • Sillito, A. M., Jones, H. E., Gerstein, G. L., & West, D. C. (1994). Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature, 369, 479–482.

    Article  PubMed  CAS  Google Scholar 

  • Solinas, S., Forti, L., Cesana, E., Mapelli, J., De Schutter, E., & D’Angelo, E. (2007). Computational reconstruction of pacemaking and intrinsic electroresponsiveness in cerebellar golgi cells. Frontiers in Cellular Neuroscience, 1(12), 2.

    PubMed  Google Scholar 

  • Song, S., Sjöström, P. J., Reigl, M., Nelson, S., & Chklovskii, D. B. (2005). Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biology, 3(3), 507–519.

    Article  CAS  Google Scholar 

  • Soto, G., Kopell, N., & Sen, K. (2006). Network architecture, receptive fields, and neuromodulation: computational and functional implications of cholinergic modulation in primary auditory cortex. Journal of Neurophysiology, 96, 2972–2983.

    Article  PubMed  Google Scholar 

  • Storm, J. F. (1987). Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. The Journal of Physiology, 385(1), 733–759.

    PubMed  CAS  Google Scholar 

  • Storm, J. F. (1989). An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. The Journal of Physiology, 409, 171–190.

    PubMed  CAS  Google Scholar 

  • Sun, X., Gu, X. Q., & Haddad, G. G. (2003). Calcium influx via L- and N-type calcium channels activates a transient large-conductance Ca2+ −activated K+ current in mouse neocortical pyramidal neurons. The Journal of Neuroscience, 23(9), 3639–3648.

    PubMed  CAS  Google Scholar 

  • Taylor, A. L., Hickey, T. J., Prinz, A. A., & Marder, E. (2006). Structure and visualization of high-dimensional conductance spaces. Journal of Neurophysiology, 96, 891–905.

    Article  PubMed  Google Scholar 

  • Traub, R. D., Wong, R. K., Miles, R., & Michelson, H. (1991). A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. Journal of Neurophysiology, 66(2), 635–650.

    PubMed  CAS  Google Scholar 

  • Traub, R. D., Buhl, E. H., Gloveli, T., & Whittington, M. A. (2003). Fast rhythmic bursting can be induced in layer 2/3 cortical neurons by enhancing persistent Na+ conductance or by blocking BK channels. Journal of Neurophysiology, 89(2), 909–921.

    Article  PubMed  CAS  Google Scholar 

  • Traub, R. D., Contreras, D., Cunningham, M. O., Murray, H., LeBeau, F. E., Roopun, A., et al. (2005). Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts. Journal of Neurophysiology, 93, 2194–2232.

    Article  PubMed  Google Scholar 

  • Turrigiano, G., Abbott, L. F., & Marder, E. (1994). Activity-dependent changes in the intrinsic properties of cultured neurons. Science, 264, 974–977.

    Article  PubMed  CAS  Google Scholar 

  • Umbriaco, D., Watkins, K. C., Descarries, L., Cozzari, C., & Hartman, B. K. (1994). Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. The Journal of Comparative Neurology, 348(3), 351–373.

    Article  PubMed  CAS  Google Scholar 

  • Usrey, W. M. (2002). The role of spike timing for thalamocortical processing. Current Opinion in Neurobiology, 12, 411–417.

    Article  PubMed  CAS  Google Scholar 

  • van Der Werf, Y. D., Witter, M. P., & Groenewegen, H. J. (2002). The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Research Reviews, 39, 107–140.

    Article  PubMed  Google Scholar 

  • Van Geit, W., Achard, P., & De Schutter, E. (2007). Neurofitter: a parameter tuning package for a wide range of electrophysiological neuron models. Frontiers in Neuroinformatics, 1, 1–17.

    PubMed  Google Scholar 

  • Versace, M., Ames, H., Léveillé, J., Fortenberry, B., & Gorchetchnikov, A. (2008). Kinness: a modular framework for computational neuroscience. Neuroinformatics, 6, 291–309.

    Article  PubMed  Google Scholar 

  • Villalobos, C., Shakkottai, V. G., Chandy, K. G., Michelhaugh, S. K., & Andrade, R. (2004). SKca channels mediate the medium but not the slow calcium-activated afterhyperpolarization in cortical neurons. Journal of Neuroscience, 24(14), 3537–3542.

    Article  PubMed  CAS  Google Scholar 

  • Vogalis, F., Storm, J. F., & Lancaster, B. (2003). SK channels and the varieties of slow after-hyperpolarizations in neurons. European Journal of Neuroscience, 18, 3155–3166.

    Article  PubMed  Google Scholar 

  • Wallner, M., Meera, P., & Toro, L. (1999). Molecular basis of fast inactivation in voltage and Ca2+ −activated K+ channels: a transmembrane beta-subunit homolog. Proceedings of the National Academy of Sciences of the United States of America, 96(7), 4137–4142.

    Article  PubMed  CAS  Google Scholar 

  • Wang, X. J., Liu, Y., Sanchez-Vives, M. V., & McCormick, D. A. (2003). Adaptation and temporal decorrelation by single neurons in the primary visual cortex. Journal of Neurophysiology, 89, 3279–3293.

    Article  PubMed  Google Scholar 

  • Watt, A., van Rossum, M., MacLeod, K., Nelson, S., & Turrigiano, G. (2000). Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron, 26(3), 659–670.

    Article  PubMed  CAS  Google Scholar 

  • Weaver, C. M., & Wearne, S. L. (2008). Neuronal firing sensitivity to morphologic and active mebrane parameters. PLoS Computational Biology, 4(1), 130–150.

    Article  CAS  Google Scholar 

  • Wei, A. D., Gutman, G. A., Aldrich, R., Chandy, K. G., Grissmer, S., & Wulff, H. (2005). International union of pharmacology. LII. nomenclature and molecular relationships of calcium-activated potassium channels. Pharmacological Reviews, 57(4), 463–472.

    Article  PubMed  CAS  Google Scholar 

  • Wersing, H., Beyn, W., & Ritter, H. (2001). Dynamical stability conditions for recurrent neural networks with unsaturating piecewise linear transfer functions. Neural Computation, 13, 1811–1825.

    Article  PubMed  CAS  Google Scholar 

  • Williams, J. A., Comisarow, J., Day, J., Fibiger, H. C., & Reiner, P. B. (1994). State-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis. Journal of Neuroscieince, 14(9), 5236–5242.

    CAS  Google Scholar 

  • Wilson, C. J., Weyrick, A., Terman, D., Hallworth, N. E., & Bevan, M. D. (2004). A model of reverse spike frequency adaptation and repetitive firing of subthalamic nucleus neurons. Journal of Neurophysiology, 91(5), 1963–1980.

    Article  PubMed  Google Scholar 

  • Winters, B. D., Bartko, S. J., Saksida, L. M., & Bussey, T. J. (2007). Scopolamine infused into perirhinal cortex improves object recognition memory by blocking the acquisition of interfering object information. Learning & Memory, 14(9), 590–596.

    Article  Google Scholar 

  • Zhang, Y. Q., Lu, S.-G., Ji, Y.-P., Zhao, Z.-Q., & Mei, J. (2004). Electrophysiological and pharmacological properties of nucleus basalis magnocellularis neurons in rats. Acta Pharmacologica Sinica, 25(2), 161–170.

    PubMed  Google Scholar 

Download references

Acknowledgements

J.P., M.V., and S.G. were supported in part by CELEST, an NSF Science of Learning Center (NSF SBE-0354378). J.P. and S.G. were supported by the SyNAPSE program of DARPA (HR0011-09-C-0001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen Grossberg.

Additional information

Action Editor: Barry Richmond

Rights and permissions

Reprints and permissions

About this article

Cite this article

Palma, J., Versace, M. & Grossberg, S. After-hyperpolarization currents and acetylcholine control sigmoid transfer functions in a spiking cortical model. J Comput Neurosci 32, 253–280 (2012). https://doi.org/10.1007/s10827-011-0354-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-011-0354-8

Keywords

Navigation