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Tuning Neocortical Pyramidal Neurons between Integrators and Coincidence Detectors

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Abstract

Do cortical neurons operate as integrators or as coincidence detectors? Despite the importance of this question, no definite answer has been given yet, because each of these two views can find its own experimental support. Here we investigated this question using models of morphologically-reconstructed neocortical pyramidal neurons under in vivo like conditions. In agreement with experiments we find that the cell is capable of operating in a continuum between coincidence detection and temporal integration, depending on the characteristics of the synaptic inputs. Moreover, the presence of synaptic background activity at a level comparable to intracellular measurements in vivo can modulate the operating mode of the cell, and act as a switch between temporal integration and coincidence detection. These results suggest that background activity can be viewed as an important determinant of the integrative mode of pyramidal neurons. Thus, background activity not only sharpens cortical responses but it can also be used to tune an entire network between integration and coincidence detection modes.

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References

  • Abeles M (1982) Role of the cortical neuron: Integrator or coincidence detector? Isr. J. Med. Sci. 18: 83-92.

    PubMed  Google Scholar 

  • Abeles M, Bergman H, Margalit E, Vaadia E (1993) Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J. Neurophysiol. 70: 1629-1638.

    PubMed  Google Scholar 

  • Aertsen A, Diesmann M, Gewaltig MO (1996) Propagation of synchronous spiking activity in feedforward neural networks. J. Physiology (Paris) 90: 243-247.

    Google Scholar 

  • Bair W, Koch C (1996) Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Computation 15: 1185-1202.

    Google Scholar 

  • Barlow H (1995) The neuron doctrine in perception. In: MS Gazzaniga, ed. The Cognitive Neurosciences. MIT Press. pp. 415-435.

  • Bell CC, Han VZ, Sugawara Y, Grant K (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387: 278-281.

    Article  PubMed  Google Scholar 

  • Bernander Ö, Douglas RJ, Martin KAC, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. USA 88: 11569-11573.

    PubMed  Google Scholar 

  • Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18: 10464-10472.

    PubMed  Google Scholar 

  • Bugmann G, Christodoulou C, Taylor JG (1997) Role of temporal integration and fluctuation detection in the highly irregular firing of a leaky integrator neuron model with partial reset. Neural. Comp. 9: 985-1000.

    Google Scholar 

  • Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256: 1025-1027.

    PubMed  Google Scholar 

  • Contreras D, Destexhe A, Steriade M (1997) Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J. Neurophysiol. 78: 335-350.

    PubMed  Google Scholar 

  • deCharms RC, Merzenich MM (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381: 610-613.

    Article  PubMed  Google Scholar 

  • deCharms RC, Zador A (2000) Neural representation and the cortical code. Annu. Rev. Neurosci. 23: 613-647.

    Article  PubMed  Google Scholar 

  • DeFelipe J, Fariñas I (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39: 563-607.

    Article  PubMed  Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission. In: C Koch, I Segev, eds. Methods in Neuronal Modeling, 2nd edn. MIT Press, Cambridge, MA. pp. 1-26.

    Google Scholar 

  • Destexhe A, Paré D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol. 81: 1531-1547.

    PubMed  Google Scholar 

  • Diesmann M, Gewaltig MO, Aertsen A (1996) Characterization of synfire activity by propagating “pulse packets.” In: JM Bower, ed. Computational Neuroscience. Academic Press, San Diego. pp. 59-64.

    Google Scholar 

  • Diesmann M, Gewaltig MO, Aertsen A (1999) Stable propagation of synchronous spiking in cortical neural networks. Nature 402: 529-533.

    Article  PubMed  Google Scholar 

  • Engel AK, König P, Kreiter AK, Schillen TB, Singer W (1992) Temporal coding in the visual cortex: New vistas on integration in the nervous system. Trends Neurosci. 15: 218-226.

    Article  PubMed  Google Scholar 

  • Gerstein GL, Bedenbaugh P, Aertsen AMHJ (1989) Neuronal assemblies. IEEE Trans. Biomed. Eng. 36: 4-14.

    Article  PubMed  Google Scholar 

  • Gray CM (1994) Synchronous oscillations in neuronal systems: Mechanisms and functions. J. Comput. Neurosci. 1: 11-38.

    PubMed  Google Scholar 

  • Han VZ, Grant K, Bell CC (2000) Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27: 611-622.

    Article  PubMed  Google Scholar 

  • Häusser M, Spruston N, Stuart GJ (2000) Diversity and dynamics of dendritic signaling. Science 290: 739-744.

    Article  PubMed  Google Scholar 

  • Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Computation 9: 1179-1209.

    PubMed  Google Scholar 

  • Hô N, Destexhe A (2000) Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J. Neurophysiol. 84: 1488-1496.

    PubMed  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117: 500-544.

    PubMed  Google Scholar 

  • Holmes WR (1986) Cable theory modeling of the effectiveness of synaptic inputs in cortical pyramidal cells. Ph.D. Thesis, University of California, Los Angeles.

    Google Scholar 

  • Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J. Neurophysiol. 75: 1806-1814.

    PubMed  Google Scholar 

  • Huguenard JR, Hamill OP, Prince DA (1988) Developmental changes in Na+ conductances in rat neocortical neurons: Appearance of a slow inactivating component. J. Neurophysiol. 59: 778-795.

    PubMed  Google Scholar 

  • Johnston D, Magee JC, Colbert CM, Christie BR (1996) Active properties of neuronal dendrites. Annu. Rev. Neurosci. 19: 165-186.

    Article  PubMed  Google Scholar 

  • Kisley MA, Gerstein GL (1999) The continuum of operating modes for a passive model neuron. Neural Comp. 11: 1139-1154.

    Article  Google Scholar 

  • Koch C, Laurent G (1999) Complexity and the nervous system. Science 284: 96-98.

    Article  PubMed  Google Scholar 

  • König P, Engel AK, Roelfsema PR, Singer W (1995) How precise is neuronal synchronization? Neural Comp. 7: 469-485.

    Google Scholar 

  • König P, Engel AK, Singer W (1996) Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19: 130-137.

    Article  PubMed  Google Scholar 

  • Kretzberg J, Egelhaaf M, Warzecha A-K (2001) Membrane potential fluctuations determine the precision of spike timing and synchronous activity: A model study. J. Comp. Neurosci. 10: 79-97.

    Article  Google Scholar 

  • Krüger J, Becker JD (1991) Recognizing the visual stimulus from neuronal discharges. Trends Neurosci. 14: 282-286.

    Article  PubMed  Google Scholar 

  • Lábos E (2000) Codes, operations, measurements and neural networks. Biosystems 58: 9-18.

    Article  PubMed  Google Scholar 

  • Larkman AU (1991) Dendritic morphology of pyramidal neurons of the visual cortex of the rat. III. Spine distributions. J. Comp. Neurol. 306: 332-343.

    PubMed  Google Scholar 

  • Lytton WW (1996) Optimizing synaptic conductance calculation for network simulations. Neural Computation 8: 501-509.

    PubMed  Google Scholar 

  • MacGregor RJ (1991) Sequential configuration model for firing patterns in local neural networks. Biol. Cybern. 65: 339-349.

    Article  PubMed  Google Scholar 

  • Magee JC (2000) Dendritic integration of excitatory synaptic input. Nature Rev. Neurosci. 1: 181-190.

    Article  Google Scholar 

  • Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268: 1503-1506.

    PubMed  Google Scholar 

  • Marŝálek P, Koch C, Maunsell J (1997) On the relationship between synaptic input and spike output jitter in individual neurons. Proc. Natl. Acad. Sci. USA 94: 735-740.

    Article  PubMed  Google Scholar 

  • McClurkin JW, Optican LM, Richmond BJ, Gawne TJ (1991) Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. Science 253: 675-677.

    PubMed  Google Scholar 

  • Murthy VN, Fetz EE (1994) Effects of input synchrony on the firing rate of a three-compartment cortical neuron model. Neural Comp. 6: 1111-1126.

    Google Scholar 

  • Noda H, Adey R (1970) Firing variability in cat association cortex during sleep and wakefulness. Brain Res. 18: 513-526.

    Article  PubMed  Google Scholar 

  • Nowak LG, Sanchez-Vives MV, McCormick DA (1997a) Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb. Cortex 7: 487-501.

    Article  PubMed  Google Scholar 

  • Nowak LG, Sanchez-Vives MV, McCormick DA (1997b) Membrane potential trajectory preceding visually evoked action potentials in cat’s visual cortex. Soc. Neurosci. Abstr. 23: 14.

    Google Scholar 

  • Panzeri S, Petersen RS, Schultz SR, Lebedev M, Diamond ME (2001) The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29: 769-777.

    Article  PubMed  Google Scholar 

  • Panzeri S, Schultz SR (2001) A unified approach to the study of temporal, correlational, and rate coding. Neural Comp. 13: 1311-1349.

    Article  Google Scholar 

  • Panzeri S, Schultz SR, Treves A, Rolls ET (1999) Correlations and the encoding of information in the nervous system. Proc. R. Soc. Lond. B Biol. Sci. 266: 1001-1012.

    Article  PubMed  Google Scholar 

  • Paré D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical neurons in vivo. J. Neurophysiol. 79: 1450-1460.

    PubMed  Google Scholar 

  • Prut Y, Vaadia E, Bergman H, Haalman I, Slovin H, Abeles M (1998) Spatiotemporal structure of cortical activity: Properties and behavioral relevance. J. Neurophysiol. 79: 2857-2874.

    PubMed  Google Scholar 

  • Reinagel P, Reid RC (2000) Temporal coding of visual information in the thalamus. J. Neurosci. 20: 5392-5400.

    PubMed  Google Scholar 

  • Riehle A, Grün S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278: 1950-1953.

    Google Scholar 

  • Rudolph M, Destexhe A (2001a) Correlation detection and resonance in neural systems with distributed noise sources. Phys. Rev. Lett. 86: 3662-3665.

    Article  PubMed  Google Scholar 

  • Rudolph M, Destexhe A (2001b) Do neocortical pyramidal neurons display stochastic resonance? J. Comp. Neurosci. 11: 19-42.

    Article  Google Scholar 

  • Schwindt PC, CrillW E (1997) Local and propagated dendritic action potentials evoked by glutamate iontophoresis on rat neocortical pyramidal neurons. J. Neurophysiol. 77: 2466-2483.

    PubMed  Google Scholar 

  • Segundo JP (2000) Some thoughts about neural coding and spike trains. Biosystems 58: 3-7.

    Article  PubMed  Google Scholar 

  • Segundo JP, Perkel DH, Moore GP (1966) Spike probability in neurones: Influence of temporal structure in the train of synaptic events. Kybernetik 3: 67-82.

    Article  PubMed  Google Scholar 

  • Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4: 569-579.

    Article  PubMed  Google Scholar 

  • Shadlen MN, Newsome WT (1995) Is there a signal in the noise? Curr. Opin. Neurobiol. 5: 248-250.

    Article  PubMed  Google Scholar 

  • Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J. Neurosci. 18: 3870-3896.

    PubMed  Google Scholar 

  • Shinomoto S, Sakai Y, Funahashi S (1999) The Ornstein-Uhlenbeck process does not reproduce spiking statistics of neurons in prefrontal cortex. Neural Comput. 11: 935-951.

    Article  PubMed  Google Scholar 

  • Smith DR, Smith GK (1965) A statistical analysis of the continuous activity of single cortical neurons in the cat unanesthetized isolated forebrain. Biophys. J. 5: 47-74.

    Google Scholar 

  • Softky WR (1994) Sub-millisecond coincidence detection in active dendritic trees. Neuroscience 58: 13-41.

    Article  PubMed  Google Scholar 

  • Softky WR (1995) Simple codes versus efficient codes. Curr. Opin. Neurobiol. 5: 239-247.

    Article  PubMed  Google Scholar 

  • Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13: 334-350.

    PubMed  Google Scholar 

  • Stein RB (1967) Some models of neuronal variability. Biophys. J. 7: 37-68.

    Google Scholar 

  • Stevens CF, Zador AM (1998) Input synchrony and the irregular firing of cortical neurons. Nature Neurosci. 1: 210-217.

    Article  PubMed  Google Scholar 

  • Stuart G, Spruston N, Sakmann B, Häusser M (1997) Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20: 125-131.

    Article  PubMed  Google Scholar 

  • Theunissen F, Miller JP (1995) Temporal encoding in nervous systems: A rigorous definition. J. Comput. Neurosci. 2: 149-162.

    PubMed  Google Scholar 

  • Tovée MJ, Rolls ET, Treves A, Bellis RP (1993) Information encoding and the responses of single neurons in the primate temporal visual cortex. J. Neurophysiol. 70: 640-654.

    PubMed  Google Scholar 

  • Traub RD, Miles R (1991) Neuronal Networks of the Hippocampus. Cambridge University Press.

  • Troyer TW, Miller KD (1997) Physiological gain leads to high ISI variability in a simple model of a cortical regular spiking cell. Neural. Comp. 9: 971-983.

    Google Scholar 

  • Tsodyks MV, Sejnowski T (1995) Rapid state switching in balanced cortical network models. Network 6: 111-124.

    Google Scholar 

  • Usher M, Stemmler M, Koch C, Olami Z (1994) Network amplification of local fluctuations causes high spike rate variability, fractal Tuning Neocortical Pyramidal Neurons 251 firing patterns and oscillatory local field potentials. Neural. Comp. 6: 795-836.

    Google Scholar 

  • Vaadia E, Haalman I, Abeles M, Bergman H, Prut Y, Slovin H, Aertsen A (1995) Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373: 515-518.

    Article  PubMed  Google Scholar 

  • van Vreeswijk C, Sompolinsky H (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274: 1724-1726.

    Article  PubMed  Google Scholar 

  • White EL (1989) Cortical Circuits. Birkhauser. Boston.

    Google Scholar 

  • Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370: 140-143.

    Article  PubMed  Google Scholar 

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  1. Unité de Neuroscience Intégratives et Computationnelles, CNRS, UPR-2191, Bat. 32-33, Avenue de la Terrasse, 91198, Gif-sur-Yvette, France

    Michael Rudolph & Alain Destexhe

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  1. Michael Rudolph
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  2. Alain Destexhe
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Rudolph, M., Destexhe, A. Tuning Neocortical Pyramidal Neurons between Integrators and Coincidence Detectors. J Comput Neurosci 14, 239–251 (2003). https://doi.org/10.1023/A:1023245625896

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