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The response of cortical neurons to in vivo-like input current: theory and experiment

I. Noisy inputs with stationary statistics

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Abstract

The study of several aspects of the collective dynamics of interacting neurons can be highly simplified if one assumes that the statistics of the synaptic input is the same for a large population of similarly behaving neurons (mean field approach). In particular, under such an assumption, it is possible to determine and study all the equilibrium points of the network dynamics when the neuronal response to noisy, in vivo-like, synaptic currents is known. The response function can be computed analytically for simple integrate-and-fire neuron models and it can be measured directly in experiments in vitro. Here we review theoretical and experimental results about the neural response to noisy inputs with stationary statistics. These response functions are important to characterize the collective neural dynamics that are proposed to be the neural substrate of working memory, decision making and other cognitive functions. Applications to the case of time-varying inputs are reviewed in a companion paper (Giugliano et al. in Biol Cybern, 2008). We conclude that modified integrate-and-fire neuron models are good enough to reproduce faithfully many of the relevant dynamical aspects of the neuronal response measured in experiments on real neurons in vitro.

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References

  • Abbott L (1999) Lapicque’s introduction of the integrate-and-fire model neuron (1907). Brain Res Bull 50: 303–304

    CAS  PubMed  Google Scholar 

  • Abbott L, Chance F (2005) Drivers and modulators from push-pull and balanced synaptic input. Prog Brain Res 149: 147–55

    CAS  PubMed  Google Scholar 

  • Abbott L, van Vreeswijk C (1993) Asynchronous states in networks of pulse-coupled oscillators. Phys Rev E 48: 1483–1490

    Google Scholar 

  • Amit D (1995) The hebbian paradigm reintegrated: local reverberations as internal representations. Behav Brain Sci 18: 617–657

    Article  Google Scholar 

  • Amit D, Brunel N (1997a) Dynamics of a recurrent network of spiking neurons before and following learning. Netw Comput Neural Syst 8: 373–404

    Google Scholar 

  • Amit D, Brunel N (1997b) Model of global spontaneous activity and local structured (learned) delay activity during delay. Cereb Cortex 7: 237–252

    CAS  PubMed  Google Scholar 

  • Amit DJ, Mongillo G (2003) Spike-driven synaptic dynamics generating working memory states. Neural Comput 15: 565–596

    PubMed  Google Scholar 

  • Amit D, Tsodyks M (1991a) Quantitative study of attractor neural network retrieving at low spike rates: I. Substrate-spikes, rates and neuronal gain. Network 2: 259–273

    Google Scholar 

  • Amit D, Tsodyks M (1991b) Quantitative study of attractor neural network retrieving at low spike rates: II. Low-rate retrieval in symmetric networks. Network 2: 275–294

    Google Scholar 

  • Amit D, Fusi S, Yakovlev V (1997) Paradigmatic working memory (attractor) cell in IT cortex. Neural Comput 9: 1071–1093

    CAS  PubMed  Google Scholar 

  • Arsiero M, Lüscher HR, Lundstrom B, Giugliano M (2007) The impact of input fluctuations on the frequency-current relationships of layer 5 pyramidal neurons in the rat medial prefrontal cortex. J Neurosci 27: 3274–3284

    CAS  PubMed  Google Scholar 

  • Benda J, Hennig R (2008) Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comput Neurosci 24: 113–136

    PubMed  Google Scholar 

  • Benda J, Herz A (2003) A universal model for spike-frequency adaptation. Neural Comput 15: 2523–2564

    PubMed  Google Scholar 

  • Braitenberg V, Schüz A (1991) Anatomy of the cortex. Springer, Berlin

    Google Scholar 

  • Brown LD, Tony Cai T, Das Gupta A (2001) Interval estimation for a binomial proportion. Stat Sci 16: 101–133

    Google Scholar 

  • Brunel N (2000a) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8: 183–208

    CAS  PubMed  Google Scholar 

  • Brunel N (2000b) Persistent activity and the single cell f-I curve in a cortical network model. Network 11: 261–280

    CAS  PubMed  Google Scholar 

  • Brunel N, Hakim V (1999) Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput 11: 1621–1671

    CAS  PubMed  Google Scholar 

  • Brunel N, van Rossum M (2007) Lapicque’s 1907 paper: from frogs to integrate-and-fire. Biol Cybern 97: 337–339

    PubMed  Google Scholar 

  • Brunel N, Sergi S (1998) Firing frequency of leaky integrate-and-fire neurons with synaptic currents dynamic. J Theor Biol 195: 87–95

    CAS  PubMed  Google Scholar 

  • Brunel N, Wang XJ (2001) Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J Comput Neurosci 11: 63–85

    CAS  PubMed  Google Scholar 

  • Burkitt A (2006) A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol Cybern 95: 1–19

    CAS  PubMed  Google Scholar 

  • Burkitt AN (2001) Balanced neurons: analysis of leaky integrate-and-fire neurons with reversal potentials. Biol Cybern 85: 247–255

    CAS  PubMed  Google Scholar 

  • Burkitt AN, Meffin H, Grayden DB (2003) Study of neuronal gain in a conductance-based leaky integrate-and-fire neuron model with balanced excitatory and inhibitory input. Biol Cybern 89: 119–125

    CAS  PubMed  Google Scholar 

  • Capocelli R, Ricciardi L (1971) Diffusion approximation and first passage time problem for a model neuron. Kybernetik 8: 214–223

    CAS  PubMed  Google Scholar 

  • Chacron M, Longtin A, Maler L (2001) Negative interspike interval correlations increase the neuronal capacity for encoding time-dependent stimuli. J Neurosci 21: 5328–5343

    CAS  PubMed  Google Scholar 

  • Chacron M, Lindner B, Longtin A (2007) Threshold fatigue and information transfer. J Comput Neurosci 23: 301–311

    PubMed  Google Scholar 

  • Chance F, Abbott L, Reyes A (2002) Gain modulation from background synaptic input. Neuron 35: 773–782

    CAS  PubMed  Google Scholar 

  • Connors B, Gutnick M, Prince D (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48: 1302–1320

    CAS  PubMed  Google Scholar 

  • Cox DR, Miller HD (1965) The theory of stochastic processes. Chapman & Hall, New York

    Google Scholar 

  • Curti E, Mongillo G, La Camera G, Amit DJ (2004) Mean-Field and capacity in realistic networks of spiking neurons storing sparsely coded random memories. Neural Comput 16: 2597–2637

    PubMed  Google Scholar 

  • DeFelipe J, Elston G, Fujita I, Fuster J, Harrison K, Hof P, Kawaguchi Y, Martin K, Rockland K, Thomson A, Wang S, White E, Yuste R (2002) Neocortical circuits: evolutionary aspects and specificity versus non-specificity of synaptic connections. Remarks, main conclusions and general comments and discussion. J Neurocytol 31: 387–416

    Google Scholar 

  • Del Giudice P, Fusi S, Mattia M (2003) Modelling the formation of working memory with networks of integrate-and-fire neurons connected by plastic synapses. J Physiol Paris 97: 659–681

    PubMed  Google Scholar 

  • Descalzo V, Nowak L, Brumberg J, McCormick D, Sanchez-Vives M (2005) Slow adaptation in fast spiking neurons in visual cortex. J Neurophysiol 93: 1111–1118

    CAS  PubMed  Google Scholar 

  • Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ (2001) Fluctuating dynamic conductances recreate in-vivo like activity in neocortical neurons. Neuroscience 107: 13–24

    CAS  PubMed  Google Scholar 

  • Doiron B, Lindner B, Longtin A, Maler L, Bastian J (2004) Oscillatory activity in electrosensory neurons increases with the spatial correlation of the stochastic input stimulus. Phys Rev Lett 93: 048,101

    Google Scholar 

  • Douglas R, Martin K (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419–451

    CAS  PubMed  Google Scholar 

  • Elston G (2002) Cortical heterogeneity: implications for visual processing and polysensory integration. J Neurocytol 31: 317–335

    PubMed  Google Scholar 

  • Ermentrout B (1998) Linearization of fI curves by adaptation. Neural Comput 10(7): 1721–1729

    CAS  PubMed  Google Scholar 

  • Fleidervish I, Friedman A, Gutnick M (1996) Slow inactiavation of Na + current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol (Cambridge) 493: 83–7

    CAS  Google Scholar 

  • Fourcaud N, Brunel N (2002) Dynamics of the firing probability of noisy integrate-and-fire neurons. Neural Comput 14: 2057–2110

    PubMed  Google Scholar 

  • Fourcaud-Trocmé N, Brunel N (2005) Dynamics of the instantaneous firing rate in response to changes in input statistics. J Comp Neurosci 18(3): 311–321

    Google Scholar 

  • Fourcaud-Trocmé N, Hansel H, van Vreeswijk C, Brunel N (2003) How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci 23: 11,628–11,640

    Google Scholar 

  • Funahashi S, Bruce C, Goldman-Rakic P (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61: 331–349

    CAS  PubMed  Google Scholar 

  • Fusi S, Mattia M (1999) Collective behavior of networks with linear (VLSI) integrate and fire neurons. Neural Comput 11: 633–652

    CAS  PubMed  Google Scholar 

  • Fusi S, Asaad W, Miller E, Wang X (2007) A neural circuit model of flexible sensorimotor mapping: learning and forgetting on multiple timescales. Neuron 54: 319–333

    CAS  PubMed  Google Scholar 

  • Fuster J, Jervey J (1981) Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. Science 212: 952–955

    CAS  PubMed  Google Scholar 

  • Fuster JM (1995) Memory in the cerebral cortex. MIT Press, Cambridge

    Google Scholar 

  • Gabbiani F, Koch C (1998) Principles of spike train analysis. In: Koch C, Segev I (eds) Methods in neuronal modeling: from synapses to networks, 2 edn. MIT Press, Cambridge, pp 313–360

    Google Scholar 

  • Gardiner CW (1985) Handbook of stochastic methods. Springer, Heidelberg

    Google Scholar 

  • Gershon E, Wiener M, Latham P, Richmond B (1998) Coding strategies in monkey V1 and inferior temporal cortices. J Neurophysiol 79: 1135–1144

    CAS  PubMed  Google Scholar 

  • Gerstner W (2000) Population dynamics of spiking neurons: fast transients, asynchronous states, and locking. Neural Comput 12: 43–90

    CAS  PubMed  Google Scholar 

  • Gigante G, Del Giudice P, Mattia M (2007a) Frequency-dependent response properties of adapting spiking neurons. Math Biosci 207: 336–351

    PubMed  Google Scholar 

  • Gigante G, Mattia M, Del Giudice P (2007b) Diverse population-bursting modes of adapting spiking neurons. Phys Rev Lett 98: 148,101

    Google Scholar 

  • Giugliano M, La Camera G, Rauch A, Lüscher HR, Fusi S (2002) Non-monotonic current-to-rate response function in a novel integrate-and-fire model neuron. In: Dorronsoro JR (ed) Proceedings of ICANN 2002, Lecture Notes in Computer Science, vol 2415. Springer, Heidelberg, pp 141–46

  • Giugliano M, Darbon P, Arsiero M, Lüscher HR, J Streit J (2004) Single-neuron discharge properties and network activity in dissociated cultures of neocortex. J Neurophysiol 92: 977–996

    CAS  PubMed  Google Scholar 

  • Giugliano M, La Camera G, Fusi S, Senn W (2008) The response function of cortical neurons: theory and experiment. II. Time-varying and spatially distributed inputs. Biol Cybern

  • Golowasch J, Goldman M, Abbott L, Marder E (2002) Failure of averaging in the construction of a conductance-based neuron model. J Neurophysiol 87: 1129–1131

    PubMed  Google Scholar 

  • Gupta A, Wang Y, Markram H (2000) Organizing Principles for a Diversity of GABAergic Interneurons and Synapses in the Neocortex. Science 287: 273–278

    CAS  PubMed  Google Scholar 

  • Gutkin B, Ermentrout G (1997) Dynamics of membrane excitability determine interspike interval variability: a link between spike generation mechanisms and cortical spike train statistics. Neural Comput 10(5): 1047–1065

    Google Scholar 

  • Hanson FB, Tuckwell HC (1983) Diffusion approximation for neural activity including synaptic reversal potentials. J Theor Neurobiol 2: 127–153

    Google Scholar 

  • Higgs M, Slee S, Spain W (2006) Diversity of gain modulation by noise in neocortical neurons: regulation by the slow afterhyperpolarization conductance. J Neurosci 26: 8787–8799

    CAS  PubMed  Google Scholar 

  • Holden AV (1976) Models of stochastic activity of neurons. Springer, New York

    Google Scholar 

  • Holt G, Softky W, Koch C, Douglas R (1996) Comparison of discharge variability in vitro and in vivo in cat cortex neurons. J Neurophysiol 75(5): 1806–1814

    CAS  PubMed  Google Scholar 

  • Johannesma PIM (1968) Diffusion models for the stochastic activity of neurons. In: Caianiello ER (eds) Neural networks. Springer, Berlin, pp 116–144

    Google Scholar 

  • Jolivet R, Lewis T, Gerstner W (2004) Generalized integrate-and-fire models of neuronal activity approximate spike trains of a detailed model to a high degree of accuracy. J Neurophysiol 92: 959–976

    PubMed  Google Scholar 

  • Jolivet R, Rauch A, Lüscher H, Gerstner W (2006) Predicting spike timing of neocortical pyramidal neurons by simple threshold models. J Comput Neurosci 21: 35–49

    PubMed  Google Scholar 

  • Jolivet R, Kobayashi R, Rauch A, Naud R, Shinomoto S, Gerstner W (2008) A benchmark test for a quantitative assessment of simple neuron models. J Neurosci Methods 169: 417–424

    PubMed  Google Scholar 

  • Knight BW (1972a) Dynamics of encoding of a populations of neurons. J Gen Physiol 59: 734–736

    CAS  PubMed  Google Scholar 

  • Knight BW (1972b) The relationship between the firing rate of a single neuron and the level of activity in a network of neurons. Experimental evidence for resonance enhancement in the population response. J Gen Physiol 59: 767

    CAS  PubMed  Google Scholar 

  • Koch K, Fuster J (1989) Unit activity in monkey parietal cortex related to haptic perception and temporary memory. Exp Brain Res 76: 292–306

    CAS  PubMed  Google Scholar 

  • Kostal L, Lánský P, Rospars J (2007) Neuronal coding and spiking randomness. Eur J Neurosci 26: 2693–2701

    PubMed  Google Scholar 

  • Kriener B, Tetzlaff T, Aertsen A, Diesmann M, Rotter S (2008) Correlations and population dynamics in cortical networks. Neural Comput 20: 2185–2226

    PubMed  Google Scholar 

  • Kumar A, Rotter S, Aertsen A (2008a) Conditions for propagating synchronous spiking and asynchronous firing rates in a cortical network model. J Neurosci 28: 5268–5280

    CAS  PubMed  Google Scholar 

  • Kumar A, Schrader S, Aertsen A, Rotter S (2008b) The high-conductance state of cortical networks. Neural Comput 20: 1–43

    PubMed  Google Scholar 

  • La Camera G (1999) Learning overlapping stimuli in a recurrent network of spiking neurons (in Italian). Università di Roma “La Sapienza– Roma, Italy

  • La Camera G, Rauch A, Senn W, Lüscher HR, Fusi S (2002) Firing rate adaptation without losing sensitivity to input fluctuations. In: Dorronsoro JR (ed) Proceedings of ICANN 2002, Lecture Notes in Computer Science, vol 2415, Springer, Heidelberg, pp 180–85

  • La Camera G, Rauch A, Senn W, Lüscher HR, Fusi S (2004a) Minimal models of adapted neuronal response to in vivo-like input currents. Neural Comput 16: 2101–2124

    PubMed  Google Scholar 

  • La Camera G, Senn W, Fusi S (2004b) Comparison between networks of conductance- and current-driven neurons: stationary spike rates and subthreshold depolarization. Neurocomputing 58-60C: 253–258

    Google Scholar 

  • La Camera G, Rauch A, Thurbon D, Lüscher HR, Senn W, Fusi S (2006) Multiple time scales of temporal response in pyramidal and fast spiking cortical neurons. J Neurophysiol 96: 3448–3464

    PubMed  Google Scholar 

  • Lánský P, Lánská V (1987) Diffusion approximation of the neuronal model with synaptic reversal potentials. Biol Cybern 56: 19–26

    PubMed  Google Scholar 

  • Lánský P, Sato S (1999) The stochastic diffusion models of nerve membrane depolarization and interspike interval generation. J Peripher Nerv Syst 4: 27–42

    PubMed  Google Scholar 

  • Lapicque L (1907) Recherches quantitatives sur lexcitation electrique des nerfs traitee comme une polarization. J Physiol Pathol Gen 9: 620–635

    Google Scholar 

  • Lapicque L (2007) Quantitative investigations of electrical nerve excitation treated as polarization. 1907. Biol Cybern 97: 341–349

    PubMed  Google Scholar 

  • Larkum M, Senn W, Lüscher H (2004) Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex 14: 1059–1070

    PubMed  Google Scholar 

  • Lee D, Port N, Kruse W, Georgopoulos A (1998) Variability and Correlated Noise in the Discharge of Neurons in Motor and Parietal Areas of the Primate Cortex. J Neurosci 18(3): 1161–1170

    CAS  PubMed  Google Scholar 

  • Lerchner A, Ursta C, Hertz J, Ahmadi M, Ruffiot P, Enemark S (2006) Response variability in balanced cortical networks. Neural Comput 18(3): 634–659

    PubMed  Google Scholar 

  • Lindner B, Schimansky-Geier L, Longtin A (2002) Maximizing spike train coherence or incoherence in the leaky integrate-and-fire model. Phys Rev E Stat Nonlin Soft Matter Phys 66: 031,916

    Google Scholar 

  • Lindner B, Chacron M, Longtin A (2005) Integrate-and-fire neurons with threshold noise: a tractable model of how interspike interval correlations affect neuronal signal transmission. Phys Rev E Stat Nonlin Soft Matter Phys 72: 021,911

    Google Scholar 

  • Liu YH, Wang XJ (2001) Spike-frequency adaptation of a generalized leaky integrate-and-fire model neuron. J Comput Neurosci 10: 25–45

    CAS  PubMed  Google Scholar 

  • London M, Segev I (2001) Synaptic scaling in vitro and in vivo. Nat Neurosci 4: 853–855

    CAS  PubMed  Google Scholar 

  • Lowen S, Teich M (1992) Auditory-nerve action potentials form a nonrenewal point process over short as well as long time scales. J Acoust Soc Am 92(2 Pt 1): 803–806

    CAS  PubMed  Google Scholar 

  • Mascaro M, Amit D (1999) Effective neural response function for collective population states. Netw Comput Neural Syst 10: 351–373

    CAS  Google Scholar 

  • Mattia M, Del Giudice P (2002) Population dynamics of interacting spiking neurons. Phys Rev E 66: 051,917

    Google Scholar 

  • McCormick DA, Connors BW, Lighthall JW, Prince D (1985) Comparative electrophysiology of pyramidal and sparsely stellate neurons of the neocortex. J Neurophysiol 54: 782–806

    CAS  PubMed  Google Scholar 

  • Meunier C, Segev I (2002) Playing the devil’s advocate: is the Hodgkin-Huxley model useful. Trends Neurosci 25: 558–563

    CAS  PubMed  Google Scholar 

  • Mezard M, Parisi G, Virasoro MA (1987) Spin glass theory and beyond. World Scientific, Singapore

    Google Scholar 

  • Miyashita Y (1988) Neural correlate of visual associative long-term mamory in the primate temporal cortex. Nature 335: 817–820

    CAS  PubMed  Google Scholar 

  • Miyashita Y, Chang H (1988) Neural correlate of pictorial short-term memory in the primate temporal cortex. Nature 331: 68–70

    CAS  PubMed  Google Scholar 

  • Mongillo G, Barak O, Tsodyks M (2008) Synaptic theory of working memory. Science 319: 1543–1546

    CAS  PubMed  Google Scholar 

  • Moreno R, de la Rocha J, Renart A, Parga N (2002) Response of spiking neurons to correlated inputs. Phys Rev Lett 89: 288,101

    Google Scholar 

  • Moreno-Bote R, Parga N (2004) Role of synaptic filtering on the firing response of simple model neurons. Phys Rev Lett 92: 028,102

    Google Scholar 

  • Moreno-Bote R, Parga N (2005) Membrane potential and response properties of populations of cortical neurons in the high conductance state. Phys Rev Lett 94: 088,103

    Google Scholar 

  • Moreno-Bote R, Renart A, Parga N (2008) Theory of input spike auto- and cross-correlations and their effect on the response of spiking neurons. Neural Comput 20: 1651–1705

    PubMed  Google Scholar 

  • Muller E, Buesing L, Schemmel J, Meier K (2007) Spike-frequency adapting neural ensembles: beyond mean adaptation and renewal theories. Neural Comput 19: 2958–3010

    PubMed  Google Scholar 

  • Nawrot M, Boucsein C, Rodriguez Molina V, Aertsen A, Grn S, Rotter S (2007) Serial interval statistics of spontaneous activity in cortical neurons. Neurocomputing 70: 1717–1722

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nykamp D, Tranchina D (2000) A population density approach that facilitates large-scale modeling of neural networks: analysis and an application to orientation tuning. J Comput Neurosci 8: 19–50

    CAS  PubMed  Google Scholar 

  • Ohki K, Reid R (2007) Specificity and randomness in the visual cortex. Curr Opin Neurobiol 17: 401–407

    CAS  PubMed  Google Scholar 

  • Oram M, Wiener M, Lestienne R, Richmond B (1999) Stochastic nature of precisely timed spike patterns in visual system neural responses. J Neurophysiol 81: 3021–3033

    CAS  PubMed  Google Scholar 

  • Powers R, Sawczuk A, Musick J, Binder M (1999) Multiple mechanisms of spike-frequency adaptation in motoneurones. J Physiol (Paris) 93: 101–114

    CAS  Google Scholar 

  • Rauch A, La Camera G, Lüscher HR, Senn W, Fusi S (2003) Neocortical cells respond as integrate-and-fire neurons to in vivo-like input currents. J Neurophysiol 90: 1598–1612

    PubMed  Google Scholar 

  • Reich D, Victor J, Knight B, Ozaki T, Kaplan A (1997) Response variability and timing precision of neuronal spike trains in vivo. J Neurophysiol 77: 2836–2841

    CAS  PubMed  Google Scholar 

  • Renart A, Brunel N, Wang XJ (2003) Mean-field theory of recurrent cortical networks: from irregularly spiking neurons to working memory. In: Feng J (ed) Computational Neuroscience: a comprehensive approach. CRC Press, Boca Raton

  • Reutimann J, Yakovlev V, Fusi S, Senn W (2004) Climbing neuronal activity as an event-based cortical representation of time. J Neurosci 24: 3295–3303

    CAS  PubMed  Google Scholar 

  • Richardson MJE (2004) The effects of synaptic conductance on the voltage distribution and firing rate of spiking neurons. Phys Rev E 69: 051,918

    Google Scholar 

  • Richardson MJE (2007) Firing-rate response of linear and nonlinear integrate-and-fire neurons to modulated current-based and conductance-based synaptic drive. Phys Rev E 76: 021,919

    Google Scholar 

  • Richardson MJE, Gerstner W (2005) Synaptic shot noise and conductance fluctuations affect the membrane voltage with equal significance. Neural Comput 17: 923–947

    PubMed  Google Scholar 

  • Rigotti M, Ben Dayan Rubin D, Wang X, Fusi S (2008) Internal representation of task rules by recurrent dynamics: the importance of the diversity of neural responses (Submitted)

  • Robinson H, Kawai N (1993) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49(3): 157–165

    CAS  PubMed  Google Scholar 

  • Rolls ET, Deco G (2001) The computational neuroscience of vision. Oxford University Press, Oxford

    Google Scholar 

  • van Rossum M, Turrigiano G, Nelson S (2002) Fast propagation of firing rates through layered networks of noisy neurons. J Neurosci 22: 1956–1966

    PubMed  Google Scholar 

  • Sah P (1996) Ca2+-activated K+ currents in neurons: types, physiological roles and modulation. Trends Neurosci 19: 150–154

    CAS  PubMed  Google Scholar 

  • Sakai Y, Funahashi S, Shinomoto S (1999) Temporally correlated inputs to leaky integrate-and-fire models can reproduce spiking statistics of cortical neurons. Neural Netw 12(7–): 1181–1190

    PubMed  Google Scholar 

  • Salinas E, Sejnowski TJ (2001) Gain modulation in the central nervous system: where behavior, neurophysiology and computation meet. Neuroscientist 7: 430–440

    CAS  PubMed  Google Scholar 

  • Salinas E, Sejnowski TJ (2002) Integrate-and-fire neurons driven by correlated stochastic input. Neural Comput 14: 2111–2155

    PubMed  Google Scholar 

  • Salinas E, Thier P (2000) Gain modulation: a major computational principle of the central nervous system. Neuron 27: 15–21

    CAS  PubMed  Google Scholar 

  • Sanchez-Vives M, Nowak L, McCormick D (2000) Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J Neurosci 20: 4286–4299

    CAS  PubMed  Google Scholar 

  • Sawczuk A, Powers R, Binder M (1997) Contribution of outward currents to spike frequency adaptation in hypoglossal motoneurons of the rat. J Physiol 78: 2246–2253

    CAS  Google Scholar 

  • Shadlen M, Newsome W (1998) The variable discharge of cortical neurons: implications for connectivity, computation and information coding. J Neurosci 18: 3870–3896

    CAS  PubMed  Google Scholar 

  • Sharp AA, O’Neil MB, Abbott LF, Marder E (1993) Dynamic clamp—computer generated conductances in real neurons. J Neurophysiol 69: 992–995

    CAS  PubMed  Google Scholar 

  • Shinomoto S, Shima K, Tanji J (2003) Differences in spiking patterns among cortical neurons. Neural Comput 15(12): 2823–2842

    PubMed  Google Scholar 

  • Silberberg G, Bethge M, Markram H, Pawelzik K, Tsodyks M (2004) Dynamics of population rate codes in ensembles of neocortical neurons. J Neurophysiol 91: 704–709

    CAS  PubMed  Google Scholar 

  • Stein RB (1965) A theoretical analysis of neuronal variability. Biophys J 5: 173–194

    CAS  PubMed  Google Scholar 

  • Svirskis G, Rinzel J (2000) Influence of temporal correlation of synaptic input on the rate and variability of firing in neurons. Biophys J 5: 629–637

    Google Scholar 

  • Thurley K, Senn W, Lüscher H (2008) Dopamine increases the gain of the input-output response of rat prefrontal pyramidal neurons. J Neurophysiol 99(6): 2985–97

    PubMed  Google Scholar 

  • Treves A (1993) Mean field analysis of neuronal spike dynamics. NETWORK 4: 259–284

    Article  Google Scholar 

  • Troyer T, Miller K (1997) Physiological gain leads to high ISI variability in a simple model of a cortical regular spiking cell. Neural Comput 9: 971–983

    CAS  PubMed  Google Scholar 

  • Tsodyks M, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. PNAS 94: 719–723

    CAS  PubMed  Google Scholar 

  • Tsodyks M, Pawelzik K, Markram H (1998) Neural networks with dynamic synapses. Neural Comput 10: 821–835

    CAS  PubMed  Google Scholar 

  • Tuckwell HC (1988) Introduction to theoretical neurobiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24: 10,440–10,453

    CAS  Google Scholar 

  • Victor J (2005) Spike train metrics. Curr Opin Neurobiol 15(5): 585–592

    CAS  PubMed  Google Scholar 

  • Vogels T, Abbott L (2005) Signal propagation and logic gating in networks of integrate-and-fire neurons. J Neurosci 25: 10,786–10,795

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Wang XJ (1998) Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J Neurophysiol 79: 1549–1566

    CAS  PubMed  Google Scholar 

  • Wang XJ (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19(21): 9587–9603

    CAS  PubMed  Google Scholar 

  • Wang XJ (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24(8): 455–463

    CAS  PubMed  Google Scholar 

  • Wang XJ (2002) Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36: 955–968

    CAS  PubMed  Google Scholar 

  • Wiener MC, Oram MW, Liu Z, Richmond BJ (2001) Consistency of encoding in monkey visual cortex. J Neurosci 21(20): 8210–8221

    CAS  PubMed  Google Scholar 

  • Wilbur W, Rinzel J (1983) A theoretical basis for large coefficient of variation and bimodality in neuronal interspike interval distribution. J Theor Biol 105: 345–368

    CAS  PubMed  Google Scholar 

  • Wilson F, Scalaidhe S, Goldman-Rakic P (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260: 1955–1958

    CAS  PubMed  Google Scholar 

  • Winograd M, Destexhe A, Sanchez-Vives M (2008) Hyperpolarization-activated graded persistent activity in the prefrontal cortex. Proc Natl Acad Sci USA 105: 7298–7303

    CAS  PubMed  Google Scholar 

  • Wong KF, Wang XJ (2006) A recurrent network mechanism of time integration in perceptual decisions. J Neurosci 26: 1314–1328

    CAS  PubMed  Google Scholar 

  • Yakovlev V, Fusi S, Berman E, Zohary E (1998) Inter-trial neuronal activity in infero-temporal cortex: a putative vehicle to generate long term associations. Nat Neurosci 1: 310–317

    CAS  PubMed  Google Scholar 

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Correspondence to Giancarlo La Camera.

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G. La Camera is supported by the Intramural Research Program of the National Institute of Mental Health. M. Giugliano is supported by the European Commission (FACETS Project FP6-2004-IST-FETPI-015879, EUSynapse Project LSHM-CT-2005-019055). W. Senn is supported by the Swiss National Science Foundation, grant No. 3152A0-105966. S. Fusi is supported by the Swiss National Science Foundation, grant PP00A-106556. The views expressed in this article do not necessarily represent the views of the NIMH, NIH, or the US Government.

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La Camera, G., Giugliano, M., Senn, W. et al. The response of cortical neurons to in vivo-like input current: theory and experiment. Biol Cybern 99, 279–301 (2008). https://doi.org/10.1007/s00422-008-0272-7

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  • DOI: https://doi.org/10.1007/s00422-008-0272-7

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