Abstract
The response of a neuron in the visual cortex to stimuli of different contrast placed in its receptive field is commonly characterized using the contrast response curve. When attention is directed into the receptive field of a V4 neuron, its contrast response curve is shifted to lower contrast values (Reynolds et al., 2000). The neuron will thus be able to respond to weaker stimuli than it responded to without attention. Attention also increases the coherence between neurons responding to the same stimulus (Fries et al., 2001). We studied how the firing rate and synchrony of a densely interconnected cortical network varied with contrast and how they were modulated by attention. The changes in contrast and attention were modeled as changes in driving current to the network neurons.
We found that an increased driving current to the excitatory neurons increased the overall firing rate of the network, whereas variation of the driving current to inhibitory neurons modulated the synchrony of the network. We explain the synchrony modulation in terms of a locking phenomenon during which the ratio of excitatory to inhibitory firing rates is approximately constant for a range of driving current values.
We explored the hypothesis that contrast is represented primarily as a drive to the excitatory neurons, whereas attention corresponds to a reduction in driving current to the inhibitory neurons. Using this hypothesis, the model reproduces the following experimental observations: (1) the firing rate of the excitatory neurons increases with contrast; (2) for high contrast stimuli, the firing rate saturates and the network synchronizes; (3) attention shifts the contrast response curve to lower contrast values; (4) attention leads to stronger synchronization that starts at a lower value of the contrast compared with the attend-away condition. In addition, it predicts that attention increases the delay between the inhibitory and excitatory synchronous volleys produced by the network, allowing the stimulus to recruit more downstream neurons.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Albrecht DG, Hamilton DB (1982) Striate cortex of monkey and cat: contrast response function. J. Neurophysiol. 48: 217–237.
Albrecht DG, Geisler WS, Frazor RA, Crane AM (2002) Visual cortex neurons of monkeys and cats: Temporal dynamics of the contrast response function. J. Neurophysiol. 88: 888–913.
Alitto HJ, Usrey WM (2004) Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex. J. Neurophysiol. 91: 2797–2808.
Aradi I, Soltesz I (2002) Modulation of network behaviour by changes in variance in interneuronal properties. J. Physiol. 538: 220–251.
Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J. Neurosci. 21: 2687–2698.
Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. USA 99: 13222–13227.
Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90: 2987–3000.
Bichot NP, Rossi AF, Desimone R (2005) Parallel and serial neural mechanisms for visual search in macaque area V4. Science 308: 529–534.
Binzegger T, Douglas RJ, Martin KA (2004) A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24: 8441–8453.
Blasdel GG (1992a) Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J. Neurosci. 12: 3115–3138.
Blasdel GG (1992b) Orientation selectivity, preference, and continuity in monkey striate cortex. J. Neurosci. 12: 3139–3161.
Borgers C, Kopell N (2003) Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity. Neural. Comput. 15: 509–538.
Borgers C, Kopell N (2005) Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons. Neural. Comput. 17: 557–608.
Borgers C, Epstein S, Kopell NJ (2005) Background gamma rhythmicity and attention in cortical local circuits: A computational study. Proc. Natl. Acad. Sci. USA 102: 7002–7007.
Brunel N, Hakim V (1999) Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural. Comput. 11: 1621–1671.
Brunel N, Wang XJ (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J. Neurophysiol 90: 415–430.
Bush P, Sejnowski T (1996) Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models. J. Comput. Neurosci. 3: 91–110.
Callaway EM (1998) Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21: 47–74.
Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35: 773–782.
Constantinidis C, Goldman-Rakic PS (2002) Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J. Neurophysiol. 88: 3487–3497.
Cooper JR, Bloom FE, Roth RH (1996) The Biochemical Basis of Neuropharmacology, 7th Edition. Oxford: Oxford University Press.
Coull JT (2005) Psychopharmacology of human attention. In: Neurobiology of Attention (L Itti, G Rees, JK Tsotsos, eds.), 50–56.: Elsevier Academic Press, San Diego.
Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18: 193–222.
Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27: 419–451.
Feldman RS, Meyer JS, Quenzer LF (1997) Principles of Neuropsychopharmacology.: Sinauer Associates, Sunderland, Massachusetts
Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ (2003) Synaptic background noise controls the input/output characteristics of single cells in anin vitro model ofin vivo activity. Neuroscience 122: 811–829.
Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560–1563.
Geisler C, Brunel N, Wang XJ (2005) Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges. J. Neurophysiol 94: 4344–4361.
Gerald CF, Wheatley PO (1999) Applied Numerical Analysis, 6th ed.: Addison-Wesley, Reading, California.
Ghose GM, Ts’o DY (1997) Form processing modules in primate area V4. J. Neurophysiol. 77: 2191–2196.
Golomb D, Amitai Y (1997) Propagating neuronal discharges in neocortical slices: Computational and experimental study. J. Neurophysiol. 78: 1199–1211.
Golomb D, Hansel D (2000) The number of synaptic inputs and the synchrony of large, sparse neuronal networks. Neural. Comput. 12: 1095–1139.
Gray CM, Viana Di Prisco G (1997) Stimulus-dependent neuronal oscillations and local synchronization in striate cortex of the alert cat. J. Neurosci. 17: 3239–3253.
Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273–278.
Hansel D, van Vreeswijk C (2002) How noise contributes to contrast invariance of orientation tuning in cat visual cortex. J. Neurosci. 22: 5118–5128.
Hansel D, Mato G (2003) Asynchronous states and the emergence of synchrony in large networks of interacting excitatory and inhibitory neurons. Neural. Comput. 15: 1–56.
Hasselmo ME, McGaughy J (2004) High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog. Brain Res. 145: 207–231.
Hasselmo ME, Schnell E, Barkai E (1995) Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J. Neurosci. 15: 5249–5262.
Henrie JA, Shapley R (2005) LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol 94: 479–490.
Hubel DH (1959) Single unit activity in striate cortex of unrestrained cats. J. Physiol. 147: 226–238.
Hubel DH, Wiesel TN (1959) Receptive fields of single neurones in the cat’s striate cortex. J. Physiol. 148: 574–591.
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol. 160: 106–154.
Kayser C, Konig P (2004) Stimulus locking and feature selectivity prevail in complementary frequency ranges of V1 local field potentials. Eur. J. Neurosci. 19: 485–489.
Kohn A, Smith MA (2005) Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J. Neurosci. 25: 3661–3673.
Krnjevic K (1993) Central cholinergic mechanisms and function. Prog. Brain Res. 98: 285–292.
Luck SJ, Chelazzi L, Hillyard SA, Desimone R (1997) Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77: 24–42.
Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5: 793–807.
McAdams CJ, Maunsell JH (1999) Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19: 431–441.
Miller KD, Troyer TW (2002) Neural noise can explain expansive, power-law nonlinearities in neural response functions. J. Neurophysiol. 87: 653–659.
Milstein JA, Dalley JW, Robbins TW (2005) Neuropharmacology of Attention. In L. Itti, G. Rees, JK. Tsotsos, (eds), Neurobiology of Attention, pp.57–62. San Diego: Elsevier Academic Press.
Moran J, Desimone R (1985) Selective attention gates visual processing in the extrastriate cortex. Science 229: 782–784.
Ohzawa I, Sclar G, Freeman RD (1982) Contrast gain control in the cat visual cortex. Nature 298: 266–268.
Olufsen MS, Whittington MA, Camperi M, Kopell N (2003) New roles for the gamma rhythm: population tuning and preprocessing for the Beta rhythm. J. Comput. Neurosci. 14: 33–54.
Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical Recipes.: Cambridge University Press, Cambridge.
Rauch A, La Camera G, Luscher HR, Senn W, Fusi S (2003) Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. J. Neurophysiol. 90: 1598–1612.
Reynolds JH, Desimone R (2003) Interacting roles of attention and visual salience in V4. Neuron 37: 853–863.
Reynolds JH, Chelazzi L (2004) Attentional modulation of visual processing. Ann. Rev. of Neurosci. 27: 611–647.
Reynolds JH, Pasternak T, Desimone R (2000) Attention increases sensitivity of V4 neurons. Neuron 26: 703–714.
Richardson MJ (2004) Effects of synaptic conductance on the voltage distribution and firing rate of spiking neurons. Phys. Rev. E. Stat. Nonlin. Soft. Matter Phys. 69: 051918.
Rols G, Tallon-Baudry C, Girard P, Bertrand O, Bullier J (2001) Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey. Vis. Neurosci. 18: 527–540.
Rudolph M, Destexhe A (2003) The discharge variability of neocortical neurons during high-conductance states. Neuroscience 119: 855–873.
Salin PA, Bullier J (1995) Corticocortical connections in the visual system: Structure and function. Physiol. Rev. 75: 107–154.
Salinas E, Sejnowski T (2000) Impact of correlated synaptic input on output variability in simple neuronal models. J. Neurosci. 20: 6193–6209.
Sarter M, Hasselmo ME, Bruno JP, Givens B (2005) Unraveling the attentional functions of cortical cholinergic inputs: Interactions between signal-driven and cognitive modulation of signal detection. Brain Res. Brain Res. Rev. 48: 98–111.
Sclar G, Freeman RD (1982) Orientation selectivity in the cat’s striate cortex is invariant with stimulus contrast. Exp. Brain Res. 46: 457–461.
Shepherd GM, Stepanyants A, Bureau I, Chklovskii D, Svoboda K (2005) Geometric and functional organization of cortical circuits. Nat. Neurosci. 8: 782–790.
Song S, Sjostrom PJ, Reigl M, Nelson S, Chklovskii DB (2005) Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS. Biol. 3: e68.
Swadlow HA (2003) Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex. Cereb. Cortex 13: 25–32.
Taylor K, Mandon S, Freiwald WA, Kreiter AK (2005) Coherent Oscillatory Activity in Monkey Area V4 Predicts Successful Allocation of Attention. Cereb. Cortex 15: 1424–1437.
Tiesinga P, Fellous J-M, Salinas E, Jose JV, Sejnowski T (2004) Synchronization as a mechanism for attentional gain modulation. Neurocomputing 58–60: 641–646.
Tiesinga P, Fellous J-M, Salinas E, Jose J, Sejnowski T (2005) Inhibitory synchrony as a mechanism for attentional gain modulation. J. Physiol. (Paris) 98: 296–314.
Tiesinga PHE, Jose JV (2000) Robust gamma oscillations in networks of inhibitory hippocampal interneurons. Network-Computation in Neural Systems 11: 1–23.
Tiesinga PHE, Sejnowski TJ (2004) Rapid temporal modulation of synchrony by competition in cortical interneuron networks. Neural. Comput. 16: 251–275.
Tiesinga PHE, Jose JV, Sejnowski TJ (2000) Comparison of current-driven and conductance-driven neocortical model neurons with Hodgkin-Huxley voltage-gated channels. Physical Review E 62: 8413–8419.
Tiesinga PHE, Fellous JM, Jose JV, Sejnowski TJ (2001) Computational model of carbachol-induced delta, theta, and gamma oscillations in the hippocampus. Hippocampus 11: 251–274.
Traub RD, Contreras D, Cunningham MO, Murray H, LeBeau FE, Roopun A, Bibbig A, Wilent WB, Higley MJ, Whittington MA (2005) Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts. J. Neurophysiol. 93: 2194–2232.
Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrast-invariant orientation tuning in cat visual cortex: Thalamocortical input tuning and correlation-based intracortical connectivity. J. Neurosci. 18: 5908–5927.
Wang XJ, Buzsaki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16: 6402–6413.
Wang XJ, Tegner J, Constantinidis C, Goldman-Rakic PS (2004) Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. Proc. Natl. Acad. Sci. USA 101:1368–1373.
White JA, Chow CC, Ritt J, Soto-Trevino C, Kopell N (1998) Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. J. Comput. Neurosci. 5: 5–16.
Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612–615.
Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH (2000) Inhibition-based rhythms: Experimental and mathematical observations on network dynamics. Int. J. Psychophysiol. 38: 315–336.
Yoshimura Y, Dantzker JL, Callaway EM (2005) Excitatory cortical neurons form fine-scale functional networks. Nature 433: 868–873.
Author information
Authors and Affiliations
Corresponding author
Additional information
Action Editor: David Golomb
Rights and permissions
About this article
Cite this article
Buia, C., Tiesinga, P. Attentional modulation of firing rate and synchrony in a model cortical network. J Comput Neurosci 20, 247–264 (2006). https://doi.org/10.1007/s10827-006-6358-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10827-006-6358-0