Dendritic Nonlinearities Reduce Network Size Requirements and Mediate ON and OFF States of Persistent Activity in a PFC Microcircuit Model

PLoS Computational Biology

Volumn 10, Issue 7, 2014, Pages

  Papoutsi, Athanasia ^a,b   Sidiropoulou, Kyriaki ^a,b   Poirazi, Panayiota ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE NEURONS; BIOPHYSICAL MODEL; DENDRITICS; LARGE PARTS; MINIMUM NETWORKS; NETWORK SIZE; PERSISTENT ACTIVITIES; SMALL CLUSTERS; TECHNOLOGICAL ADVANCES; TUNABLES;

NEURONS;

ADENOSINE PHOSPHATE; DEOXYADENOSINE DIPHOSPHATE; N METHYL DEXTRO ASPARTIC ACID; 4 AMINOBUTYRIC ACID; N METHYLASPARTIC ACID;

ARTICLE; BRAIN FUNCTION; CELL INTERACTION; DENDRITE; DENDRITIC CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NONLINEAR SYSTEM; PREDICTION; PREFRONTAL CORTEX; PYRAMIDAL NERVE CELL; SHORT TERM MEMORY; SIMULATION; SPIKE WAVE; STIMULUS RESPONSE; SUPPORT VECTOR MACHINE; SYNAPTIC TRANSMISSION; WORKING MEMORY; ACTION POTENTIAL; BIOLOGICAL MODEL; BIOLOGY; BIOPHYSICS; COMPUTER SIMULATION; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; BIOPHYSICAL PHENOMENA; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; GAMMA-AMINOBUTYRIC ACID; MODELS, NEUROLOGICAL; N-METHYLASPARTATE; NEURONS;

EID: 84905457332     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003764     Document Type: Article

References (62)

1. Seung HS, (2009) Reading the book of memory: sparse sampling versus dense mapping of connectomes. Neuron 62: 17-29 doi:10.1016/j.neuron.2009.03.020.
2. Feldt S, Bonifazi P, Cossart R, (2011) Dissecting functional connectivity of neuronal microcircuits: experimental and theoretical insights. Trends Neurosci 34: 225-236 doi:10.1016/j.tins.2011.02.007.
3. Ko H, Hofer SB, Pichler B, Buchanan KA, Sjöström PJ, et al. (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473: 87-91 doi:10.1038/nature09880.
4. Yassin L, Benedetti BL, Jouhanneau J-S, Wen JA, Poulet JF, et al. (2010) An embedded subnetwork of highly active neurons in the neocortex. Neuron 68: 1043-1050 doi:10.1016/j.neuron.2010.11.029.
5. Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP, (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12: 919-926 doi:10.1038/nn.2337.
6. Perin R, Telefont M, Markram H, (2013) Computing the size and number of neuronal clusters in local circuits. Front Neuroanat 7: 1 doi:10.3389/fnana.2013.00001.
7. Otsuka T, Kawaguchi Y, (2008) Firing-pattern-dependent specificity of cortical excitatory feed-forward subnetworks. J Neurosci 28: 11186-11195 doi:10.1523/JNEUROSCI.1921-08.2008.
8. Wang Y, Markram H, Goodman PH, Berger TK, Ma J, et al. (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci 9: 534-542 doi:10.1038/nn1670.
9. Papoutsi A, Sidiropoulou K, Cutsuridis V, Poirazi P, (2013) Induction and modulation of persistent activity in a layer V PFC microcircuit model. Front Neural Circuits 7: 161 doi:10.3389/fncir.2013.00161.
10. Wang M, Yang Y, Wang C-J, Gamo NJ, Jin LE, et al. (2013) NMDA Receptors Subserve Persistent Neuronal Firing during Working Memory in Dorsolateral Prefrontal Cortex. Neuron 77: 736-749 doi:10.1016/j.neuron.2012.12.032.
11. Wang X-J, (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19: 9587-9603.
12. Sidiropoulou K, Lu F-M, Fowler MA, Xiao R, Phillips C, et al. (2009) Dopamine modulates an mGluR5-mediated depolarization underlying prefrontal persistent activity. Nat Neurosci 12: 190-199 doi:10.1038/nn.2245.
13. Gutkin BS, Laing CR, Colby CL, Chow CC, Ermentrout GB, (2001) Turning on and off with excitation: the role of spike-timing asynchrony and synchrony in sustained neural activity. J Comput Neurosci 11: 121-134.
14. Compte A, (2006) Computational and in vitro studies of persistent activity: edging towards cellular and synaptic mechanisms of working memory. Neuroscience 139: 135-151 doi:10.1016/j.neuroscience.2005.06.011.
15. Compte A, Brunel N, Goldman-Rakic PS, Wang X-J, (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10: 910-923.
16. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA, (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178 doi:10.1038/nature01171.
17. Lau P-M, Bi G-Q, (2005) Synaptic mechanisms of persistent reverberatory activity in neuronal networks. Proc Natl Acad Sci U S A 102: 10333-10338 doi:10.1073/pnas.0500717102.
18. Milojkovic BA, Zhou WL, Antic SD, (2007) Voltage and calcium transients in basal dendrites of the rat prefrontal cortex. J Physiol 585: 447-468 doi:10.1113/jphysiol.2007.142315.
19. Chalifoux JR, Carter AG, (2011) Glutamate spillover promotes the generation of NMDA spikes. J Neurosci 31: 16435-16446 doi:10.1523/JNEUROSCI.2777-11.2011.
20. Oikonomou KD, Short SM, Rich MT, Antic SD, (2012) Extrasynaptic glutamate receptor activation as cellular bases for dynamic range compression in pyramidal neurons. Front Physiol 3: 334 doi:10.3389/fphys.2012.00334.
21. Miller EK, (2000) The prefrontal cortex and cognitive control. Nat Rev Neurosci 1: 59-65 doi:10.1038/35036228.
22. Mann EO, Kohl MM, Paulsen O, (2009) Distinct roles of GABA(A) and GABA(B) receptors in balancing and terminating persistent cortical activity. J Neurosci 29: 7513-7518 doi:10.1523/JNEUROSCI.6162-08.2009.
23. Sidiropoulou K, Poirazi P, (2012) Predictive Features of Persistent Activity Emergence in Regular Spiking and Intrinsic Bursting Model Neurons. PLoS Comput Biol 8: e1002489 doi:10.1371/journal.pcbi.1002489.
24. Seamans JK, Durstewitz D, Christie BR, Stevens CF, Sejnowski TJ, (2001) Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci U S A 98: 301-306 doi:10.1073/pnas.011518798.
25. Wang J, O'Donnell P, (2001) D(1) dopamine receptors potentiate nmda-mediated excitability increase in layer V prefrontal cortical pyramidal neurons. Cereb Cortex 11: 452-462 doi:10.1093/cercor/11.5.452.
26. Gentet LJ, Avermann M, Matyas F, Staiger JF, Petersen CCH, (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65: 422-435 doi:10.1016/j.neuron.2010.01.006.
27. Crochet S, Poulet JF, Kremer Y, Petersen CCH, (2011) Synaptic mechanisms underlying sparse coding of active touch. Neuron 69: 1160-1175 doi:10.1016/j.neuron.2011.02.022.
28. Wang H, Stradtman GG, Wang XJ, Gao WJ, (2008) A specialized NMDA receptor function in layer 5 recurrent microcircuitry of the adult rat prefrontal cortex. Proc Natl Acad Sci U S A 105: 16791-16976 doi:10.1073/pnas.0804318105.
29. Tseng KY, O'Donnell P, (2005) Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cereb Cortex 15: 49-57 doi:10.1093/cercor/bhh107.
30. Shu Y, Hasenstaub AR, McCormick DA, (2003) Turning on and off recurrent balanced cortical activity. Nature 423: 288-293 doi:10.1038/nature01614.1.
31. Winograd M, Destexhe A, Sanchez-Vives MV, (2008) Hyperpolarization-activated graded persistent activity in the prefrontal cortex. Proc Natl Acad Sci U S A 105: 7298-7303 doi:10.1073/pnas.0800360105.
32. Major G, Larkum ME, Schiller J, (2013) Active properties of neocortical pyramidal neuron dendrites. Annu Rev Neurosci 36: 1-24 doi:10.1146/annurev-neuro-062111-150343.
33. McCormick DA, Shu Y, Hasenstaub AR, Sanchez-Vives MV, Badoual M, et al. (2003) Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb Cortex 13: 1219 doi:10.1093/cercor/bhg104.
34. Funahashi S, Bruce CJ, Goldman-Rakic PS, (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61: 331-349.
35. Miller EK, Erickson CA, Desimone R, (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16: 5154-5167.
36. Diester I, Nieder A, (2008) Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J Neurosci 28: 7737-7747 doi:10.1523/JNEUROSCI.1347-08.2008.
37. Myme CIO, Sugino K, Turrigiano GG, Nelson SB, (2003) The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. J Neurophysiol 90: 771-779 doi:10.1152/jn.00070.2003.
38. Lewis DA, González-Burgos G, (2006) Pathophysiologically based treatment interventions in schizophrenia. Nat Med 12: 1016-1022 doi:10.1038/nm1478.
39. Lim S, Goldman MS, (2013) Balanced cortical microcircuitry for maintaining information in working memory. Nat Neurosci 16: 1306-1314 doi:10.1038/nn.3492.
40. Schiller J, Major G, Koester HJ, Schiller Y, (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404: 285-289 doi:10.1038/35005094.
41. Major G, Polsky A, Denk W, Schiller J, Tank DW, (2008) Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J Neurophysiol 99: 2584-2601 doi:10.1152/jn.00011.2008.
42. Larkum ME, Nevian T, Sandler M, Polsky A, Schiller J, (2009) Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325: 756-760 doi:10.1126/science.1171958.
43. Palmer LM, Shai AS, Reeve JE, Anderson HL, Paulsen O, et al. (2014) NMDA spikes enhance action potential generation during sensory input. Nat Neurosci pp. 1-10 doi:10.1038/nn.3646.
44. Murayama M, Pérez-Garci E, Nevian T, Bock T, Senn W, et al. (2009) Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457: 1137-1141 doi:10.1038/nature07663.
45. Smith SL, Smith IT, Branco T, Häusser M, (2013) Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 503: 115-120 doi:10.1038/nature12600.
46. Xu N, Harnett MT, Williams SR, Huber D, O'Connor DH, et al. (2012) Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492: 247-251 doi:10.1038/nature11601.
47. Börgers C, Talei Franzesi G, Lebeau FEN, Boyden ES, Kopell NJ, (2012) Minimal size of cell assemblies coordinated by gamma oscillations. PLoS Comput Biol 8: e1002362 doi:10.1371/journal.pcbi.1002362.
48. Oswald AM, Doiron B, Rinzel J, Reyes AD, (2009) Spatial profile and differential recruitment of GABAB modulate oscillatory activity in auditory cortex. J Neurosci 29: 10321-10334 doi:10.1523/JNEUROSCI.1703-09.2009.
49. Litwin-Kumar A, Doiron B, (2012) Slow dynamics and high variability in balanced cortical networks with clustered connections. Nat Neurosci 15: 1498-1505 doi:10.1038/nn.3220.
50. Sanchez-Vives MV, McCormick DA, (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-1034 doi:10.1038/79848.
51. Li CY, Poo MM, Dan Y, (2009) Burst spiking of a single cortical neuron modifies global brain state. Science 324: 643-646 doi:10.1126/science.1169957.
52. Yamada M, Pita MDCR, Iijima T, Tsutsui KI, (2010) Rule-dependent anticipatory activity in prefrontal neurons. Neurosci Res 67: 162-171 doi:10.1016/j.neures.2010.02.011.
53. Balleine BW, Leung BK, Ostlund SB, (2011) The orbitofrontal cortex, predicted value, and choice. Ann N Y Acad Sci 1239: 43-50 doi:10.1111/j.1749-6632.2011.06270.x.
54. Tziridis K, Dicke PW, Thier P, (2009) The role of the monkey dorsal pontine nuclei in goal-directed eye and hand movements. J Neurosci 29: 6154-6166 doi:10.1523/JNEUROSCI.0581-09.2009.
55. Sanders H, Berends M, Major G, Goldman MS, Lisman JE, (2013) NMDA and GABAB (KIR) conductances: the "perfect couple" for bistability. J Neurosci 33: 424-429 doi:10.1523/JNEUROSCI.1854-12.2013.
56. Van Wingerden M, Vinck M, Tijms V, Ferreira IRS, Jonker AJ, et al. (2012) NMDA receptors control cue-outcome selectivity and plasticity of orbitofrontal firing patterns during associative stimulus-reward learning. Neuron 76: 813-825 doi:10.1016/j.neuron.2012.09.039.
57. Haider B, Duque A, Hasenstaub AR, McCormick DA, (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26: 4535-4545 doi:10.1523/JNEUROSCI.5297-05.2006.
58. Hines ML, Carnevale NT, (2001) NEURON: a tool for neuroscientists. Neuroscientist 7: 123-135.
59. Kuroda M, Yokofujita J, Murakami K, (1998) An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus. Prog Neurobiol 54: 417-458.
60. Yoshimura Y, Dantzker JLM, Callaway EM, (2005) Excitatory cortical neurons form fine-scale functional networks. Nature 433: 868-873 doi:10.1038/nature03252.
61. Petreanu L, Mao T, Sternson SM, Svoboda K, (2009) The subcellular organization of neocortical excitatory connections. Nature 457: 1142-1145 doi:10.1038/nature07709.
62. Yamashita T, Pala A, Pedrido L, Kremer Y, Welker E, et al. (2013) Membrane potential dynamics of neocortical projection neurons driving target-specific signals. Neuron 80: 1477-1490 doi:10.1016/j.neuron.2013.10.059.