Potential mechanisms underlying intercortical signal regulation via cholinergic neuromodulators

Journal of Neuroscience

Volumn 35, Issue 45, 2015, Pages 15000-15014

  Lee, Jung H ^a   Whittington, Miles A ^b   Kopell, Nancy J ^a  

^a Boston University   (United States)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Cholinergic modulation; Computational model; Cortical rhythms; Dynamical regulation; Intercortical communication

Indexed keywords

KAINIC ACID; KAINIC ACID RECEPTOR;

ARTICLE; ASSOCIATION CORTEX; CHOLINERGIC SYNAPSE; CHOLINERGIC TRANSMISSION; COMPUTER MODEL; ELECTRIC POTENTIAL; GAMMA RHYTHM; NERVE CELL NETWORK; NEUROMODULATION; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SIMULATION; SPIKE WAVE; ARTIFICIAL NEURAL NETWORK; BETA RHYTHM; BRAIN CORTEX; CHOLINERGIC NERVE CELL; HUMAN; NERVE TRACT; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BETA RHYTHM; CEREBRAL CORTEX; CHOLINERGIC NEURONS; GAMMA RHYTHM; HUMANS; NEURAL NETWORKS (COMPUTER); NEURAL PATHWAYS; SIGNAL TRANSDUCTION;

EID: 84946944725     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0629-15.2015     Document Type: Article

References (64)

1. Ainsworth M, Lee S, Cunningham MO, Roopun AK, Traub RD, Kopell NJ, Whittington MA (2011) Dual gamma rhythm generators control interlaminar synchrony in auditory cortex. J Neurosci 31:17040-17051. CrossRef Medline
2. Akam TE, Kullmann DM (2012) Efficient “communication through coherence” requires oscillations structured to minimize interference between signals. PLoS Comput Biol 8:e1002760. CrossRef Medline
3. Arroyo S, Bennett C, Aziz D, Brown SP, Hestrin S (2012) Prolonged disynaptic inhibition in the cortex mediated by slow, Non- 7 nicotinic excitation of a specific subset of cortical interneurons. J Neurosci 32: 3859–3864. CrossRef Medline
4. Bastos AM, Vezoli J, Bosman CA, Schoffelen J-M, Oostenveld R, Dowdall JR, Fries P (2015) Visual areas exert feedforward and feedback influences through distinct frequency channels. Neuron 390–401.
5. Bauer M, Kluge C, Bach D, Bradbury D, Heinze HJ, Dolan, RJ, Driver J (2012) Cholinergic enhancement of visual attention and neural oscillations in the human brain. Curr Biol 22:397-402. CrossRef Medline
6. Börgers C, Kopell N (2005) Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons. Neural Comput 17:557-608. CrossRef Medline
7. Börgers C, Kopell NJ (2008) Gamma oscillations and stimulus selection. Neural Comput 20:383-414. CrossRef Medline
8. Börgers C, Franzesi G, LeBeau FEN, Boyden EE, Kopell NJ (2012) Minimal size of cell assemblies coordinated by gamma oscillations. PLoS Comput Biol 8:e1002362. CrossRef Medline
9. Bosman CA, Schoffelen JM, Brunet N, Oostenveld R, Bastos AM, Womelsdorf T, Rubehn B, Stieglitz T, De Weerd P, Fries P (2012) Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75:875-888. CrossRef Medline
10. Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315: 1860–1862. CrossRef Medline
11. Butler PD, Silverstein SM, Dakin SC (2008) Visual perception and its impairment in schizophrenia. Biol Psychiatry 64:40–47. CrossRef Medline
12. Chalk M, Herrero JL, Gieselmann MA, Delicato LS, Gotthardt S, Thiele A (2010) Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1. Neuron 66:114-125. CrossRef Medline
13. Debener S, Herrmann CS, Kranczioch C, Gembris D, Engel AK (2003) Topdown attentional processing enhances auditory evoked gamma band activity. Neuroreport 14:683-686. CrossRef Medline
14. Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1:195–230. CrossRef Medline
15. Donner TH, Siegel M, Fries P, Engel AK (2009) Buildup of choicepredictive activity in human motor cortex during perceptual decision making. Curr Biol 19:1581–1585. CrossRef Medline
16. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47. Medline
17. Flynn G, Alexander D, Harris A, Whitford T, Wong W, Galletly C, Silverstein S, Gordon E, Williams LM (2008) Increased absolute magnitude of gamma synchrony in first-episode psychosis. Shizophr Res 105:262–271. CrossRef Medline
18. Freeman J, Simoncelli, EP (2011) Metamers of the ventral stream. Nat Neurosci 14:1195–1201. CrossRef Medline
19. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480. CrossRef Medline
20. Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209-224. CrossRef Medline
21. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560–1563. CrossRef Medline
22. Ghitza O (2012) On the role of theta-driven syllabic parsing in decoding speech: Intelligibility of speech with a manipulated modulation spectrum. Front Psychol 3:238. Medline
23. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75–79. CrossRef Medline
24. Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) visual cortex during attention. Science 324:1207–1210. Medline
25. Gulledge AT, Park SB, Kawaguchi Y, Stuart GJ (2007) Heterogeneity of phasic cholinergic signaling in neocortical neurons. J Neurophysiol 97:2215–2229. CrossRef Medline
26. Haydar SN, Dunlop J (2010) Neuronal nicotinic acetylcholine receptorstargets for the development of drugs to treat cognitive impairment associated with schizophrenia and Alzheimer’s disease. Curr Top Med Chem 10:144-152. CrossRef Medline
27. Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A (2008) Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 454:1110-1114. CrossRef Medline
28. Jadi MP, Sejnowski TJ (2014) Cortical oscillations arise from contextual interactions that regulate sparse coding. Proc Natl Acad Sci U S A 111: 6780–6785. CrossRef Medline
29. Kramer MA, Roopun AK, Carracedo LM, Traub RD, Whittington MA, Kopell NJ (2008) Rhythm generation through period concatenation in rat somatosensory cortex. PLoS Comput Biol 4:e1000169. CrossRef Medline
30. Kruglikov I, Rudy B (2008) Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58:911–924. CrossRef Medline
31. Kwon JS, O’Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton ME, McCarley RW (1999) Gammafrequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry 56:1001–1005. CrossRef Medline
32. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 94:1904-1911. CrossRef Medline
33. Lee JH, Whittington MA, Kopell NJ (2013) Top-down beta rhythms support selective attention via inter-laminar interaction: a model. PLoS Comput Biol 9:e1003164. CrossRef Medline
34. Levy RB, Reyes AD, Aoki C (2008) Cholinergic modulation of local pyramid-interneuron synapses exhibiting divergent short-term dynamics in rat sensory cortex. Brain Res 1215:97–104. CrossRef Medline
35. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312–324. CrossRef Medline
36. Markov NT, Kennedy H (2013) The importance of being hierarchical. Curr Opin Neurobiol 23:187–194. CrossRef Medline
37. Martin LF, Kem WR, Freedman R (2004) Alpha-7 nicotinic receptor agonist: potential new candidates for the treatment of schizophrenia. Psychopharmacology (Berl) 174:54–64. Medline
38. Martin LF, Freedman R (2007) Schizophrenia and the alpha7 nicotinic acetylcholine receptor. Int Rev Neurobiol 78:225–246. CrossRef Medline
39. Mazzoni A, Panzeri S, Logothetis NK, Brunel N (2008) Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons. PLoS Comput Biol 4:e1000239. CrossRef Medline
40. Meltzer JA, Zaveri HP, Goncharova II, Distasio MM, Papademetris X, Spencer SS, Spencer DD, Constable RT (2008) Effects of working memory load on oscillatory power in human intracranial EEG. Cereb Cortex 18: 1843–1855. CrossRef Medline
41. Mitchell JF, Sundberg KA, Reynolds JH (2007) Differential attentiondependent response modulation across cell classes in macaque visual area V4. Neuron 55:131–141. CrossRef Medline
42. Mitra P, Bokil H (2007) Observed brain dynamics. New York: Oxford UP.
43. Otsuka T, Kawaguchi Y (2009) Cortical inhibitory cell types differentially form intralaminar and inter-laminar subnetworks with excitatory neurons. J Neurosci 29:10533–10540. CrossRef Medline
44. Parikh V, Kozak R, Martinez V, Sarter M (2007) Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56:141–154. CrossRef Medline
45. Pesaran B, Nelson MJ, Andersen RA (2008) Free choice activates a decision circuit between frontal and parietal cortex. Nature 453:406–409. CrossRef Medline
46. Peyrache A, Battaglia FP, Destexhe A (2011) Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc Natl Acad Sci U S A 108:17207–17212. CrossRef Medline
47. Reynolds JH, Chelazzi L (2004) Attentional modulation of visual processing. Annu Rev Neurosci 27:611-647. CrossRef Medline
48. Roopun AK, Middleton SJ, Cunningham MO, LeBeau FE, Bibbig A, Whittington MA, Traub RD (2006) A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortex. Proc Natl Acad Sci U S A 103:15646-15650. CrossRef Medline
49. Roopun AK, Lebeau FE, Rammell J, Cunningham MO, Traub RD, Whittington MA (2010) Cholinergic neuromodulation controls directed temporal communication in neocortex in vitro. Front Neural Circuits 4:8. Medline
50. Saalmann YB, Pigarev IN, Vidyasagar TR (2007) Neural mechanisms of visual attention: how top-down feedback highlights relevant locations. Science 316:1612–1615. CrossRef Medline
51. Saalmann YB, Pinsk MA, Wang L, Li X, Kastner S (2012) The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337:753–756. CrossRef Medline
52. Seth AK (2010) A MATLAB toolbox for Granger causal connectivity analysis. J Neurosci Methods 186:262–273. CrossRef Medline
53. Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53:735–746. CrossRef Medline
54. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586. CrossRef Medline
55. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW (2004) Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci U S A 101:17288-17293. CrossRef Medline
56. Thiele A (2013) Muscarinic signaling in the brain. Annu Rev Neurosci 36: 271–294. CrossRef Medline
57. Thomson AM, West DC, Hahn J, Deuchars J (1996) IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol 496:81–102. Medline
58. Traub RD, Bibbig A, LeBeau FE, Cunningham MO, Whittington MA (2005) Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model. J Physiol 562:3-8. CrossRef Medline
59. Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N (2008) Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol 99:2656-2671. CrossRef Medline
60. Wang X (2007) Neural coding strategies in auditory cortex. Hear Res 229: 81–93. CrossRef Medline
61. Wang XJ (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90:1195–1268. CrossRef Medline
62. 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. CrossRef Medline
63. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609-1612. CrossRef Medline
64. Xiang Z, Huguenard JR, Prince DA (1998) Cholinergic switching within neocortical inhibitory networks. Science 281:985–988. CrossRef Medline