Basal forebrain activation controls contrast sensitivity in primary visual cortex

BMC Neuroscience

Volumn 14, Issue , 2013, Pages

  Bhattacharyya, Anwesha ^a   Veit, Julia ^a   Kretz, Robert ^a   Bondar, Igor ^b   Rainer, Gregor ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b INSTITUTE OF HIGHER NERVOUS ACTIVITY AND NEUROPHYSIOLOGY   (Russian Federation)

Author keywords

Cholinergic; Gamma oscillations; Orientation tuning

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CONTRAST SENSITIVITY; CONTROLLED STUDY; FOREBRAIN; LOCAL FIELD POTENTIAL; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; ORIENTATION; SPECTRAL SENSITIVITY; STIMULUS RESPONSE; STRIATE CORTEX;

ANIMALS; BRAIN MAPPING; CONTRAST SENSITIVITY; ELECTRIC STIMULATION; EVOKED POTENTIALS, VISUAL; ORIENTATION; PHOTIC STIMULATION; PROSENCEPHALON; SPECTRUM ANALYSIS; TUPAIIDAE; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84878191693     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-14-55     Document Type: Article

References (83)

1. Lehmann J, Nagy JI, Atmadia S, Fibiger HC. The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat. Neuroscience 1980, 5(7):1161-1174. 10.1016/0306-4522(80)90195-5, 7402465.
2. Mesulam MM, Mufson EJ, Levey AI, Wainer BH. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 1983, 214(2):170-197. 10.1002/cne.902140206, 6841683.
3. Baxter MG, Chiba AA. Cognitive functions of the basal forebrain. Curr Opin Neurobiol 1999, 9(2):178-183. 10.1016/S0959-4388(99)80024-5, 10322180.
4. Deco G, Thiele A. Attention: oscillations and neuropharmacology. Eur J Neurosci 2009, 30(3):347-354. 10.1111/j.1460-9568.2009.06833.x, 2777251, 19614749.
5. Hasselmo ME, Sarter M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 2011, 36(1):52-73. 10.1038/npp.2010.104, 2992803,2992803, 20668433.
6. Dotigny F, Ben Amor AY, Burke M, Vaucher E. Neuromodulatory role of acetylcholine in visually-induced cortical activation: behavioral and neuroanatomical correlates. Neuroscience 2008, 154(4):1607-1618. 10.1016/j.neuroscience.2008.04.030, 18515016.
7. Fine A, Hoyle C, Maclean CJ, Levatte TL, Baker HF, Ridley RM. Learning impairments following injection of a selective cholinergic immunotoxin, ME20.4 IgG-saporin, into the basal nucleus of Meynert in monkeys. Neuroscience 1997, 81(2):331-343. 10.1016/S0306-4522(97)00208-X, 9300425.
8. Ridley RM, Baker HF, Leow-Dyke A, Cummings RM. Further analysis of the effects of immunotoxic lesions of the basal nucleus of Meynert reveals substantial impairment on visual discrimination learning in monkeys. Brain Res Bull 2005, 65(5):433-442. 10.1016/j.brainresbull.2005.02.025, 15833598.
9. Conner JM, Culberson A, Packowski C, Chiba AA, Tuszynski MH. Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 2003, 38(5):819-829. 10.1016/S0896-6273(03)00288-5, 12797965.
10. Klinkenberg I, Blokland A. The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev 2010, 34(8):1307-1350. 10.1016/j.neubiorev.2010.04.001, 20398692.
11. Klinkenberg I, Sambeth A, Blokland A. Acetylcholine and attention. Behav Brain Res 2011, 221(2):430-442. 10.1016/j.bbr.2010.11.033, 21108972.
12. Ridley RM, Bowes PM, Baker HF, Crow TJ. An involvement of acetylcholine in object discrimination learning and memory in the marmoset. Neuropsychologia 1984, 22(3):253-263. 10.1016/0028-3932(84)90073-3, 6431311.
13. Aggelopoulos NC, Liebe S, Logothetis NK, Rainer G. Cholinergic control of visual categorization in macaques. Front Behav Neurosci 2011, 5:73. 3215973, 22110428.
14. Smith AT, Baker-Short CM. Pharmacological separation of mechanisms contributing to human contrast sensitivity. Vis Neurosci 1993, 10(6):1073-1079. 10.1017/S095252380001018X, 8257664.
15. Bentley P, Vuilleumier P, Thiel CM, Driver J, Dolan RJ. Cholinergic enhancement modulates neural correlates of selective attention and emotional processing. NeuroImage 2003, 20(1):58-70. 10.1016/S1053-8119(03)00302-1, 14527570.
16. Bentley P, Driver J, Dolan RJ. Cholinergic modulation of cognition: insights from human pharmacological functional neuroimaging. Prog Neurobiol 2011, 94(4):360-388. 10.1016/j.pneurobio.2011.06.002, 3382716, 21708219.
17. Hars B, Maho C, Edeline JM, Hennevin E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience 1993, 56(1):61-74. 10.1016/0306-4522(93)90562-T, 8232918.
18. Edeline JM, Hars B, Maho C, Hennevin E. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Exp Brain Res 1994, 97(3):373-386.
19. Kang JI, Vaucher E. Cholinergic pairing with visual activation results in long-term enhancement of visual evoked potentials. PLoS One 2009, 4(6):e5995. 10.1371/journal.pone.0005995, 2696093, 19543405.
20. Puckett AC, Pandya PK, Moucha R, Dai W, Kilgard MP. Plasticity in the rat posterior auditory field following nucleus basalis stimulation. J Neurophysiol 2007, 98(1):253-265. 10.1152/jn.01309.2006, 17460101.
21. Reed A, Riley J, Carraway R, Carrasco A, Perez C, Jakkamsetti V, Kilgard MP. Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 2011, 70(1):121-131. 10.1016/j.neuron.2011.02.038, 21482361.
22. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 1999, 19(5):1599-1609.
23. Shinoe T, Matsui M, Taketo MM, Manabe T. Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 2005, 25(48):11194-11200. 10.1523/JNEUROSCI.2338-05.2005, 16319319.
24. McCoy P, Norton TT, McMahon LL. Layer 2/3 synapses in monocular and binocular regions of tree shrew visual cortex express mAChR-dependent long-term depression and long-term potentiation. J Neurophysiol 2008, 100(1):336-345. 10.1152/jn.01134.2007, 2493490, 18480372.
25. Sillito AM, Kemp JA. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res 1983, 289(1-2):143-155.
26. Murphy PC, Sillito AM. Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience 1991, 40(1):13-20. 10.1016/0306-4522(91)90170-S, 2052147.
27. Sato H, Hata Y, Masui H, Tsumoto T. A functional role of cholinergic innervation to neurons in the cat visual cortex. J Neurophysiol 1987, 58(4):765-780.
28. Disney AA, Aoki C, Hawken MJ. Gain modulation by nicotine in macaque v1. Neuron 2007, 56(4):701-713. 10.1016/j.neuron.2007.09.034, 2875676, 18031686.
29. Disney AA, Aoki C, Hawken MJ. Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition. J Neurophysiol 2012, 108(7):1907-1923. 10.1152/jn.00188.2012, 22786955.
30. Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A. Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 2008, 454(7208):1110-1114. 10.1038/nature07141, 2666819, 18633352.
31. Soma S, Shimegi S, Osaki H, Sato H. Cholinergic modulation of response gain in the primary visual cortex of the macaque. J Neurophysiol 2011, 107(1):283-291.
32. Jimenez-Capdeville ME, Dykes RW, Myasnikov AA. Differential control of cortical activity by the basal forebrain in rats: a role for both cholinergic and inhibitory influences. J Comp Neurol 1997, 381(1):53-67. 10.1002/(SICI)1096-9861(19970428)381:1<53::AID-CNE5>3.0.CO;2-J, 9087419.
33. Goard M, Dan Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 2009, 12(11):1444-1449. 10.1038/nn.2402, 3576925, 19801988.
34. Kuo MC, Rasmusson DD, Dringenberg HC. Input-selective potentiation and rebalancing of primary sensory cortex afferents by endogenous acetylcholine. Neuroscience 2009, 163(1):430-441. 10.1016/j.neuroscience.2009.06.026, 19531370.
35. Laxton AW, Lozano AM. Deep brain stimulation for the treatment of Alzheimer disease and dementias. World Neurosurg 2012,
36. Hardenacke K, Kuhn J, Lenartz D, Maarouf M, Mai JK, Bartsch C, Freund HJ, Sturm V. Stimulate or degenerate: deep brain stimulation of the nucleus basalis meynert in Alzheimer dementia. World Neurosurg 2012,
37. Bhattacharyya A, Biessmann F, Veit J, Kretz R, Rainer G. Functional and laminar dissociations between muscarinic and nicotinic cholinergic neuromodulation in the tree shrew primary visual cortex. Eur J Neurosci 2012, 35(8):1270-1280. 10.1111/j.1460-9568.2012.08052.x, 22487086.
38. Freund TF, Meskenaite V. gamma-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc Natl Acad Sci U S A 1992, 89(2):738-742. 10.1073/pnas.89.2.738, 48314, 1731348.
39. Levey AI, Hallanger AE, Wainer BH. Cholinergic nucleus basalis neurons may influence the cortex via the thalamus. Neurosci Lett 1987, 74(1):7-13. 10.1016/0304-3940(87)90042-5, 2436108.
40. Sclar G, Maunsell JH, Lennie P. Coding of image contrast in central visual pathways of the macaque monkey. Vision Res 1990, 30(1):1-10. 10.1016/0042-6989(90)90123-3, 2321355.
41. Albrecht DG, Hamilton DB. Striate cortex of monkey and cat: contrast response function. J Neurophysiol 1982, 48(1):217-237.
42. Shapley R, Hawken M, Xing D. The dynamics of visual responses in the primary visual cortex. Prog Brain Res 2007, 165:21-32.
43. Bosking WH. V1 neurons: in tune with the neighbors. Neuron 2008, 57(5):627-628. 10.1016/j.neuron.2008.02.026, 18341982.
44. Tigges J, Shantha TR. Atlas of the tree shrew 1969, Baltimore, USA: Williams and Wilkins Company.
45. Rye DB, Wainer BH, Mesulam MM, Mufson EJ, Saper CB. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 1984, 13(3):627-643. 10.1016/0306-4522(84)90083-6, 6527769.
46. Muller CM, Singer W. Acetylcholine-induced inhibition in the cat visual cortex is mediated by a GABAergic mechanism. Brain Res 1989, 487(2):335-342. 10.1016/0006-8993(89)90837-8, 2731048.
47. Zinke W, Roberts MJ, Guo K, McDonald JS, Robertson R, Thiele A. Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized Marmoset monkeys. Eur J Neurosci 2006, 24(1):314-328. 10.1111/j.1460-9568.2006.04882.x, 1888486, 16882027.
48. Katzner S, Busse L, Carandini M. GABAA inhibition controls response gain in visual cortex. J Neurosci 2011, 31(16):5931-5941. 10.1523/JNEUROSCI.5753-10.2011, 3083851, 21508218.
49. Atallah BV, Bruns W, Carandini M, Scanziani M. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 2012, 73(1):159-170. 10.1016/j.neuron.2011.12.013, 22243754.
50. Cano M, Bezdudnaya T, Swadlow HA, Alonso JM. Brain state and contrast sensitivity in the awake visual thalamus. Nat Neurosci 2006, 9(10):1240-1242. 10.1038/nn1760, 16964255.
51. Alitto HJ, Moore BD, Rathbun DL, Usrey WM. A comparison of visual responses in the lateral geniculate nucleus of alert and anaesthetized macaque monkeys. J Physiol 2011, 589(Pt 1):87-99. 3039262, 20603332.
52. McCormick DA, Prince DA. Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci U S A 1985, 82(18):6344-6348. 10.1073/pnas.82.18.6344, 391050, 3862134.
53. McCormick DA, Prince DA. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 1986, 375:169-194. 1182754, 2879035.
54. Krnjevic K, Pumain R, Renaud L. The mechanism of excitation by acetylcholine in the cerebral cortex. J Physiol 1971, 215(1):247-268. 1331876, 5579661.
55. Disney AA, Domakonda KV, Aoki C. Differential expression of muscarinic acetylcholine receptors across excitatory and inhibitory cells in visual cortical areas V1 and V2 of the macaque monkey. J Comp Neurol 2006, 499(1):49-63. 10.1002/cne.21096, 16958109.
56. Freund TF, Gulyas AI. GABAergic interneurons containing calbindin D28K or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J Comp Neurol 1991, 314(1):187-199. 10.1002/cne.903140117, 1686776.
57. Disney AA, Aoki C. Muscarinic acetylcholine receptors in macaque V1 are most frequently expressed by parvalbumin-immunoreactive neurons. J Comp Neurol 2008, 507(5):1748-1762. 10.1002/cne.21616, 2845159, 18265004.
58. Prusky GT, Shaw C, Cynader MS. Nicotine receptors are located on lateral geniculate nucleus terminals in cat visual cortex. Brain Res 1987, 412(1):131-138. 10.1016/0006-8993(87)91447-8, 3607444.
59. Gritti I, Mainville L, Jones BE. Codistribution of GABA- with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J Comp Neurol 1993, 329(4):438-457. 10.1002/cne.903290403, 8454735.
60. Gritti I, Mainville L, Mancia M, Jones BE. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 1997, 383(2):163-177. 10.1002/(SICI)1096-9861(19970630)383:2<163::AID-CNE4>3.0.CO;2-Z, 9182846.
61. Henny P, Jones BE. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 2008, 27(3):654-670. 10.1111/j.1460-9568.2008.06029.x, 2426826, 18279318.
62. Wilson NR, Runyan CA, Wang FL, Sur M. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 2012, 488(7411):343-348. 10.1038/nature11347, 3653570, 22878717.
63. Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH. The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 1987, 262(1):105-124. 10.1002/cne.902620109, 2442206.
64. Thomson AM. Neocortical layer 6, a review. Front Neuroanat 2010, 4:13. 2885865, 20556241.
65. Lam YW, Sherman SM. Functional organization of the somatosensory cortical layer 6 feedback to the thalamus. Cereb Cortex 2010, 20(1):13-24. 10.1093/cercor/bhp077, 2792186, 19447861.
66. Dringenberg HC, Sparling JS, Frazer J, Murdoch J. Generalized cortex activation by the auditory midbrain: Mediation by acetylcholine and subcortical relays. Exp Brain Res 2006, 174(1):114-123. 10.1007/s00221-006-0427-5, 16575576.
67. Metherate R, Cox CL, Ashe JH. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 1992, 12(12):4701-4711.
68. Cape EG, Jones BE. Differential modulation of high-frequency gamma-electroencephalogram activity and sleep-wake state by noradrenaline and serotonin microinjections into the region of cholinergic basalis neurons. J Neurosci 1998, 18(7):2653-2666.
69. Cape EG, Manns ID, Alonso A, Beaudet A, Jones BE. Neurotensin-induced bursting of cholinergic basal forebrain neurons promotes gamma and theta cortical activity together with waking and paradoxical sleep. J Neurosci 2000, 20(22):8452-8461.
70. Lin SC, Gervasoni D, Nicolelis MA. Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles. J Neurophysiol 2006, 96(6):3209-3219. 10.1152/jn.00524.2006, 16928796.
71. Buhl EH, Tamas G, Fisahn A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 1998, 513(Pt 1):117-126. 2231263, 9782163.
72. Oke OO, Magony A, Anver H, Ward PD, Jiruska P, Jefferys JG, Vreugdenhil M. High-frequency gamma oscillations coexist with low-frequency gamma oscillations in the rat visual cortex in vitro. Eur J Neurosci 2010, 31(8):1435-1445. 10.1111/j.1460-9568.2010.07171.x, 20384769.
73. Rodriguez R, Kallenbach U, Singer W, Munk MH. Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. J Neurosci 2004, 24(46):10369-10378. 10.1523/JNEUROSCI.1839-04.2004, 15548651.
74. Luiten PG, Gaykema RP, Traber J, Spencer DG. Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Phaseolus vulgaris leucoagglutinin. Brain Res 1987, 413(2):229-250. 10.1016/0006-8993(87)91014-6, 3300852.
75. Buzsaki G, Wang XJ. Mechanisms of gamma oscillations. Annu Rev Neurosci 2012, 35:203-225. 10.1146/annurev-neuro-062111-150444, 22443509.
76. Borgers C, Epstein S, Kopell NJ. Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model. Proc Natl Acad Sci U S A 2008, 105(46):18023-18028. 10.1073/pnas.0809511105, 2584712, 19004759.
77. Battaglia D, Hansel D. Synchronous chaos and broad band gamma rhythm in a minimal multi-layer model of primary visual cortex. PLoS Comput Biol 2011, 7(10):e1002176. 10.1371/journal.pcbi.1002176, 3188510, 21998568.
78. Wang Y, Fujita I, Murayama Y. Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex. Nat Neurosci 2000, 3(8):807-813. 10.1038/77712, 10903574.
79. Leventhal AG, Wang Y, Pu M, Zhou Y, Ma Y. GABA and its agonists improved visual cortical function in senescent monkeys. Science 2003, 300(5620):812-815. 10.1126/science.1082874, 12730605.
80. Veit J, Bhattacharyya A, Kretz R, Rainer G. Neural response dynamics of spiking and local field potential activity depend on CRT monitor refresh rate in the tree shrew primary visual cortex. J Neurophysiol 2011, 106(5):2303-2313. 10.1152/jn.00388.2011, 21849615.
81. Wong-Riley MT, Norton TT. Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew:normal patterns and the effect of retinal impulse blockage. J Comp Neurol 1988, 272(4):562-578. 10.1002/cne.902720409, 2843584.
82. Lin SC, Nicolelis MA. Neuronal ensemble bursting in the basal forebrain encodes salience irrespective of valence. Neuron 2008, 59(1):138-149. 10.1016/j.neuron.2008.04.031, 2697387, 18614035.
83. Richardson RT, DeLong MR. Context-dependent responses of primate nucleus basalis neurons in a go/no-go task. J Neurosci 1990, 10(8):2528-2540.