Basal forebrain dynamics during a tactile discrimination task

Journal of Neurophysiology

Volumn 112, Issue 5, 2014, Pages 1179-1191

  Thomson, Eric ^a,d   Lou, Jason ^a   Sylvester, Kathryn ^a   McDonough, Annie ^a   Tica, Stefani ^a   Nicolelis, Miguel A ^a,b,c,d  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Duke University   (United States)

^c DUKE UNIVERSITY   (United States)

^d Edmond and Lily Safra International Institute of Neuroscience of Natal   (Brazil)

Author keywords

Basal forebrain; Reward processing; Whisker system

Indexed keywords

ANIMAL; FEMALE; FOREBRAIN; LONG EVANS RAT; NERVE CELL; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; RAT; REWARD; TOUCH; VIBRISSA;

ANIMALS; BASAL FOREBRAIN; DISCRIMINATION (PSYCHOLOGY); FEMALE; NEURONS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, LONG-EVANS; REWARD; TOUCH PERCEPTION; VIBRISSAE;

EID: 84906908971     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00040.2014     Document Type: Article

References (71)

1. Alenda A, Nunez A. Cholinergic modulation of sensory interference in rat primary somatosensory cortical neurons. Brain Res 1133: 158-167, 2007.
2. Aston-Jones G, Cohen JD. An integrative theory of locus coeruleus-norepi-nephrine function: adaptive gain and optimal performance. Annu Rev Neu-rosci 28: 403-450, 2005.
3. Baskerville KA, Chang HT, Herron P. Topography of cholinergic afferents from the nucleus basalis of Meynert to representational areas of sensorimo-tor cortices in the rat. J Comp Neurol 335: 552-562, 1993.
4. Bear MF, Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320: 172-176, 1986.
5. Berg RW, Friedman B, Schroeder LF, Kleinfeld D. Activation of nucleus basalis facilitates cortical control of a brain stem motor program. J Neuro-physiol 94: 699-711, 2005.
6. Bigl V, Woolf NJ, Butcher LL. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 8: 727-749, 1982.
7. Chubykin AA, Roach EB, Bear MF, Shuler MG. A cholinergic mechanism for reward timing within primary visual cortex. Neuron 77: 723-735, 2013.
8. Derdikman D, Yu C, Haidarliu S, Bagdasarian K, Arieli A, Ahissar E. Layer-specific touch-dependent facilitation and depression in the somato-sensory cortex during active whisking. J Neurosci 26: 9538-9547, 2006.
9. Detari L, Rasmusson DD, Semba K. The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog Neurobiol 58: 249-277, 1999.
10. Fawcett T. An introduction to ROC analysis. Pattern Recogn Lett 27: 861-874, 2006.
11. Gandhi SP, Heeger DJ, Boynton GM. Spatial attention affects brain activity in human primary visual cortex. Proc Natl Acad Sci USA 96: 3314-3319, 1999.
12. Goard M, Dan Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12: 1444-1449, 2009.
13. Gritti I, Mainville L, Mancia M, Jones BE. GABAergic and other noncho-linergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 383: 163-177, 1997.
14. Howard MA 3rd, Simons DJ. Physiologic effects of nucleus basalis magno-cellularis stimulation on rat barrel cortex neurons. Exp Brain Res 102: 21-33, 1994.
15. Hubel DH, Wiesel TN. Receptive fields, binocular interaction and functional architecture in cats visual cortex. J Physiol 160: 106-154, 1962.
16. Hubel DH, Wiesel TN. Receptive fields of single neurones in the cat's striate cortex. J Physiol 148: 574-591, 1959.
17. Hupe JM, James AC, Payne BR, Lomber SG, Girard P, Bullier J. Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 394: 784-787, 1998.
18. Hur EE, Zaborszky L. Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization study [corrected]. J Comp Neurol 483: 351-373, 2005.
19. Imas OA, Ropella KM, Ward BD, Wood JD, Hudetz AG. Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat. Neurosci Lett 387: 145-150, 2005.
20. Jacobs SE, Juliano SL. The impact of basal forebrain lesions on the ability of rats to perform a sensory discrimination task involving barrel cortex. J Neurosci 15: 1099-1109, 1995.
21. Johnson GA, Calabrese E, Badea A, Paxinos G, Watson C. A multidimensional magnetic resonance histology atlas of the Wistar rat brain. Neuroim-age 62: 1848-1856, 2012.
22. Jones BE. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26: 578-586, 2005.
23. Karmarkar UR, Dan Y. Experience-dependent plasticity in adult visual cortex. Neuron 52: 577-585, 2006.
24. Kilgard MP, Merzenich MM. Cortical map reorganization enabled by nucleus basalis activity. Science 279: 1714-1718, 1998.
25. Kleinfeld D, Ahissar E, Diamond ME. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol 16: 435-444, 2006.
26. Krupa DJ, Ghazanfar AA, Nicolelis MA. Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc Natl Acad Sci USA 96: 8200-8205, 1999.
27. Krupa DJ, Matell MS, Brisben AJ, Oliveira LM, Nicolelis MA. Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci 21: 5752-5763, 2001.
28. Krupa DJ, Wiest MC, Shuler MG, Laubach M, Nicolelis MA. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 304: 1989-1992, 2004.
29. Kuo MC, Rasmusson DD, Dringenberg HC. Input-selective potentiation and rebalancing of primary sensory cortex afferents by endogenous acetylcho-line. Neuroscience 163: 430-441, 2009.
30. Lamour Y, Dutar P, Jobert A. Topographic organization of basal forebrain neurons projecting to the rat cerebral cortex. Neurosci Lett 34: 117-122, 1982.
31. Laplante F, Morin Y, Quirion R, Vaucher E. Acetylcholine release is elicited in the visual cortex, but not in the prefrontal cortex, by patterned visual stimulation: a dual in vivo microdialysis study with functional correlates in the rat brain. Neuroscience 132: 501-510, 2005.
32. Lee S, Carvell GE, Simons DJ. Motor modulation of afferent somatosensory circuits. Nat Neurosci 11: 1430-1438, 2008.
33. Lee SH, Dan Y. Neuromodulation of brain states. Neuron 76: 209-222, 2012.
34. Lin SC, Gervasoni D, Nicolelis MA. Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles. J Neuro-physiol 96: 3209-3219, 2006.
35. Lin SC, Nicolelis MA. Neuronal ensemble bursting in the basal forebrain encodes salience irrespective of valence. Neuron 59: 138-149, 2008.
36. Ma M, Luo M. Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J Neurosci 32: 10105-10116, 2012.
37. McKinney M, Coyle JT, Hedreen JC. Topographic analysis of the innerva-tion of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 217: 103-121, 1983.
38. Metherate R, Cox CL, Ashe JH. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12: 4701-4711, 1992.
39. Mitchell SJ, Richardson RT, Baker FH, DeLong MR. The primate nucleus basalis of Meynert: neuronal activity related to a visuomotor tracking task. Exp Brain Res 68: 506-515, 1987.
40. Muir JL, Everitt BJ, Robbins TW. AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function. J Neurosci 14: 2313-2326, 1994.
41. Muir JL, Everitt BJ, Robbins TW. Reversal of visual attentional dysfunction following lesions of the cholinergic basal forebrain by physostigmine and nicotine but not by the 5-HT3 receptor antagonist, ondansetron. Psychop-harmacology (Berl) 118: 82-92, 1995.
42. Nicolelis MA, Fanselow EE. Dynamic shifting in thalamocortical processing during different behavioural states. Philos Trans R Soc Lond B Biol Sci 357: 1753-1758, 2002.
43. Nunez A, Dominguez S, Buno W, Fernandez de Sevilla D. Cholinergic-mediated response enhancement in barrel cortex layer V pyramidal neurons. J Neurophysiol 108: 1656-1668, 2012.
44. Oken BS, Salinsky MC, Elsas SM. Vigilance, alertness, or sustained attention: physiological basis and measurement. Clin Neurophysiol 117: 1885-1901, 2006.
45. Pais-Vieira M, Lebedev MA, Wiest MC, Nicolelis MA. Simultaneous top-down modulation of the primary somatosensory cortex and thalamic nuclei during active tactile discrimination. J Neurosci 33: 4076-4093, 2013.
46. Pang K, Williams MJ, Egeth H, Olton DS. Nucleus basalis magnocellularis and attention: effects of muscimol infusions. Behav Neurosci 107: 1031-1038, 1993.
47. Pantoja J, Ribeiro S, Wiest M, Soares E, Gervasoni D, Lemos NA, Nicolelis MA. Neuronal activity in the primary somatosensory thalamocor-tical loop is modulated by reward contingency during tactile discrimination. J Neurosci 27: 10608-10620, 2007.
48. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Waltham, MA: Academic Press/Elsevier, 2007.
49. Pinto L, Goard MJ, Estandian D, Xu M, Kwan AC, Lee SH, Harrison TC, Feng G, Dan Y. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16: 1857-1863, 2013.
50. Pleger B, Blankenburg F, Ruff CC, Driver J, Dolan RJ. Reward facilitates tactile judgments and modulates hemodynamic responses in human primary somatosensory cortex. J Neurosci 28: 8161-8168, 2008.
51. Rasmusson DD, Smith SA, Semba K. Inactivation of prefrontal cortex abolishes cortical acetylcholine release evoked by sensory or sensory pathway stimulation in the rat. Neuroscience 149: 232-241, 2007.
52. Richardson RT, DeLong MR. Context-dependent responses of primate nucleus basalis neurons in a go/no-go task. J Neurosci 10: 2528-2540, 1990.
53. Saper CB. Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J Comp Neurol 222: 313-342, 1984.
54. Sarter M, Hasselmo ME, Bruno JP, Givens B. 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, 2005.
55. Steinmetz PN, Roy A, Fitzgerald PJ, Hsiao SS, Johnson KO, Niebur E. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404: 187-190, 2000.
56. Szymusiak R. Magnocellular nuclei of the basal forebrain: substrates of sleep and arousal regulation. Sleep 18: 478-500, 1995.
57. Szymusiak R, Alam N, McGinty D. Discharge patterns of neurons in cholinergic regions of the basal forebrain during waking and sleep. Behav Brain Res 115: 171-182, 2000.
58. Tremblay N, Warren RA, Dykes RW. Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. J Neurophysiol 64: 1212-1222, 1990.
59. Verdier D, Dykes RW. Long-term cholinergic enhancement of evoked potentials in rat hindlimb somatosensory cortex displays characteristics of long-term potentiation. Exp Brain Res 137: 71-82, 2001.
60. Voytko ML, Olton DS, Richardson RT, Gorman LK, Tobin JR, Price DL. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14: 167-186, 1994.
61. Webster HH, Rasmusson DD, Dykes RW, Schliebs R, Schober W, Bruckner G, Biesold D. Long-term enhancement of evoked potentials in raccoon somatosensory cortex following co-activation of the nucleus basalis of Meynert complex and cutaneous receptors. Brain Res 545: 292-296, 1991.
62. Weinberger NM. The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiol Learn Mem 80: 268-284, 2003.
63. Wiest M, Thomson E, Meloy J. Multielectrode recordings in the somatosen-sory system. Methods for Neural Ensemble Recordings, edited by Nicolelis MAL. Boca Raton, FL: CRC, 2008.
64. Wiest MC, Bentley N, Nicolelis MA. Heterogeneous integration of bilateral whisker signals by neurons in primary somatosensory cortex of awake rats. J Neurophysiol 93: 2966-2973, 2005.
65. Wiest MC, Thomson E, Pantoja J, Nicolelis MA. Changes in S1 neural responses during tactile discrimination learning. J Neurophysiol 104: 300-312, 2010.
66. Wilson FA, Rolls ET. Learning and memory is reflected in the responses of reinforcement-related neurons in the primate basal forebrain. J Neurosci 10: 1254-1267, 1990.
67. Yu AJ, Dayan P. Uncertainty, neuromodulation, and attention. Neuron 46: 681-692, 2005.
68. Zaborszky L, Csordas A, Mosca K, Kim J, Gielow MR, Vadasz C, Nadasdy Z. Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb Cortex. First published August 19, 2013; doi:10.1093/cercor/bht210.
69. Zaborsky L, van den Pol A, Gyengesi E. The basal forebrain cholinergic projection system in mice. The Mouse Nervous System, edited by Paxinos G, Watson C, Puelles L. Amsterdam: Elsevier Academic: 2012, p. 684-718.
70. Zar JH. Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall, 1996.
71. Zhang H. Exploring conditions for the optimality of naive Bayes. Int J Pattern Recogn 19: 183-198, 2005.