Basal forebrain control of wakefulness and cortical rhythms

Nature Communications

Volumn 6, Issue , 2015, Pages

  Anaclet, Christelle ^a   Pedersen, Nigel P ^a   Ferrari, Loris L ^a   Venner, Anne ^a   Bass, Caroline E ^b   Arrigoni, Elda ^a   Fuller, Patrick M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID; PROTEIN C FOS;

BRAIN; CELLS AND CELL COMPONENTS; COGNITION; DRUG; INHIBITION; NEUROLOGY; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL ACTIVATION; CHOLINERGIC NERVE CELL; COGNITION; CONTROLLED STUDY; DEMENTIA; ELECTROENCEPHALOGRAM; FOREBRAIN; GENE TARGETING; GLUTAMATERGIC NERVE CELL; MINIMALLY CONSCIOUS STATE; MOUSE; NERVE CELL; NONHUMAN; TARGET CELL; WAKEFULNESS; ANIMAL; BASAL FOREBRAIN; ELECTROENCEPHALOGRAPHY; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; REM SLEEP; SLEEP;

MUS;

ANIMALS; BASAL FOREBRAIN; BRAIN WAVES; CEREBRAL CORTEX; CHOLINERGIC NEURONS; ELECTROENCEPHALOGRAPHY; GABAERGIC NEURONS; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MICE; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; SLEEP; SLEEP, REM; WAKEFULNESS;

EID: 84946606054     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9744     Document Type: Article

References (62)

1. Buzsaki, G. H. and Gage, F. in Activation to Acquisition. Functional aspects of the Basal Forebrain Cholinergic System (ed. Richardson, R. T.) (Birkhauser, 1991).
2. Abe, K., Inokawa, M., Kashiwagi, A. and Yanagihara, T. Amnesia after a discrete basal forebrain lesion. J. Neurol. Neurosurg. Psychiatry. 65, 126-130 (1998).
3. Kilgard, M. P. and Merzenich, M. M. Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714-1718 (1998).
4. Pinto, L. et al. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16, 1857-1863 (2013).
5. Goard, M. and Dan, Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12, 1444-1449 (2009).
6. Salmond, C. H., Chatfield, D. A., Menon, D. K., Pickard, J. D. and Sahakian, B. J. Cognitive sequelae of head injury: involvement of basal forebrain and associated structures. Brain 128, 189-200 (2005).
7. Sarter, M. Neuronal mechanisms of the attentional dysfunctions in senile dementia and schizophrenia: two sides of the same coin? Psychopharmacology (Berl.) 114, 539-550 (1994).
8. Heimer, L. Basal forebrain in the context of schizophrenia. Brain Res. Brain Res. Rev. 31, 205-235 (2000).
9. Fuller, P., Sherman, D., Pedersen, N. P., Saper, C. B. and Lu, J. Reassessment of the structural basis of the ascending arousal system. J. Comp. Neurol. 519, 933-956 (2011).
10. Buzsaki, G. et al. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8, 4007-4026 (1988).
11. Conner, J. M., Culberson, A., Packowski, C., Chiba, A. A. and Tuszynski, M. H. Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 38, 819-829 (2003).
12. Shinotoh, H. et al. Progressive loss of cortical acetylcholinesterase activity in association with cognitive decline in Alzheimers disease: a positron emission tomography study. Ann. Neurol. 48, 194-200 (2000).
13. Kapas, L. et al. The effects of immunolesions of nerve growth factor-receptive neurons by 192 IgG-saporin on sleep. Brain Res. 712, 53-59 (1996).
14. Kaur, S., Junek, A., Black, M. A. and Semba, K. Effects of ibotenate and 192IgG-saporin lesions of the nucleus basalis magnocellularis/substantia innominata on spontaneous sleep and wake states and on recovery sleep after sleep deprivation in rats. J. Neurosci. 28, 491-504 (2008).
15. Duque, A., Balatoni, B., Detari, L. and Zaborszky, L. EEG correlation of the discharge properties of identified neurons in the basal forebrain. J. Neurophysiol. 84, 1627-1635 (2000).
16. Hassani, O. K., Lee, M. G., Henny, P. and Jones, B. E. Discharge profiles of identified GABAergic in comparison to cholinergic and putative glutamatergic basal forebrain neurons across the sleep-wake cycle. J. Neurosci. 29, 11828-11840 (2009).
17. Anaclet, C. et al. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat. Neurosci. 17, 1217-1224 (2014).
18. Llinas, R. R. and Steriade, M. Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95, 3297-3308 (2006).
19. Steriade, M., McCormick, D. A. and Sejnowski, T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679-685 (1993).
20. Schiff, N. D. Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann. N. Y. Acad. Sci. 1129, 105-118 (2008).
21. Berridge, C. W. and Foote, S. L. Enhancement of behavioral and electroencephalographic indices of waking following stimulation of noradrenergic beta-receptors within the medial septal region of the basal forebrain. J. Neurosci. 16, 6999-7009 (1996).
22. Xu, C., Datta, S., Wu, M. and Alreja, M. Hippocampal theta rhythm is reduced by suppression of the H-current in septohippocampal GABAergic neurons. Eur. J. Neurosci. 19, 2299-2309 (2004).
23. Cape, E. G. and Jones, B. E. Effects of glutamate agonist versus procaine microinjections into the basal forebrain cholinergic cell area upon gamma and theta EEG activity and sleep-wake state. Eur. J. Neurosci. 12, 2166-2184 (2000).
24. Portas, C. M., Thakkar, M., Rainnie, D. G., Greene, R. W. and McCarley, R. W. Role of adenosine in behavioral state modulation: a microdialysis study in the freely moving cat. Neuroscience 79, 225-235 (1997).
25. Blanco-Centurion, C. et al. Adenosine and sleep homeostasis in the Basal forebrain. J. Neurosci. 26, 8092-8100 (2006).
26. Dunnett, S. B., Everitt, B. J. and Robbins, T. W. The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci. 14, 494-501 (1991).
27. Sofroniew, M. V., Eckenstein, F., Thoenen, H. and Cuello, A. C. Topography of choline acetyltransferase-containing neurons in the forebrain of the rat. Neurosci. Lett. 33, 7-12 (1982).
28. Perry, E. K., Perry, R. H., Blessed, G. and Tomlinson, B. E. Changes in brain cholinesterases in senile dementia of Alzheimer type. Neuropathol. Appl. Neurobiol. 4, 273-277 (1978).
29. Perry, E. K. et al. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J. 2, 1457-1459 (1978).
30. Metherate, R., Cox, C. L. and Ashe, J. H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701-4711 (1992).
31. Bakin, J. S. and Weinberger, N. M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl Acad. Sci. USA 93, 11219-11224 (1996).
32. Froemke, R. C., Merzenich, M. M. and Schreiner, C. E. A synaptic memory trace for cortical receptive field plasticity. Nature 450, 425-429 (2007).
33. Bierer, L. M. et al. Neurochemical correlates of dementia severity in Alzheimers disease: relative importance of the cholinergic deficits. J. Neurochem. 64, 749-760 (1995).
34. Arendt, T. Impairment in memory function and neurodegenerative changes in the cholinergic basal forebrain system induced by chronic intake of ethanol. J. Neural. Transm. Suppl. 44, 173-187 (1994).
35. Irmak, S. O. and de Lecea, L. Basal forebrain cholinergic modulation of sleep transitions. Sleep 37, 1941-1951 (2014).
36. Han, Y. et al. Selective activation of cholinergic basal forebrain neurons induces immediate sleep-wake transitions. Curr. Biol. 24, 693-698 (2014).
37. Henny, P. and Jones, B. E. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur. J. Neurosci. 27, 654-670 (2008).
38. Henny, P. and Jones, B. E. Innervation of orexin/hypocretin neurons by GABAergic, glutamatergic or cholinergic basal forebrain terminals evidenced by immunostaining for presynaptic vesicular transporter and postsynaptic scaffolding proteins. J. Comp. Neurol. 499, 645-661 (2006).
39. Sarter, M. and Bruno, J. P. The neglected constituent of the basal forebrain corticopetal projection system: GABAergic projections. Eur. J. Neurosci. 15, 1867-1873 (2002).
40. Freund, T. F. and Meskenaite, V. Gamma-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc. Natl Acad. Sci. USA 89, 738-742 (1992).
41. Semba, K., Reiner, P. B., McGeer, E. G. and Fibiger, H. C. Morphology of cortically projecting basal forebrain neurons in the rat as revealed by intracellular iontophoresis of horseradish peroxidase. Neuroscience 20, 637-651 (1987).
42. Zaborszky, L. and Duque, A. Local synaptic connections of basal forebrain neurons. Behav. Brain Res. 115, 143-158 (2000).
43. Williams, S. and Boksa, P. Gamma oscillations and schizophrenia. J. Psychiatry Neurosci. 35, 75-77 (2010).
44. Qiu, M. H., Yao, Q. L., Vetrivelan, R., Chen, M. C. and Lu, J. Nigrostriatal dopamine acting on globus pallidus regulates sleep. Cereb Cortex. pii: bhu241. (2014).
45. Gritti, I., Manns, I. D., Mainville, L. and Jones, B. E. Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J. Comp. Neurol. 458, 11-31 (2003).
46. Bickford, M. E., Gunluk, A. E., Van Horn, S. C. and Sherman, S. M. GABAergic projection from the basal forebrain to the visual sector of the thalamic reticular nucleus in the cat. J. Comp. Neurol. 348, 481-510 (1994).
47. Yang, C. et al. Cholinergic neurons excite cortically projecting basal forebrain GABAergic neurons. J. Neurosci. 34, 2832-2844 (2014).
48. Kim, T. et al. Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc. Natl Acad. Sci. USA 112, 3535-3540 (2015).
49. McKenna, J. T. et al. Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. J. Comp. Neurol. 521, 1225-1250 (2013).
50. Theyel, B. B., Llano, D. A. and Sherman, S. M. The corticothalamocortical circuit drives higher-order cortex in the mouse. Nat. Neurosci. 13, 84-88 (2010).
51. Vanderwolf, C. H. and Stewart, D. J. Thalamic control of neocortical activation: a critical re-evaluation. Brain Res. Bull. 20, 529-538 (1988).
52. Villablanca, J. and Salinas-Zeballos, M. E. Sleep-wakefulness, EEG and behavioral studies of chronic cats without the thalamus: the athalamic cat. Arch. Ital. Biol. 110, 383-411 (1972).
53. Fonseca, A. C. et al. Improvement of sleep architecture in the follow up of a patient with bilateral paramedian thalamic stroke. Clin. Neurol. Neurosurg. 113, 911-913 (2011).
54. Lutkenhoff, E. S. et al. Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann. Neurol. 78, 68-76 (2015).
55. Sohal, V. S., Zhang, F., Yizhar, O. and Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702 (2009).
56. Schiff, N. D. et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603 (2007).
57. Rossi, J. et al. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell. Metab. 13, 195-204 (2011).
58. Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142-154 (2011).
59. Krashes, M. J. et al. An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature 507, 238-242 (2014).
60. Alexander, G. M. et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63, 27-39 (2009).
61. Ullmann, J. F., Watson, C., Janke, A. L., Kurniawan, N. D. and Reutens, D. C. A segmentation protocol and MRI atlas of the C57BL/6J mouse neocortex. Neuroimage 78, 196-203 (2013).
62. Clark, K. R., Liu, X., McGrath, J. P. and Johnson, P. R. Highly purified recombinant adeno-associated virus vectors are biologically active and free of detectable helper and wild-type viruses. Hum. Gene Ther. 10, 1031-1039 (1999).