Adaptive changes in firing of primary auditory cortical neurons following illumination shift from light to dark in freely moving guinea pigs

Cerebral Cortex

Volumn 20, Issue 2, 2010, Pages 339-351

  Ojima, Hisayuki ^a,b   Taoka, Miki ^a   Iriki, Atsushi ^a,b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Baseline discharge; Free moving; Laminar specificity; Light and dark; Natural sounds

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; BEHAVIOR CHANGE; BRAIN CELL; BRAIN STEM; FEMALE; GUINEA PIG; ILLUMINATION; MALE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; AUDITORY PERCEPTION; BRAIN MAPPING; DARK ADAPTATION; DARKNESS; ELECTROPHYSIOLOGY; FEMALE; GUINEA PIGS; LIGHT; LIGHTING; MALE; MOVEMENT; NEURONS; NEUROPSYCHOLOGICAL TESTS; PERCEPTUAL MASKING; PHOTIC STIMULATION; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 74249120188     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp103     Document Type: Article

References (83)

1. Aston-Jones G, Cohen JD. 2005. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci. 28:403-450. (Pubitemid 41098911)
2. Aston-Jones G, Rajkowski J, Cohen J. 2000. Locus coeruleus and regulation of behavioral flexibility and attention. Prog Brain Res. 126:165-182.
3. Badia P, Myers B, Boecker M, Culpepper J, Harsh JR. 1991. Bright light effects on body temperature, alertness, EEG and behavior. Physiol Behav. 50:583-588.
4. Berridge CW, Waterhouse BD. 2003. The locus coeruleus-noradrenergic system. modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev. 42:33-84.
5. Bizley JK, Nodal FR, Bajo VM, Nelken I, King AJ. 2007. Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb Cortex. 17:2172-2189.
6. Borbely AA. 1976. Sleep and motor activity of the rat during ultra-short light-dark cycles. Brain Res. 114:305-317.
7. Borbely AA, Huston JP, Waser PG. 1975. Control of sleep states in the rat by short light-dark cycles. Brain Res. 95:89-101.
8. Bouret S, Sara SJ. 2004. Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur J Neurosci. 20:791-802.
9. Bouret S, Sara SJ. 2005. Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28:574-582.
10. Briand LA, Gritton H, Howe WM, Young DA, Sarter M. 2007. Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog Neurobiol. 83:69-91.
11. Brosch M, Selezneva E, Scheich H. 2005. Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys. J Neurosci. 20:6797-6806.
12. Budinger E, Heil P, Hess A, Scheich H. 2006. Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems. Neuroscience. 143:1065-1083.
13. Connors BW, Amitai Y. 1995. Functions of local circuits in neocortex: synchrony and laminae. In: Gutnick MJ, Mody I, editors. The cortical neuron. New York: Oxford University Press. p. 123-140.
14. Crowne DP, Richardson CM, Ward G. 1983. Brief deprivation of vision after unilateral lesions of the frontal eye field prevents contralateral inattention. Science. 220:527-530.
15. de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA. 2006. Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol. 496:27-71.
16. Dean P, Redgrave P. 1984. Superior colliculus and visual neglect in rat and hamster. III. Functional implications. Brain Res. 320:155-163. (Pubitemid 15131088)
17. Devilbiss DM, Waterhouse BD. 2004. The effects of tonic locus ceruleus output on sensory-evoked responses of ventral posterior medial thalamic and barrel field cortical neurons in the awake rat. J Neurosci. 24:10773-10785.
18. Diamond IT, Jones EG, Powell TP. 1969. The projection of the auditory cortex upon the diencephalon and brain stem in the cat. Brain Res. 15:305-340.
19. Eimer M, van Velzen J, Forster B, Driver J. 2003. Shifts of attention in light and in darkness: an ERP study of supramodal attention control and crossmodal links in spatial attention. Cogn Brain Res. 15:308-323.
20. Escudero M, Vidal PP. 1996. A quantitative study of electroencepha- lography, eye movements and neck electromyography characterizing the sleep-wake cycle of the guinea-pig. Eur J Neurosci. 8:572-580.
21. Falchier A, Clavagnier S, Barone P, Kennedy H. 2002. Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci. 22:5749-5759.
22. Felleman DJ, Van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1:1-47.
23. Foote SL, Bloom FE, Aston-Jones G. 1983. Nucleus locus coeruleus: new evidence of anatomical and physiological specificity. Physiol Rev. 63:844-891.
24. Foote SL, Freedman R, Oliver AP. 1975. Effects of putative neuro-transmitters on neuronal activity in monkey auditory cortex. Brain Res. 86:229-242.
25. Foxe JJ, Morocz IA, Murray MM, Higgins BA, Javitt DC, Schroeder CE. 2000. Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res Cogn Brain Res. 10:77-83.
26. Foxe JJ, Wylie GR, Martinez A, Schroeder CE, Javitt DC, Guilfoyle D, Ritter W, Murray MM. 2002. Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J Neuro-physiol. 88:540-543.
27. Fu KM, Shah AS, O'Connell MN, McGinnis T, Eckholdt H, Lakatos P, Smiley J, Schroeder CE. 2004. Timing and laminar profile of eye-position effects on auditory responses in primate auditory cortex. J Neurophysiol. 92:3522-3531.
28. Goff ML, Finger FW. 1966. Activity rhythms and adiurnal light-dark control. Science. 154:1346-1349.
29. Grillon C, Pellowski M, Merikangas KR, Davis M. 1997. Darkness facilitates the acoustic startle reflex in humans. Biol Psychiatry. 42:453-460.
30. Grillon C, Morgan CA, 3rd, Davis M, Southwick SM. 1998. Effect of darkness on acoustic startle in Vietnam veterans with PTSD. Am J Psychiatry. 155:812-817.
31. Gu Q. 2002. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience. 111:815-835.
32. Harper LV. 1976. Behavior. In: Wagner JE, Manning PJ, editors. The biology of the guinea pig. New York, San Francisco, London: Academic Press. p. 31-51.
33. Hjaltason H, Tegner R. 1992. Darkness improves line bisection in unilateral spatial neglect. Cortex. 28:353-358.
34. Inan S, Mitchell T, Song A, Bizzell J, Belger A. 2004. Hemodynamic correlates of stimulus repetition in the visual and auditory cortices: an fMRI study. Neuroimage. 21:886-893.
35. Ison JR, Bowen GP, Kellogg CK. 1991. Potentiation of acoustic startle behavior in the rat (Rattus norvegicus) at the onset of darkness. J Comp Psychol. 105:3-9.
36. Jacobs BL. 1986. Single unit activity of locus coeruleus neurons in behaving animals. Prog Neurobiol. 27:183-194.
37. Jodo E, Chiang C, Aston-Jones G. 1998. Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons. Neuroscience. 83:63-79.
38. Jonsson G. 1980. Chemical neurotoxins as denervation tools in neurobiology. Annu Rev Neurosci. 3:169-187.
39. Kayser C, Petkov CI, Logothetis NK. 2008. Visual modulation of neurons in auditory cortex. Cereb Cortex. 18:1560-1574.
40. Krishna BS, Semple MN. 2000. Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J Neurophysiol. 84:255-273.
41. Lakatos P, Chen CM, O'Connell MN, Mills A, Schroeder CE. 2007. Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron. 18:279-292.
42. Larkman AU. 1991. Dendritic morphology of pyramidal neurones of the visual cortex of the rat: I. Branching patterns. J Comp Neurol. 306:307-319.
43. Larkum ME, Senn W, Luscher HR. 2004. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex. 14:1059-1070.
44. Laurienti PJ, Burdette JH, Wallace MT, Yen YF, Field AS, Stein BE. 2002. Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci. 14:420-429.
45. Lavenex P, Amaral DG. 2000. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus. 10:420-430.
46. Lee HS, Kim MA, Waterhouse BD. 2005. Retrograde double-labeling study of common afferent projections to the dorsal raphe and the nuclear core of the locus coeruleus in the rat. J Comp Neurol. 481:179-193.
47. Lehmann C, Herdener M, Esposito F, Hubl D, di Salle F, Scheffler K, Bach DR, Federspiel A, Kretz R, Dierks T, et al. 2006. Differential patterns of multisensory interactions in core and belt areas of human auditory cortex. Neuroimage. 31:294-300.
48. Lisk RD, Sawyer CH. 1966. Induction of paradoxical sleep by lights-off stimulation. Proc Soc Exp Biol Med. 123:664-667.
49. Luppi PH, Aston-Jones G, Akaoka H, Chouvet G, Jouvet M. 1995. Afferent projections to the rat locus coeruleus demonstrated by retrograde and anterograde tracing with cholera-toxin B subunit and Phaselolus vulgaris leucoagglutinin. Neuroscience. 65:119-160.
50. Ma X, Suga N. 2005. Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex. Proc Natl Acad Sci USA. 102:9335-9340.
51. Manning A, Dawkins MS. 1998. An introduction to animal behavior. 5th edn. Cambridge: Cambridge University Press.
52. Martuzzi R, Murray MM, Michel CM, Thiran JP, Maeder PP, Clarke S, Meuli RA. 2007. Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cereb Cortex. 17:1672-1679.
53. Metherate R, Ashe JH, Weinberger NM. 1990. Acetylcholine modifies neuronal acoustic rate-level functions in guinea pig auditory cortex by an action at muscarinic receptors. Synapse. 6:364-368.
54. Metherate R, Weinberger NM. 1989. Acetylcholine produces stimulus-specific receptive field alterations in cat auditory cortex. Brain Res. 480:372-377.
55. Miles RC, Ratoosh P, Meyer DR. 1956. Absence of color vision in guinea pig. J Neurophysiol. 19:254-258.
56. Miller AM, Obermeyer WH, Behan M, Benca RM. 1998. The superior colliculus-pretectum mediates the direct effects of light on sleep. Proc Natl Acad Sci USA. 95:8957-8962.
57. Nicoll RA, Malenka RC, Kauer JA. 1990. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol Rev. 70:513-565.
58. Ojima H. 1994. Terminal morphology and distribution of cortico-thalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb Cortex. 4:646-663.
59. Ojima H, Honda CN, Jones EG. 1992. Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. Cereb Cortex. 2:197-216.
60. Ojima H, Takayanagi M, Potapov D, Homma R. 2005. Isofrequency bandlike zones of activation revealed by optical imaging of intrinsic signals in the cat primary auditory cortex. Cereb Cortex. 15:1497-1509.
61. Pena JL, Perez-Perera L, Bouvier M, Velluti RA. 1999. Sleep and wakefulness modulation of the neuronal firing in the auditory cortex of the guinea pig. Brain Res. 816:463-470.
62. Perrin F, Peigneux P, Fuchs S, Verhaeghe S, Laureys S, Middleton B, Degueldre C, Del Fiore G, Vandewalle G, Balteau E, et al. 2004. Nonvisual responses to light exposure in the human brain during the circadian night. Curr Biol. 14:1842-1846.
63. Redgrave P, Westby GW, Dean P. 1993. Functional architecture of rodent superior colliculus: relevance of multiple output channels. Prog Brain Res. 95:69-77.
64. Redies H, Sieben U, Creutzfeldt OD. 1989. Functional subdivisions in the auditory cortex of the guinea pig. J Comp Neurol. 282:473-488. (Pubitemid 19122891)
65. Robbins TW. 2005. Chemistry of the mind: neurochemical modulation of prefrontal cortical function. J Comp Neurol. 493:140-146.
66. Rockland KS, Ojima H. 2003. Multisensory convergence in calcarine visual areas in macaque monkey. Int J Psychophysiol. 50:19-26.
67. Rockland KS, Pandya DN. 1979. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179:3-20.
68. Rood JP. 1972. Ecology and behavioural comparisons of three genera of Argentine cavies. Animal Behav. 5:1-83.
69. Ross SB. 1976. Long-term effects of N-2-chlorethyl-N-ethyl-2-bromo- benzylamine hydrochloride on noradrenergic neurones in the rat brain and heart. Br J Pharmacol. 58:521-527.
70. Rhodes PA, Llinas RR. 2001. Apical tuft input efficacy in layer 5 pyramidal cells from rat visual cortex. J Physiol. 536:167-187.
71. Rouiller EM, Simm GM, Villa AE, de Ribaupierre Y, de Ribaupierre F. 1991. Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp Brain Res. 86:483-505.
72. Sesack SR, Deutch AY, Roth RH, Bunney BS. 1989. Topographical organization of the efferent projections pf the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris lecucoagglutinin. J Comp Neurol. 290:213-242.
73. Sherman SM, Guillery RW. 2006. Exploring the thalamus and its role in cortical function. 2nd edn. Cambridge: MIT Press.
74. Silva LR, Amitai Y, Connors BW. 1991. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science. 251:432-435.
75. Vargo JM, Lai HV, Marshall JF. 1998. Light deprivation accelerates recovery from frontal cortical neglect: relation to locomotion and striatal Fos expression. Behav Neurosci. 112:387-398.
76. Walker DL, Davis M. 1997a. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci. 17:9375-9383.
77. Walker DL, Davis M. 1997b. Anxiogenic effects of high illumination levels assessed with the acoustic startle response in rats. Biol Psychiatry. 42:461-471.
78. Wallace MN, Rutkowski RG, Palmer AR. 2000. Identification and localisation of auditory areas in guinea pig cortex. Exp Brain Res. 132:445-456.
79. Waterhouse BD, Azizi SA, Burne RA, Woodward DJ. 1990. Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin microiontophoresis. Brain Res. 514:276-292.
80. Waterhouse BD, Woodward DJ. 1980. Interaction of norepinephrine with cerebrocortical activity evoked by stimulation of somatosen-sory afferent pathways in the rat. Exp Neurol. 67:11-34.
81. Werner-Reiss U, Kelly KA, Trause AS, Underhill AM, Groh JM. 2003. Eye position affects activity in primary auditory cortex of primates. Curr Biol. 13:554-562.
82. Yan J, Suga N. 1996. Corticofugal modulation of time-domain processing of biosonar information in bats. Science. 273:1100-1103.
83. Zhang Y, Suga N, Yan J. 1997. Corticofugal modulation of frequency processing in bat auditory system. Nature. 387:900-903