Dopamine-modulated recurrent corticoefferent feedback in primary sensory cortex promotes detection of behaviorally relevant stimuli

Journal of Neuroscience

Volumn 34, Issue 4, 2014, Pages 1234-1247

  Happel, Max F K ^a,b   Deliano, Matthias ^a   Handschuh, Juliane ^a   Ohl, Frank W ^a,b,c  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c Center for Behavioral Brain Science (CBBS)   (Germany)

Author keywords

Auditory cortex; Behavior; Corticoefferent recurrence; Dopamine; Perception

Indexed keywords

AUDITORY CORTEX; BEHAVIOR; CORTICOEFFERENT RECURRENCE; DOPAMINE; PERCEPTION;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; DOPAMINE; ELECTROPHYSIOLOGY; EVOKED POTENTIALS, AUDITORY; FEEDBACK, PHYSIOLOGICAL; GERBILLINAE; MALE; SYNAPTIC TRANSMISSION;

EID: 84892687251     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1990-13.2014     Document Type: Article

References (60)

1. Adesnik H, Scanziani M (2010) Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464:1155-1160. CrossRef Medline
2. Ashby FG, Casale MB (2003) A model of dopamine modulated cortical activation. Neural Netw 16:973-984. CrossRef Medline
3. Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76:695-711. CrossRef Medline
4. Briggs F, Usrey WM (2007) A fast, reciprocal pathway between the lateral geniculate nucleus and visual cortex in the macaque monkey. J Neurosci 27:5431-5436. CrossRef Medline
5. Bromberg-Martin ES, Matsumoto M, HikosakaO (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834. CrossRef Medline
6. 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. CrossRef Medline
7. Campbell MJ, Lewis DA, Foote SL, Morrison JH (1987) Distribution of choline acetyltransferase-, serotonin-, dopamine-P-hydroxylase-, tyrosine hydroxylase-immunoreactive fibers in monkey primary auditory cortex. J Comp Neurol 261:209-220. CrossRef Medline
8. Chung S, Ferster D (1998) Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20:1177-1189. CrossRef Medline
9. Covic EN, Sherman SM (2011) Synaptic properties of connections between the primary and secondary auditory cortices in mice. Cereb Cortex 21: 2425-2441. CrossRef Medline
10. Curtis CE, Lee D (2010) Beyond working memory: the role of persistent activity in decision making. Trends Cogn Sci 14:216-222. CrossRef Medline
11. Dahmen JC, Keating P, Nodal FR, Schulz AL, King AJ (2010) Adaptation to stimulus statistics in the perception and neural representation of auditory space. Neuron 66:937-948. CrossRef Medline
12. Davies PL, Chang WP, Gavin WJ (2009) Maturaration of sensory gating performance in children with an without sensory processing disorders. Int J Psychophysiol 72:187-197. CrossRef Medline
13. Deliano M, Scheich H, Ohl FW (2009) Auditory cortical activity after intracortical microstimulation and its role for sensory processing and learning. J Neurosci 29:15898-15909. CrossRef Medline
14. Douglas RJ, Martin KA (2007) Mapping the matrix: the ways of neocortex. Neuron 56:226-238. CrossRef Medline
15. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci 3 [Suppl]:1184-1191. CrossRef Medline
16. Edeline JM (2012) Beyond traditional approaches to understanding the functional role of neuromodulators in sensory cortices. Front Behav Neurosci 6:45. CrossRef Medline
17. Friston KJ, Shiner T, FitzGerald T, Galea JM, Adams R, Brown H, Dolan RJ, Moran R, Stephan KE, Bestmann S (2012) Dopamine, affordance and active inference. PLoS Comput Biol 8:e1002327. CrossRef Medline
18. Gerstein G, Kirkland K, Musial P, Talwar S (2002) Recordings, behavior and models related to corticothalamic feedback. Philos Trans R Soc B Biol Sci 357:1835-1841. CrossRef Medline
19. Happel MF, Jeschke M, Ohl FW (2010) Spectral integration in primary auditory cortex attributable to temporally precise convergence of thalamocortical and intracortical input. J Neurosci 30:11114-11127. CrossRef Medline
20. Hasselmo ME (1995) Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav Brain Res 67:1-27. CrossRef Medline
21. Hickmott PW, MerzenichMM (1998) Single-cell correlates of a representational boundary in rat somatosensory cortex. J Neurosci 18:4403-4416. Medline
22. Histed MH, Bonin V, Reid RC (2009) Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 63:508-522. CrossRef Medline
23. Jaramillo S, Zador AM (2011) The auditory cortex mediates the perceptual effects of acoustic temporal expectation. Nat Neurosci 14:246-251. CrossRef Medline
24. Kawai H, Lazar R, Metherate R (2007) Nicotinic control of axon excitability regulates thalamocortical transmission. Nat Neurosci 10:1168-1175. CrossRef Medline
25. King AJ (1997) Signal selection by cortical feedback. Curr Biol 7:R85-R88. CrossRef Medline
26. Kraus M, Schicknick H, Wetzel W, Ohl F, Staak S, Tischmeyer W (2002) Memory consolidation for the discrimination of frequency-modulated tones in Mongolian gerbils is sensitive to protein-synthesis inhibitors applied to the auditory cortex. Learn Mem 9:293-303. CrossRef Medline
27. Krimer LS, Jakab RL, Goldman-Rakic PS (1997) Quantitative threedimensional analysis of the catecholaminergic innervation of identified neurons in the macaque prefrontal cortex. J Neurosci 17:7450-7461. Medline
28. Lamme VA, Supèr H, Spekreijse H (1998) Feedforward, horizontal, and feedback processing in the visual cortex. Curr Opin Neurobiol 8:529-535. CrossRef Medline
29. Lavin A, Nogueira L, Lapish CC, Wightman RM, Phillips PE, Seamans JK (2005) Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. J Neurosci 25:5013-5023. CrossRef Medline
30. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI (2007) Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10: 1594-1600. CrossRef Medline
31. Logothetis NK, Augath M, Murayama Y, Rauch A, Sultan F, Goense J, Oeltermann A, Merkle H (2010) The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 13:1283-1291. CrossRef Medline
32. Metherate R, Kaur S, Kawai H, Lazar R, Liang K, Rose HJ (2005) Spectral integration in auditory cortex: mechanisms and modulation. Hear Res 206:146-158. CrossRef Medline
33. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37-100. Medline
34. Müller-Preuss P, MitzdorfU (1984) Functional anatomy of the inferior colliculus and the auditory cortex: current source density analyses of clickevoked potentials. Hear Res 16:133-142. CrossRef Medline
35. Ohl FW, Scheich H (2005) Learning-induced plasticity in animal and human auditory cortex. Curr Opin Neurobiol 15:470-477. CrossRef Medline
36. Ohl FW, Wetzel W, Wagner T, Rech A, Scheich H (1999) Bilateral ablation of auditory cortex in Mongolian gerbil affects discrimination of frequency modulated tones but not of pure tones. Learn Mem 6:347-362. Medline
37. Ohl FW, Scheich H, Freeman WJ (2000) Topographic analysis of epidural pure-tone-evoked potentials in gerbil auditory cortex. J Neurophysiol 83:3123-3132. Medline
38. Ohl FW, Scheich H, Freeman WJ (2001) Change in pattern of ongoing cortical activity with auditory category learning. Nature 412:733-736. CrossRef Medline
39. Phillipson OT, Kilpatrick IC, Jones MW (1987) Dopaminergic innervation of the primary visual cortex in the rat, and some correlations with human cortex. Brain Res Bull 18:621-633. Medline
40. Ranck JB Jr (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417-440. CrossRef Medline
41. Rouiller EM, Durif C (2004) The dual pattern of corticothalamic projection of the primary auditory cortex in macaque monkey. Neurosci Lett 358: 49-52. CrossRef Medline
42. Sakai M, Suga N (2002) Centripetal and centrifugal reorganization of frequency map of auditory cortex in gerbils. Proc Natl Acad Sci U S A 99: 7108-7112. CrossRef Medline
43. Sakata S, Harris KD (2009) Laminar structure and sensory-evoked population activity in auditory cortex. Neuron 64:404-418. CrossRef Medline
44. Scheich H, Heil P, Langner G (1993) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus) II. Tonotopic 2-deoxyglucose. Eur J Neurosci 5:898-914. CrossRef Medline
45. Scheich H, Brechmann A, Brosch M, Budinger E, Ohl FW, Selezneva E, Stark H, Tischmeyer W, Wetzel W (2011) Behavioral semantics of learning and crossmodal processing in auditory cortex: the semantic processor concept. Hear Res 271:3-15. CrossRef Medline
46. Schicknick H, Schott BH, Budinger E, Smalla KH, Riedel A, Seidenbecher CI, Scheich H, Gundelfinger ED, TischmeyerW (2008) Dopaminergic modulation of auditory cortex-dependent memory consolidation through mTOR. Cereb Cortex 18:2646-2658. CrossRef Medline
47. Schicknick H, Reichenbach N, Smalla KH, Scheich H, Gundelfinger ED, Tischmeyer W (2012) Dopamine modulates memory consolidation of discrimination learning in auditory cortex. Eur J Neurosci 35:763-774. CrossRef Medline
48. Schonwald A, Lechner E (2006) Attention deficit/hyperactivity disorder: complexities and controversies. Curr Opin Pediatr 18:189-195. CrossRef Medline
49. Schroeder CE, Mehta AD, Givre SJ (1998) A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. Cereb Cortex 8:575-592. CrossRef Medline
50. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58. CrossRef Medline
51. Seong HJ, Carter AG (2012) D1 receptor modulation of action potential firing in a subpopulation of layer 5 pyramidal neurons in the prefrontal cortex. J Neurosci 32:10516-10521. CrossRef Medline
52. Servan-Schreiber D, Printz H, Cohen JD (1990) A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. Science 249: 892-895. CrossRef Medline
53. Stark H, Scheich H (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a longterm microdialysis study of metabolites. J Neurochem 68:691-697. Medline
54. Stark H, Rothe T, Deliano M, Scheich H (2008) Dynamics of cortical theta activity correlates with stages of auditory avoidance strategy formation in a shuttle-box. Neurosci 151:467-475. CrossRef
55. Szymanski FD, Garcia-Lazaro JA, Schnupp JW (2009) Current source density profiles of stimulus-specific adaptation in rat auditory cortex. J Neurophysiol 102:1483-1490. CrossRef Medline
56. Tehovnik EJ, Slocum WM, Carvey CE, Schiller PH (2005) Phosphene induction and the generation of saccadic eye movements by striate cortex. J Neurophysiol 93:1-19. CrossRef Medline
57. Tritsch NX, Sabatini BL (2012) Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 76:33-50. CrossRef Medline
58. Tsumoto T, Suda K (1982) Effects of stimulation of the dorsocaudal claustrum on activities of striate cortex neurons in the cat. Brain Res 240:345-349. CrossRef Medline
59. Watanabe Y, Funahashi S (2012) Thalamic mediodorsal nucleus and working. Neurosci Biobehav Rev 36:134-142. CrossRef Medline
60. Winer JA, Miller LM, Lee CC, Schreiner CE (2005) Auditory thalamocortical transformation: structure and function. Trends Neurosci 28:255-263. CrossRef Medline