The activity in the anterior insulae is modulated by perceptual decision-making difficulty

Neuroscience

Volumn 327, Issue , 2016, Pages 79-94

  Lamichhane, Bidhan ^a   Adhikari, Bhim M ^a   Dhamala, Mukesh ^a,b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b Georgia State University   (United States)

Author keywords

Functional magnetic resonance imaging; Response time; Salience network; Task difficulty

Indexed keywords

ADULT; ANTERIOR INSULA; ARTICLE; AUDIO VISUAL ASYNCHRONY AND SYNCHRONY PERCEPTION TASK; AUDITORY PERCEPTION TEST; BEHAVIOR; BEHAVIORAL SCIENCE; BOLD SIGNAL; BRAIN FUNCTION; CONTROLLED STUDY; DECISION MAKING; FACE HOUSE CATEGORIZATION TASK; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GOAL DIRECTED BEHAVIOR; HAPPY ANGRY FACE CATEGORIZATION TASK; HUMAN; HUMAN EXPERIMENT; MALE; MENTAL TASK; NORMAL HUMAN; PERCEPTION; PRIORITY JOURNAL; RANDOM DOTS MOTION DIRECTION DISCRIMINATION TASK; RESPONSE TIME; SALIENCE NETWORK; STIMULUS RESPONSE; TASK PERFORMANCE; VISUAL PERCEPTION TEST; BRAIN CORTEX; BRAIN MAPPING; IMAGE PROCESSING; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; REACTION TIME; YOUNG ADULT;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; DECISION MAKING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PHOTIC STIMULATION; REACTION TIME; YOUNG ADULT;

EID: 84964370834     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.04.016     Document Type: Article

References (88)

1. Ackermann H., Riecker A. The contribution(s) of the insula to speech production: a review of the clinical and functional imaging literature. Brain Struct Funct 2010, 214:419-433.
2. Augustine R.J. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Rev 1996, 22:229-244.
3. Bajaj S., Lamichhane B., Adhikari B.M., Dhamala M. Amygdala mediated connectivity in perceptual decision-making of emotional facial expressions. Brain Connect 2013, 3:386-397.
4. Bamiou D.-E., Musiek F.E., Luxon L.M. The insula (Island of Reil) and its role in auditory processing. Brain Res Rev 2003, 42:143-154.
5. Binder J.R., Liebenthal E., Possing E.T., Medler A.D., Ward B.D. Neural correlates of sensory and decision processes in auditory object identification. Nat Neurosci 2004, 7:295-300.
6. Botvinick M.M., Braver T.S., Barch D.M., Carter C.S., Cohen J.D. Conflict monitoring and cognitive control. Psychol Rev 2001, 108:624-652.
7. Braver T.S., Krug M.K., Chiew K.S., Kool W., Westbrook J.A., Clement N.J., Adcock R.A., Barch D.M., Botvinick M.M., Carver C.S., Cools R., Custers R., Dickinson A., Dweck C.S., Fishbach A., Gollwitzer P.M., Hess T.M., Isaacowitz D.M., Mather M., Murayama K., Pessoa L., Samanez-Larkin G.R., Somerville L.H., MOMCAI group Mechanisms of motivation-cognition interaction: challenges and opportunities. Cogn Affect Behav Neurosci 2014, 14:443-472.
8. Brett M, Anton J-L, Valabregue R, Poline J-B (2002) Region of interest analysis using an SPM toolbox (abstract) Presented at the 8th International Conference on Functional mapping of Humal Brain, June 2-6, 2002 Sendai, Japan.
9. Bushara K.O., Grafman J., Hallett M. Neural Correlates of auditory-visual stimulus onset asynchrony detection. J Neurosci 2001, 32:300-304.
10. Bushara K.O., Hanakawa T., Immisch I., Toma K., Kansaku K., Hallett M. Neural correlates of cross-modal binding. Nat Neurosci 2003, 6:190-195.
11. Cai W., Ryali S., Chen T., Li C.S., Menon V. Dissociable roles of right inferior frontal cortex and anterior insula in inhibitory control: evidence from intrinsic and task-related functional parcellation, connectivity, and response profile analyses across multiple datasets. J Neurosci 2014, 34:14652-14667.
12. Calder A.J., Keane J., Manes F., Antoun N., Young A.W. Impaired recognition and experience of disgust following brain injury. Nat Neurosci 2000, 3:1077-1078.
13. Calvert G.A. Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb Cortex 2001, 11:1110-1123.
14. Cauda F., Costa T., Torta D.M., Sacco K., D'Agata F., Duca S., Geminiani G., Fox P.T., Vercelli A. Meta-analytic clustering of the insular cortex: characterizing the meta-analytic connectivity of the insula when involved in active tasks. Neuroimage 2012, 62:343-355.
15. Chang L.J., Yarkoni T., Khaw M.W., Sanfey A.G. Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb Cortex 2013, 23:739-749.
16. Coull J.T. FMRI studies of temporal attention: allocating attention within, or towards, time. Brain Res Cogn Brain Res 2004, 21:216-226.
17. Coull J.T., Frith C.D., Buchel C., Nobre A.C. Orienting attention in time: behavioural and neuroanatomical distinction between exogeneous and endogeneous shifts. Neuropsychologia 2000, 38:808-819.
18. Coull J.T., Vidal F., Nazarian B., Macar F. Functional anatomy of the attentional modulation of time estimation. Science 2004, 303:1506-1508.
19. Craig A.D. Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 2003, 13:500-505.
20. Craig A.D. How do you feel - now? The anterior insula and human awareness. Nat Rev Neurosci 2009, 10:59-70.
21. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat Neurosci 2004, 7:189-195.
22. Damasio A., Damasio H., Tranel D. Persistence of feelings and sentience after bilateral damage of the insula. Cereb Cortex 2013, 23:833-846.
23. Deary I.J., Simonotto E., Meyer M., Marshall A., Marshall I., Goddard N., Wardlaw J.M. The functional anatomy of inspection time: an event-related fMRI study. Neuroimage 2004, 22:1466-1479.
24. Deen B., Pitskel N.B., Pelphrey K.A. Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 2011, 21:1498-1506.
25. Eckert M.A., Menon V., Walczak A., Ahlstrom J., Denslow S., Horwitz A., Dubno J.R. At the heart of the ventral attention system: the right anterior insula. Hum Brain Mapp 2009, 30:2530-2541.
26. Ernst M., Paulus M.P. Neurobiology of decision making: a selective review from a neurocognitive and clinical perspective. Biol Psychiatry 2005, 58:597-604.
27. Friston K.J., Holmes A.P., Worsely K.J., Poline J.-B., Firth C.D., Frackowiak R.S.J. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995, 2:189-210.
28. Ghahremani A., Rastogi A., Lam S. The role of right anterior insula and salience processing in inhibitory control. J Neurosci 2015, 35:3291-3292.
29. Grinband J., Hirsch J., Ferrera V.P. A neural representation of categorization uncertainty in the human brain. Neuron 2006, 49:757-763.
30. Gu X., Gao Z., Wang X., Liu X., Knight R.T., Hof P.R., Fan J. Anterior insular cortex is necessary for empathetic pain perception. Brain 2012, 135:2726-2735.
31. Gu X., Liu X., Guise K.G., Naidich T.P., Hof P.R., Fan J. Functional dissociation of the frontoinsular and anterior cingulate cortices in empathy for pain. J Neurosci 2010, 30:3739-3744.
32. Ham T., Leff A., de Boissezon X., Joffe A., Sharp D.J. Cognitive control and the salience network: an investigation of error processing and effective connectivity. J Neurosci 2013, 33:7091-7098.
33. Harrington D.L., Boyd L.A., Mayer A.R., Sheltraw D.M., Lee R.R., Huang M., Rao S.M. Neural representation of interval encoding and decision making. Cogn Brain Res 2004, 21:193-205.
34. Heekeren H.R., Bandettini P.A., Ungerleider L.G. A general mechanism for perceptual decision-making in the human brain. Nature 2004, 431:859-862.
35. Heekeren H.R., Marrett S., Ungerleider L.G. The neural systems that mediate human perceptual decision making. Nat Rev Neurosci 2008, 9:467-479.
36. Ho T.C., Brown S., Serences J.T. Domain general mechanisms of perceptual decision making in human cortex. J Neurosci 2009, 29:8675-8687.
37. Jabbi M., Swart M., Keysers C. Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 2007, 34:1744-1753.
38. Johnstone T., van Reekum C.M., Oakes T.R., Davidson R.J. The voice of emotion: an FMRI study of neural responses to angry and happy vocal expressions. Soc Cogn Affect Neurosci 2006, 1:242-249.
39. Kikyo H., Ohki K., Miyashita Y. Neural correlates for feeling-of-knowing: an fMRI parametric analysis. Neuron 2002, 36:177-186.
40. Koelsch S., Fritz T.v., Cramon D.Y., Müller K., Friederici A.D. Investigating emotion with music: an fMRI study. Hum Brain Mapp 2006, 27:239-250.
41. Kosillo P., Smith A.T. The role of the human anterior insular cortex in time processing. Brain Struct Funct 2010, 214:623-628.
42. Krebs R.M., Boehler C.N., Roberts K.C., Song A.W., Woldorff M.G. The involvement of the dopaminergic midbrain and cortico-striatal-thalamic circuits in the integration of reward prospect and attentional task demands. Cereb Cortex 2012, 22:607-615.
43. Kurth F., Zilles K., Fox P.T., Laird A.R., Eickhoff S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 2010, 214:519-534.
44. Lamichhane B., Dhamala M. Perceptual decision-making difficulty modulates feedforward effective connectivity to the dorsolateral prefrontal cortex. Front Hum Neurosci 2015, 9:498.
45. Lamichhane B., Dhamala M. The salience network and its functional architecture in a perceptual decision: an effective connectivity study. Brain Connect 2015, 5:362-370.
46. Lamm C., Singer T. The role of anterior insular cortex in social emotions. Brain Struct Funct 2010, 214:579-591.
47. Langner R., Eickhoff S.B. Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. Psychol Bull 2013, 139:870-900.
48. Leibenluft E., Gobbini M.I., Harrison T., Haxby J.V. Mothers' neural activation in response to pictures of their children and other children. Biol Psychiatry 2004, 56:225-232.
49. Lewis J.W., Beauchamp M.S., DeYoe E. A comparison of visual and auditory motion processing in human cerebral cortex. Cereb Cortex 2000, 10:873-888.
50. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 2010, 214:655-667.
51. Mesulam M.M., Mufson E.J. Insula of the old world monkey. II: afferent cortical output and comments on function. J Comp Neurol 1982, 212:23-37.
52. Mesulam M.M., Mufson E.J. Insula of the world monkey. III: efferent cortical output and comments on function. J Comp Neurol 1982, 212:38-52.
53. Miller L.M., D'Esposito M. Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. J Neurosci 2005, 25:5884-5893.
54. Mutschler I., Schulze-Bonhage A., Glauche V., Demandt E., Speck O., Ball T. A rapid sound-action association effect in human insular cortex. PLoS ONE 2007, 2:e259.
55. Pallaer K.A., Ranganath C., Gonsalves B., LaBar K.S., Parrish T.B., Gitleman D.R., Mesulam M.-M., Reber P.J. Neural correlates of person recognition. Learn Mem 2003, 10:253-260.
56. Pessoa L., Engelmann J.B. Embedding reward signals into perception and cognition. Front Neurosci 2010, 4.
57. Pessoa L., Padmala S. Decoding near-threshold perception of fear from distributed single-trial brain activation. Cereb Cortex 2007, 17:691-701.
58. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002, 16:331-348.
59. Philiastides M.G., Sajda P. EEG-informed fMRI reveals spatiotemporal characteristics of perceptual decision making. J Neurosci 2007, 27:13082-13091.
60. Platel H., Price C., Baron J.-C., Wise R., Lambert J., Frackowiak R.S.J., Lechevalier B., Eustache F. The structural components of music perception: a functional anatomical study. Brain 1997, 120:229-243.
61. Ploner M., Lee M.C., Wiech K., Bingel U., Tracey I. Prestimulus functional connectivity determines pain perception in humans. Proc Natl Acad Sci U S A 2010, 107:355-360.
62. Ploran E.J., Nelson S.M., Velanova K., Donaldson D.I., Petersen S.E., Wheeler M.E. Evidence accumulation and the moment of recognition: dissociating perceptual recognition processes using fMRI. J Neurosci 2007, 27:11912-11924.
63. Pons F., Lewkowicz D.J. Infant perception of audio-visual speech synchrony in familiar and unfamiliar fluent speech. Acta Psychol 2014, 149:142-147.
64. Preuschoff K., Quartz S.R., Bossaerts P. Human insula activation reflects risk prediction errors as well as risk. J Neurosci 2008, 28:2745-2752.
65. Rainer G., Miller E.K. Effects of visual experience on the representation of objects in the prefrontal cortex. Neuron 2000, 27:179-189.
66. Rebola J., Castelhano J., Ferreira C., Castelo-Branco M. Functional parcellation of the operculo-insular cortex in perceptual decision making: an fMRI study. Neuropsychologia 2012, 50:3693-3701.
67. Rubia K., Smith A.T. The neural correlates of cognitive time management: a review. Acta Neurobiol Exp (Wars) 2004, 64:329-340.
68. Rushworth M.F., Walton M.E., Kennerley S.W., Bannerman D.M. Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 2004, 8:410-417.
69. Schubotz R.I., Friederici A.D., von Cramon D.Y. Time perception and motor timing: a common cortical and subcortical basis revealed by fMRI. Neuroimage 2000, 11:1-12.
70. Shenhav A., Botvinick M.M., Cohen J.D. The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 2013, 79:217-240.
71. Singer T., Critchley H.D., Preuschoff K. A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 2009, 13:334-340.
72. Sridharan D., Levitin D.J., Menon V. A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad U S A 2008, 105:12569-12574.
73. Srinivasan L., Asaad W.F., Ginat D.T., Gale J.T., Dougherty D.D., Williams Z.M., Sejnowski T.J., Eskandar E.N. Action initiation in the human dorsal anterior cingulate cortex. PLoS ONE 2013, 8:e55247.
74. Sterzer P., Kleinschmidt A. Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 2010, 214:611-622.
75. Takahashi H., Matsuura M., Koeda M., Yahata N., Suhara T., Kato M., Okubo Y. Brain activations during judgments of positive self-conscious emotion and positive basic emotion: pride and joy. Cereb Cortex 2008, 18:898-903.
76. Thielscher A., Pessoa L. Neural correlates of perceptual choice and decision making during fear-disgust discrimination. J Neurosci 2007, 27:2908-2917.
77. Tosoni A., Galati G., Romani G.L., Corbetta M. Sensory-motor mechanisms in human parietal cortex underlie arbitrary visual decisions. Nat Neurosci 2008, 11:1446-1453.
78. Touroutoglou A., Hollenbeck M., Dickerson B.C., Feldman Barrett L. Dissociable large-scale networks anchored in the right anterior insula subserve affective experience and attention. Neuroimage 2012, 60:1947-1958.
79. Tregellas J.R., Davalos D.B., Rojas D.C. Effect of task difficulty on the functional anatomy of temporal processing. Neuroimage 2006, 32:307-315.
80. Tsukiura T., Fujii T., Fukatsu R., Otsuki T., Okuda J., Umetsu A., Suzuki K., Tabuchi M., Yanagawa I., Nagasaka T., Kawashima R., Fukuda H., Takahashi S., Yamadori A. Neural basis of the retrieval of people's names: evidence from brain-damaged patients and fMRI. J Cogn Neurosci 2002, 14:922-937.
81. Uddin L.Q., Kinnison J., Pessoa L., Anderson M.L. Beyond the tripartite cognition-emotion-interoception model of the human insular cortex. J Cogn Neurosci 2014, 26:16-27.
82. van Eijk R.L.J., Kohlrausch A., Juola J.F., van de Par S. Audiovisual synchrony and temporal order judgments: effects of experimental method and stimulus type. Percept Psychophys 2008, 70:955-968.
83. van Wassenhove V., Grant K.W., Poeppel D. Temporal window of integration in auditory-visual speech perception. Neuropsychologia 2007, 45:598-607.
84. Venkatraman V., Rosati A.G., Taren A.A., Huettel S.A. Resolving response, decision, and strategic control: evidence for a functional topography in dorsomedial prefrontal cortex. J Neurosci 2009, 29:13158-13164.
85. Wiech K., Lin C.S., Brodersen K.H., Bingel U., Ploner M., Tracey I. Anterior insula integrates information about salience into perceptual decisions about pain. J Neurosci 2010, 30:16324-16331.
86. Woolgar A., Hampshire A., Thompson R., Duncan J. Adaptive coding of task-relevant information in human frontoparietal cortex. J Neurosci 2011, 31:14592-14599.
87. Zampini M., Guest S., Shore D.I., Spence C. Audio-visual simultaneity judgments. Percept Psychophys 2005, 67:531-544.
88. Zampini M., Shore D.I., Spence C. Audiovisual temporal order judgments. Exp Brain Res 2003, 152:198-210.