Advertisement

Psychopharmacology

, Volume 232, Issue 6, pp 1061–1070 | Cite as

Dopaminergic modulation of distracter-resistance and prefrontal delay period signal

  • Mirjam BloemendaalEmail author
  • Martine R. van Schouwenburg
  • Asako Miyakawa
  • Esther Aarts
  • Mark D’Esposito
  • Roshan Cools
Original Investigation

Abstract

Dopamine has long been implicated in the online maintenance of information across short delays. Specifically, dopamine has been proposed to modulate the strength of working memory representations in the face of intervening distracters. This hypothesis has not been tested in humans. We fill this gap using pharmacological neuroimaging. Healthy young subjects were scanned after intake of the dopamine receptor agonist bromocriptine or placebo (in a within-subject, counterbalanced, and double-blind design). During scanning, subjects performed a delayed match-to-sample task with face stimuli. A face or scene distracter was presented during the delay period (between the cue and the probe). Bromocriptine altered distracter-resistance, such that it impaired performance after face relative to scene distraction. Individual differences in the drug effect on distracter-resistance correlated negatively with drug effects on delay period signal in the prefrontal cortex, as well as on functional connectivity between the prefrontal cortex and the fusiform face area. These results provide evidence for the hypothesis that dopaminergic modulation of the prefrontal cortex alters resistance of working memory representations to distraction. Moreover, we show that the effects of dopamine on the distracter-resistance of these representations are accompanied by modulation of the functional strength of connections between the prefrontal cortex and stimulus-specific posterior cortex.

Keywords

Working memory Distraction Dopamine Prefrontal cortex Connectivity fMRI 

Supplementary material

213_2014_3741_MOESM1_ESM.docx (1.2 mb)
ESM 1 (DOCX 1197 kb)

References

  1. Barde LHF, Thompson-Schill SL (2002) Models of functional organization of the lateral prefrontal cortex in verbal working memory: evidence in favor of the process model. J Cogn Neurosci 14:1054–1063. doi: 10.1162/089892902320474508 CrossRefPubMedGoogle Scholar
  2. Brozoski T, Brown R, Rosvold H, Goldman P (1979) Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205(80):929–932CrossRefPubMedGoogle Scholar
  3. Chao LL, Knight RT (1995) Human prefrontal lesions increase distractibility to irrelevant sensory inputs. Neuroreport 6:1605–1610CrossRefPubMedGoogle Scholar
  4. Clapp WC, Rubens MT, Gazzaley A (2010) Mechanisms of working memory disruption by external interference. Cereb Cortex 20:859–872. doi: 10.1093/cercor/bhp150 CrossRefPubMedCentralPubMedGoogle Scholar
  5. Collins P, Wilkinson LS, Everitt BJ et al (2000) The effect of dopamine depletion from the caudate nucleus of the common marmoset (Callithrix jacchus) on tests of prefrontal cognitive function. Behav Neurosci 114:3–17CrossRefPubMedGoogle Scholar
  6. Cools R, D’Esposito M (2011) Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 69:e113–e125. doi: 10.1016/j.biopsych.2011.03.028 CrossRefPubMedCentralPubMedGoogle Scholar
  7. Cools R, Frank MJ, Gibbs SE et al (2009) Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J Neurosci 29:1538–1543. doi: 10.1523/JNEUROSCI.4467–08.2009 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Cools R, Sheridan M, Jacobs E, D’Esposito M (2007) Impulsive personality predicts dopamine-dependent changes in frontostriatal activity during component processes of working memory. J Neurosci 27:5506–5514. doi: 10.1523/JNEUROSCI.0601-07.2007 CrossRefPubMedGoogle Scholar
  9. Cools R, Stefanova E, Barker RA et al (2002) Dopaminergic modulation of high-level cognition in Parkinson’s disease: the role of the prefrontal cortex revealed by PET. Brain 125:584–594. doi: 10.1093/brain/awf052 CrossRefPubMedGoogle Scholar
  10. Curtis CE, Rao VY, D’Esposito M (2004) Maintenance of spatial and motor codes during oculomotor delayed response tasks. J Neurosci 24:3944–3952. doi: 10.1523/JNEUROSCI.5640–03.2004 CrossRefPubMedGoogle Scholar
  11. Diamond A (2007) Consequences of variations in genes that affect dopamine in prefrontal cortex. Cereb Cortex 17(Suppl 1):i161–i170. doi: 10.1093/cercor/bhm082 CrossRefPubMedCentralPubMedGoogle Scholar
  12. Druzgal TJ, D’Esposito M (2003) Dissecting contributions of prefrontal cortex and fusiform face area to face working memory. J Cogn Neurosci 15:771–784. doi: 10.1162/089892903322370708 CrossRefPubMedGoogle Scholar
  13. Durstewitz D, Kelc M, Güntürkün O (1999) A neurocomputational theory of the dopaminergic modulation of working memory functions. J Neurosci 19:2807–2822PubMedGoogle Scholar
  14. Durstewitz D, Seamans JK (2008) The dual-state theory of prefrontal cortex dopamine function with relevance to catechol-o-methyltransferase genotypes and schizophrenia. Biol Psychiatry 64:739–749. doi: 10.1016/j.biopsych.2008.05.015 CrossRefPubMedGoogle Scholar
  15. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83:1733–1750PubMedGoogle Scholar
  16. Feredoes E, Heinen K, Weiskopf N, et al. (2011) Causal evidence for frontal involvement in memory target maintenance by posterior brain areas during distracter interference of visual working memory. PNAS. doi: 10.1073/pnas.1106439108Google Scholar
  17. Floresco SB (2013) Prefrontal dopamine and behavioral flexibility: shifting from an “inverted-U” toward a family of functions. Front Neurosci 7:62. doi: 10.3389/fnins.2013.00062 CrossRefPubMedCentralPubMedGoogle Scholar
  18. Fuster JM, Alexander G. (1971) Neuron activity related to short-term memory. Science (80) 652–654.Google Scholar
  19. Gazzaley A, Rissman J, D’Esposito M (2004) Functional connectivity during working memory maintenance. Cogn Affect Behav Neurosci 4:580–599CrossRefPubMedGoogle Scholar
  20. Gibbs SEB, D’Esposito M (2005) A functional MRI study of the effects of bromocriptine, a dopamine receptor agonist, on component processes of working memory. Psychopharmacology (Berl) 180:644–653. doi: 10.1007/s00213-005-0077-5 CrossRefGoogle Scholar
  21. Jacobsen CF (1936) Studies of Cerebral Function in Primates. Psychol, CompGoogle Scholar
  22. Jha AP, Fabian SA, Aguirre GK (2004) The role of prefrontal cortex in resolving distractor interference. Cogn Affect Behav Neurosci 4:517–527CrossRefPubMedGoogle Scholar
  23. Jha AP, McCarthy G (2000) The influence of memory load upon delay-interval activity in a working-memory task: an event-related functional MRI study. J Cogn Neurosci 12(Suppl 2):90–105. doi: 10.1162/089892900564091 CrossRefPubMedGoogle Scholar
  24. Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311PubMedGoogle Scholar
  25. Kvernmo T, Härtter S, Burger E (2006) A review of the receptor-binding and pharmacokinetic properties of dopamine agonists. Clin Ther 28:1065–1078. doi: 10.1016/j.clinthera.2006.08.004 CrossRefPubMedGoogle Scholar
  26. Luciana M, Collins P (1992) Dopaminergic modulation of working n memory for spatial but not object cues in normal humans. J Cogn Neurosci 330–347Google Scholar
  27. Malmo RB (1942) Interference factors in delayed response in monkeys after removal of frontal lobes. J Neurophysiol 5:295–308Google Scholar
  28. Mattay V, Tessitore A (2002) Dopaminergic modulation of cortical function in patients with Parkinson’s disease. Ann Neurol 51:156–164. doi: 10.1002/ana.10078 CrossRefPubMedGoogle Scholar
  29. Mehta MA, Riedel WJ (2006) Dopaminergic enhancement of cognitive function. Curr Pharm Des 12:2487–2500CrossRefPubMedGoogle Scholar
  30. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202. doi: 10.1146/annurev.neuro.24.1.167 CrossRefPubMedGoogle Scholar
  31. Miller EK, Erickson CA, Desimone R (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16:5154–5167PubMedGoogle Scholar
  32. Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt impulsiveness scale. J Clin Psychol 51:768–774CrossRefPubMedGoogle Scholar
  33. Pessoa L, Gutierrez E, Bandettini P, Ungerleider L (2002) Neural correlates of visual working memory: fMRI amplitude predicts task performance. Neuron 35:975–987CrossRefPubMedGoogle Scholar
  34. Postle BR, Zarahn E, D’Esposito M (2000) Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. Brain Res Brain Res Protoc 5:57–66CrossRefPubMedGoogle Scholar
  35. Rabbit P (1966) Errors and error correction in choice-response tasks. J Exp Psychol 71:264–272CrossRefGoogle Scholar
  36. Ranganath C, Cohen MX, Dam C, D’Esposito M (2004) Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. J Neurosci 24:3917–3925. doi: 10.1523/JNEUROSCI.5053-03.2004 CrossRefPubMedGoogle Scholar
  37. Sawaguchi T, Goldman-Rakic PS (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251(80):947–950CrossRefPubMedGoogle Scholar
  38. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1–58. doi: 10.1016/j.pneurobio.2004.05.006 CrossRefPubMedGoogle Scholar
  39. Seeman P, van Tol HM (1994) Dopamine receptor pharmacology. TiPS 15:264–270. doi: 10.1016/S0072–9752(07)83004–1 PubMedGoogle Scholar
  40. Servan-Schreiber D, Printz H, Cohen JD (1990) A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. Science 249(80):892–895CrossRefPubMedGoogle Scholar
  41. Sreenivasan KK, Curtis CE, D’Esposito M (2014) Revisiting the role of persistent neural activity during working memory. Trends Cogn Sci 18:82–89. doi: 10.1016/j.tics.2013.12.001 CrossRefPubMedCentralPubMedGoogle Scholar
  42. Wang M, Vijayraghavan S, Goldman-Rakic PS (2004) Selective D2 receptor actions on the functional circuitry of working memory. Science 303(80):853–856. doi: 10.1126/science.1091162 CrossRefPubMedGoogle Scholar
  43. Yoon JH, Curtis CE, D’Esposito M (2006) Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex. Neuroimage 29:1117–1126. doi: 10.1016/j.neuroimage.2005.08.024 CrossRefPubMedGoogle Scholar
  44. Zarahn E, Aguirre G, D’Esposito M (1997) A trial-based experimental design for fMRI. Neuroimage 6:122–138. doi: 10.1006/nimg.1997.0279 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Mirjam Bloemendaal
    • 1
    Email author
  • Martine R. van Schouwenburg
    • 1
    • 2
    • 4
  • Asako Miyakawa
    • 3
  • Esther Aarts
    • 1
  • Mark D’Esposito
    • 3
  • Roshan Cools
    • 1
    • 2
  1. 1.Radboud University NijmegenDonders Institute for Brain, Cognition and Behaviour, Centre for Cognitive NeuroimagingNijmegenThe Netherlands
  2. 2.RadboudumcDonders Institute for Brain, Cognition and Behaviour, Department of PsychiatryNijmegenThe Netherlands
  3. 3.Helen Wills Neuroscience InstituteUniversity of CaliforniaBerkeleyUSA
  4. 4.Department of NeurologyUniversity of CaliforniaSan FranciscoUSA

Personalised recommendations