Infusion of D1 dopamine receptor agonist into medial frontal cortex disrupts neural correlates of interval timing

Frontiers in Behavioral Neuroscience

Volumn 9, Issue NOVEMBER, 2015, Pages

  Parker, Krystal L ^a   Ruggiero, Rafael N ^a   Narayanan, Nandakumar S ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Cognition; Dopamine; Interval timing; Medial frontal cortex; Parkinson s disease

Indexed keywords

3 ALLYL 6 CHLORO 2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; DOPAMINE 1 RECEPTOR;

ALPHA RHYTHM; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DELTA RHYTHM; DOPAMINE BRAIN LEVEL; ELECTRIC POTENTIAL; FRONTAL CORTEX; INTERVAL TIMING; MALE; MEDIAL FRONTAL CORTEX; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; RAT; SIGNAL TRANSDUCTION; TASK PERFORMANCE; TIME;

EID: 84947750707     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00294     Document Type: Article

References (46)

1. Abi-Dargham, A., Mawlawi, O., Lombardo, I., Gil, R., Martinez, D., Huang, Y., et al. (2002). Prefrontal dopamine D1 receptors and working memory in schizophrenia. J. Neurosci. 22, 3708-3719
2. Bekolay, T., Laubach, M., and Eliasmith, C. (2014). A spiking neural integrator model of the adaptive control of action by the medial prefrontal cortex. J. Neurosci. 34, 1892-1902. doi: 10.1523/JNEUROSCI.2421-13.2014
3. Bellgrove, M. A., Domschke, K., Hawi, Z., Kirley, A., Mullins, C., Robertson, I. H., et al. (2005). The methionine allele of the COMT polymorphism impairs prefrontal cognition in children and adolescents with ADHD. Exp. Brain Res. 163, 352-360. doi: 10.1007/s00221-004-2180-y
4. Caetano, M. S., and Church, R. M. (2009). A comparison of responses and stimuli as time markers. Behav. Processes 81, 298-302. doi: 10.1016/j.beproc.2009.01.014
5. Cavanagh, J. F., Cohen, M. X., and Allen, J. J. B. (2009). Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. J. Neurosci. 29, 98-105. doi: 10.1523/JNEUROSCI.4137-08.2009
6. Cavanagh, J. F., and Frank, M. J. (2014). Frontal theta as a mechanism for cognitive control. Trends Cogn. Sci. (Regul. Ed). 18, 414-421. doi: 10.1016/j.tics.2014.04.012
7. Chapin, J. K., and Nicolelis, M. A. (1999). Principal component analysis of neuronal ensemble activity reveals multidimensional somatosensory representations. J. Neurosci. Methods 94, 121-140. doi: 10.1016/S0165-0270(99)00130-2
8. Cools, R., Barker, R. A., Sahakian, B. J., and Robbins, T. W. (2001). Enhanced or impaired cognitive function in Parkinson’s disease as a function of dopaminergic medication and task demands. Cereb. Cortex 11, 1136-1143. doi: 10.1093/cercor/11.12.1136
9. Cools, R., and 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
10. Cools, R., Miyakawa, A., Sheridan, M., and D’Esposito, M. (2010). Enhanced frontal function in Parkinson’s disease. Brain 133, 225-233. doi: 10.1093/brain/awp301
11. Durstewitz, D. (2003). Self-organizing neural integrator predicts interval times through climbing activity. J. Neurosci. 23, 5342-5353
12. Fry, W., Kelleher, R. T., and Cook, L. (1960). A mathematical index of performance on fixed-interval schedules of reinforcement. J. Exp. Anal. Behav. 3, 193-199. doi: 10.1901/jeab.1960.3-193
13. Gilmore, J. H., Watts, V. J., Lawler, C. P., Noll, E. P., Nichols, D. E., and Mailman, R. B. (1995). "Full" dopamine D1 agonists in human caudate: biochemical properties and therapeutic implications. Neuropharmacology 34, 481-488. doi: 10.1016/0028-3908(95)00014-W
14. Goldman-Rakic, P. S. (1998). The cortical dopamine system: role in memory and cognition. Adv. Pharmacol. 42, 707-711. doi: 10.1016/S1054-3589(08)60846-7
15. Goldman-Rakic, P. S., Castner, S. A., Svensson, T. H., Siever, L. J., and Williams, G. V. (2004). Targeting the dopamine D1 receptor in schizophrenia: insights for cognitive dysfunction. Psychopharmacology (Berl). 174, 3-16. doi: 10.1007/s00213-004-1793-y
16. Granon, S., Passetti, F., Thomas, K. L., Dalley, J. W., Everitt, B. J., and Robbins, T. W. (2000). Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. J. Neurosci. 20, 1208-1215
17. Heijtz, R. D., Kolb, B., and Forssberg, H. (2007). Motor inhibitory role of dopamine D1 receptors: implications for ADHD. Physiol. Behav. 92, 155-160. doi: 10.1016/j.physbeh.2007.05.024
18. Janssen, P., and Shadlen, M. N. (2005). A representation of the hazard rate of elapsed time in macaque area LIP. Nat. Neurosci. 8, 234-241. doi: 10.1038/nn1386
19. Kim, J., Ghim, J.-W., Lee, J. H., and Jung, M. W. (2013). Neural correlates of interval timing in rodent prefrontal cortex. J. Neurosci. 33, 13834-13847. doi: 10.1523/JNEUROSCI.1443-13.2013
20. Kim, Y.-C., Alberico, S. L., Emmons, E., and Narayanan, N. S. (2015). New therapeutic strategies targeting D1-type dopamine receptors for neuropsychiatric disease. Front. Biol. 10, 230-238. doi: 10.1007/s11515-015-1360-4
21. Kobayashi, S., and Schultz, W. (2008). Influence of reward delays on responses of dopamine neurons. J. Neurosci. 28, 7837-7846. doi: 10.1523/JNEUROSCI.1600-08.2008
22. Kroener, S., Chandler, L. J., Phillips, P. E. M., and Seamans, J. K. (2009). Dopamine modulates persistent synaptic activity and enhances the signal-to-noise ratio in the prefrontal cortex. PLoS ONE 4:e6507. doi: 10.1371/journal.pone.0006507
23. Laubach, M. (2011) "A comparative perspective on executive and motivational control by the medial prefrontal cortex," in Neural Basis of Motivational and Cognitive Control, eds R. B. Mars, J. Sallet, M. F. S. Rushworth, and N. Yeung (Cambridge, MA: MIT Press), 95-109. doi: 10.7551/mitpress/9780262016438.003.0006
24. Merchant, H., and de Lafuente, V. (2014). Introduction to the neurobiology of interval timing. Adv. Exp. Med. Biol. 829, 1-13. doi: 10.1007/978-1-4939-1782-2_1
25. Merchant, H., Luciana, M., Hooper, C., Majestic, S., and Tuite, P. (2008). Interval timing and Parkinson’s disease: heterogeneity in temporal performance. Exp. Brain Res. 184, 233-248. doi: 10.1007/s00221-007-1097-7
26. Narayanan, N. S., Cavanagh, J. F., Frank, M. J., and Laubach, M. (2013b). Common medial frontal mechanisms of adaptive control in humans and rodents. Nat. Neurosci. 16, 1888-1897. doi: 10.1038/nn.3549
27. Narayanan, N. S., Land, B. B., Solder, J. E., Deisseroth, K., and DiLeone, R. J. (2012). Prefrontal D1 dopamine signaling is required for temporal control. Proc. Natl. Acad. Sci. U.S.A. 109, 20726-20731. doi: 10.1073/pnas.1211258109
28. Narayanan, N. S., and Laubach, M. (2006). Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron 52, 921-931. doi: 10.1016/j.neuron.2006.10.021
29. Narayanan, N. S., and Laubach, M. (2008). Neuronal correlates of post-error slowing in the rat dorsomedial prefrontal cortex. J. Neurophysiol. 100, 520-525. doi: 10.1152/jn.00035.2008
30. Narayanan, N. S., and Laubach, M. (2009). Delay activity in rodent frontal cortex during a simple reaction time task. J. Neurophysiol. 101, 2859-2871. doi: 10.1152/jn.90615.2008
31. Narayanan, N. S., and Laubach, M. (2014). "Methods for studying functional interactions among neuronal populations," in Dynamic Brain Imaging (Springer), 135-165. Available at: http://link.springer.com/protocol/10.1007/978-1-59745-543-5_7 [Accessed October 23, 2014]
32. Narayanan, N. S., Rodnitzky, R. L., and Uc, E. Y. (2013a). Prefrontal dopamine signaling and cognitive symptoms of Parkinson’s disease. Rev. Neurosci. 24, 267-278. doi: 10.1515/revneuro-2013-0004
33. Parker, K. L., Alberico, S. L., Miller, A. D., and Narayanan, N. S. (2013b). Prefrontal D1 dopamine signaling is necessary for temporal expectation during reaction time performance. Neuroscience 255, 246-254. doi: 10.1016/j.neuroscience.2013.09.057
34. Parker, K. L., Chen, K.-H., Kingyon, J. R., Cavanagh, J. F., and Narayanan, N. S. (2014). D1-dependent 4 Hz oscillations and ramping activity in rodent medial frontal cortex during interval timing. J. Neurosci. 34, 16774-16783. doi: 10.1523/JNEUROSCI.2772-14.2014
35. Parker, K. L., Chen, K.-H., Kingyon, J. R., Cavanagh, J. F., and Narayanan, N. S. (2015). Medial frontal 4-Hz activity in humans and rodents is attenuated in PD patients and in rodents with cortical dopamine depletion. J. Neurophysiol. 114, 1310-1320. doi: 10.1152/jn.00412.2015
36. Parker, K. L., Lamichhane, D., Caetano, M. S., and Narayanan, N. S. (2013a). Executive dysfunction in Parkinson’s disease and timing deficits. Front. Integr. Neurosci. 7:75. doi: 10.3389/fnint.2013.00075
37. Paz, R., Natan, C., Boraud, T., Bergman, H., and Vaadia, E. (2005). Emerging patterns of neuronal responses in supplementary and primary motor areas during sensorimotor adaptation. J. Neurosci. 25, 10941-10951. doi: 10.1523/JNEUROSCI.0164-05.2005
38. Reutimann, J., Yakovlev, V., Fusi, S., and Senn, W. (2004). Climbing neuronal activity as an event-based cortical representation of time. J. Neurosci. 24, 3295-3303. doi: 10.1523/JNEUROSCI.4098-03.2004
39. Ryman-Rasmussen, J. P., Nichols, D. E., and Mailman, R. B. (2005). Differential activation of adenylate cyclase and receptor internalization by novel dopamine D1 receptor agonists. Mol. Pharmacol. 68, 1039-1048. doi: 10.1124/mol.105.012153
40. Sauseng, P., Klimesch, W., Doppelmayr, M., Pecherstorfer, T., Freunberger, R., and Hanslmayr, S. (2005). EEG alpha synchronization and functional coupling during top-down processing in a working memory task. Hum. Brain Mapp. 26, 148-155. doi: 10.1002/hbm.20150
41. Seamans, J. K., and Yang, C. R. (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
42. Vijayraghavan, S., Wang, M., Birnbaum, S. G., Williams, G. V., and Arnsten, A. F. T. (2007). Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat. Neurosci. 10, 376-384. doi: 10.1038/nn1846
43. Williams, G. V., and Goldman-Rakic, P. S. (1995). Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376, 572-575. doi: 10.1038/376572a0
44. Xu, M., Zhang, S.-Y., Dan, Y., and Poo, M.-M. (2014). Representation of interval timing by temporally scalable firing patterns in rat prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 111, 480-485. doi: 10.1073/pnas.1321314111
45. Yang, C. R., and Seamans, J. K. (1996). Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J. Neurosci. 16, 1922-1935
46. Zahrt, J., Taylor, J. R., Mathew, R. G., and Arnsten, A. F. T. (1997). Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J. Neurosci. 17, 8528-8535