Serotonergic modulation of spatial working memory: Predictions from a computational network model

Frontiers in Integrative Neuroscience

Volumn 7, Issue SEP, 2013, Pages

  Cano Colino, Maria ^a   Almeida, Rita ^a,b   Come, Albert ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Computational model; Metacognition; Persistent activity; Prefrontal cortex; Working memory

Indexed keywords

SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN 2A RECEPTOR;

ARTICLE; ASSOCIATION; COGNITION; DISTRACTIBILITY; MENTAL PERFORMANCE; NERVE CELL NETWORK; NEUROMODULATION; PREDICTION; PREFRONTAL CORTEX; SPATIAL MEMORY; WORKING MEMORY;

EID: 84885048658     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2013.00071     Document Type: Article

References (94)

1. Amargós-Bosch, M., Bortolozzi, A., Puig, M. V., Serrats, J., Adell, A., Celada, P., et al. (2004). Co-expression and in vivo interaction of serotonin1A and serotonin2A receptors in pyramidal neurons of prefrontal cortex. Cereb. Cortex 14, 281-299. doi: 10.1093/cercor/bhg128
2. Andrade, R., Malenka, R. C., and Nicoll, R. A. (1986). A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234, 1261-1265. doi: 10.1126/science.2430334
3. Araneda, R., and Andrade, R. (1991). 5-Hydroxytryptamine2 and 5-hydroxytryptamine1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 40, 399-412. doi: 10.1016/0306-4522(91)90128-B
4. Arnsten, A. F. T. (2011). Catecholamine influences on dorsolateral prefrontal cortical networks. Biol. Psychiatry 69, e89-e99. doi: 10.1016/j.biopsych.2011.01.027
5. Arnsten, A. F. T., Wang, M. J., and Paspalas, C. D. (2012). Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses. Neuron 76, 223-239. doi: 10.1016/j.neuron.2012.08.038
6. Aston-Jones, G., and Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403-450. doi: 10.1146/annurev.neuro.28.061604.135709
7. Barnes, N. M., and Sharp, T. (1999). A review of central 5-HT receptors and their function. Neuropharmacology 38, 1083-1152. doi: 10.1016/S0028-3908(99)00010-6
8. Béïque, J.-C., Campbell, B., Perring, P., Hamblin, M. W., Walker, P., Mladenovic, L., et al. (2004). Serotonergic regulation of membrane potential in developing rat prefrontal cortex: coordinated expression of 5-Hydroxytryptamine (5-HT)1A, 5-HT2A, and 5-HT7 receptors. J. Neurosci. 24, 4807-4817. doi: 10.1523/JNEUROSCI.5113-03.2004
9. Brozoski, T. J., Brown, R. M., Rosvold, H. E., and Goldman, P. S. (1979). Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205, 929-932. doi: 10.1126/science.112679
10. Brunel, N., and Wang, X. J. (2001). Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition. J. Comput. Neurosci. 11, 63-85. doi: 10.1023/A:1011204814320
11. Cano-Colino, M., Almeida, R., Gomez-Cabrero, D., Artigas, F., and Compte, A. (2013). Serotonin regulates performance nonmonotonically in a spatial working memory network. Cereb. Cortex doi: 10.1093/cercor/bht096. [Epub ahead of print].
12. Cano-Colino, M., and Compte, A. (2012). A computational model for spatial working memory deficits in schizophrenia. Pharmacopsychiatry 45(Suppl. 1), S49-S56. doi: 10.1055/s-0032-1306314
13. Carter, O. L., Burr, D. C., Pettigrew, J. D., Wallis, G. M., Hasler, F., and Vollenweider, F. X. (2005). Using Psilocybin to investigate the relationship between attention, working memory, and the serotonin 1A and 2A receptors. J. Cogn. Neurosci. 17, 1497-1508. doi: 10.1162/089892905774597191
14. Celada, P., Puig, M. V., and Artigas, F. (2013). Serotonin modulation of cortical neurons and networks. Front. Integr. Neurosci. 7:25. doi: 10.3389/fnint.2013.00025
15. Celada, P., Puig, M. V., Casanovas, J. M., Guillazo, G., and Artigas, F. (2001). Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABA(A), and glutamate receptors. J. Neurosci. 21, 9917-9929.
16. Chudasama, Y., and Robbins, T. W. (2004). Dopaminergic modulation of visual attention and working memory in the rodent prefrontal cortex. Neuropsychopharmacology 29, 1628-1636. doi: 10.1038/sj.npp.1300490
17. Clarke, H. F., Dalley, J. W., Crofts, H. S., Robbins, T. W., and Roberts, A. C. (2004). Cognitive inflexibility after prefrontal serotonin depletion. Science 304, 878-880. doi: 10.1126/science.1094987
18. Clarke, H. F., Walker, S. C., Crofts, H. S., Dalley, J. W., Robbins, T. W., and Roberts, A. C. (2005). Prefrontal serotonin depletion affects reversal learning but not attentional set shifting. J. Neurosci. 25, 532-538. doi: 10.1523/JNEUROSCI.3690-04.2005
19. Clarke, H. F., Walker, S. C., Dalley, J. W., Robbins, T. W., and Roberts, A. C. (2007). Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. Cereb. Cortex 17, 18-27. doi: 10.1093/cercor/bhj120
20. Compte, A., Brunel, N., Goldman-Rakic, P. S., and Wang, X. J. (2000). Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb. Cortex 10, 910-923. doi: 10.1093/cercor/10.9.910
21. 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
22. Deakin, J. F. (1991). Depression and 5HT. Int. Clin. Psychopharmacol. 6(Suppl. 3), 23-28. discussion: 29-31. doi: 10.1097/00004850-199112003-00002
23. De Almeida, J., Palacios, J. M., and Mengod, G. (2008). "Distribution of 5-HT and DA receptors in primate prefrontal cortex: implications for pathophysiology and treatment, " in Serotonin-Dopamine Interaction: Experimental Evidence and Therapeutic Relevance (Elsevier), 101-115. Available online at: http://www.sciencedirect.com/science/article/pii/S0079612308009059
24. Deng, P.-Y., Poudel, S. K. S., Rojanathammanee, L., Porter, J. E., and Lei, S. (2007). Serotonin inhibits neuronal excitability by activating two-pore domain k+ channels in the entorhinal cortex. Mol. Pharmacol. 72, 208-218. doi: 10.1124/mol.107.034389
25. Destexhe, A., Mainen, Z. F., and Sejnowski, T. J. (1994). Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J. Comput. Neurosci. 1, 195-230. doi: 10.1007/BF00961734
26. Durstewitz, D., and Seamans, J. K. (2002). The computational role of dopamine D1 receptors in working memory. Neural Netw. 15, 561-572. doi: 10.1016/S0893-6080(02)00049-7
27. Eckhoff, P., Wong-Lin, K. F., and Holmes, P. (2009). Optimality and robustness of a biophysical decision-making model under norepinephrine modulation. J. Neurosci. 29, 4301-4311. doi: 10.1523/JNEUROSCI.5024-08.2009
28. Edin, F., Klingberg, T., Johansson, P., McNab, F., Tegnér, J., and Compte, A. (2009). Mechanism for top-down control of working memory capacity. Proc. Natl. Acad. Sci. U.S.A. 106, 6802-6807. doi: 10.1073/pnas.0901894106
29. Ellis, K. A., and Nathan, P. J. (2001). The pharmacology of human working memory. Int. J. Neuropsychopharmacol. 4, 299-313. doi: 10.1017/S1461145701002541
30. Evers, E. A. T., Cools, R., Clark, L., van der Veen, F. M., Jolles, J., Sahakian, B. J., et al. (2005). Serotonergic modulation of prefrontal cortex during negative feedback in probabilistic reversal learning. Neuropsychopharmacology 30, 1138-1147. doi: 10.1038/sj.npp.1300663
31. Flavell, J. H. (1979). Metacognition and cognitive monitoring: a new area of cognitive-developmental inquiry. Am. Psychol. 34, 906-911. doi: 10.1037/0003-066X.34.10.906
32. Floresco, S. B., and Phillips, A. G. (2001). Delay-dependent modulation of memory retrieval by infusion of a dopamine D1 agonist into the rat medial prefrontal cortex. Behav. Neurosci. 115, 934-939. doi: 10.1037/0735-7044.115.4.934
33. Froestl, W., Muhs, A., and Pfeifer, A. (2012). Cognitive enhancers (Nootropics). Part 1: drugs interacting with receptors. J. Alzheimers Dis. 32, 793-887.
34. Funahashi, S., Bruce, C. J., and Goldman-Rakic, P. S. (1989). Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331-349.
35. Georgopoulos, A., Schwartz, A., and Kettner, R. (1986). Neuronal population coding of movement direction. Science 233, 1416-1419. doi: 10.1126/science.3749885
36. Goldman-Rakic, P. S. (1995). Cellular basis of working memory. Neuron 14, 477-485. doi: 10.1016/0896-6273(95)90304-6
37. Goodfellow, N. M., Benekareddy, M., Vaidya, V. A., and Lambe, E. K. (2009). Layer II/III of the prefrontal cortex: inhibition by the Serotonin 5-HT1A receptor in development and Stress. J. Neurosci. 29, 10094-10103. doi: 10.1523/JNEUROSCI.1960-09.2009
38. Gruber, A. J., Dayan, P., Gutkin, B. S., and Solla, S. A. (2006). Dopamine modulation in the basal ganglia locks the gate to working memory. J. Comput. Neurosci. 20, 153-166. doi: 10.1007/s10827-005-5705-x
39. Herwig, A., Beisert, M., and Schneider, W. X. (2010). On the spatial interaction of visual working memory and attention: evidence for a global effect from memory-guided saccades. J. Vis. 10, 8. doi: 10.1167/10.5.8
40. Jacobs, B. L., and Azmitia, E. C. (1992). Structure and function of the brain serotonin system. Physiol. Rev. 72, 165-229.
41. Jakab, R. L., and Goldman-Rakic, P. S. (1998). 5-Hydroxytryptamine2A serotonin receptors in the primate cerebral cortex: Possible site of action of hallucinogenic and antipsychotic drugs in pyramidal cell apical dendrites. Proc. Natl. Acad. Sci. U.S.A. 95, 735-740. doi: 10.1073/pnas.95.2.735
42. Lee, C., Rohrer, W. H., and Sparks, D. L. (1988). Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357-360. doi: 10.1038/332357a0
43. Luciana, M., Burgund, E. D., Berman, M., and Hanson, K. L. (2001). Effects of tryptophan loading on verbal, spatial and affective working memory functions in healthy adults. J. Psychopharmacol. 15, 219-230. doi: 10.1177/026988110101500410
44. Luciana, M., Collins, P. F., and Depue, R. A. (1998). Opposing roles for dopamine and serotonin in the modulation of human spatial working memory functions. Cereb. Cortex 8, 218-226. doi: 10.1093/cercor/8.3.218
45. Ma, L., Shalinsky, M. H., Alonso, A., and Dickson, C. T. (2007). Effects of serotonin on the intrinsic membrane properties of layer II medial entorhinal cortex neurons. Hippocampus 17, 114-129. doi: 10.1002/hipo.20250
46. Mayer, J. S., and Park, S. (2012). Working memory encoding and false memory in schizophrenia and bipolar disorder in a spatial delayed response task. J. Abnorm. Psychol. 121, 784-794. doi: 10.1037/a0028836
47. Meeter, M., Talamini, L., Schmitt, J. A. J., and Riedel, W. J. (2006). Effects of 5-HT on memory and the hippocampus: model and data. Neuropsychopharmacology 31, 712-720. doi: 10.1038/sj.npp.1300869
48. Mendelsohn, D., Riedel, W. J., and Sambeth, A. (2009). Effects of acute tryptophan depletion on memory, attention and executive functions: a systematic review. Neurosci. Biobehav. Rev. 33, 926-952. doi: 10.1016/j.neubiorev.2009.03.006
49. Meneses, A. (2007). Do serotonin1-7 receptors modulate short and long-term memory? Neurobiol. Learn. Mem. 87, 561-572. doi: 10.1016/j.nlm.2006.12.005
50. Middlebrooks, P. G., and Sommer, M. A. (2011). Metacognition in monkeys during an oculomotor task. J. Exp. Psychol. Learn. Mem. Cogn. 37, 325-337. doi: 10.1037/a0021611
51. Middlebrooks, P. G., and Sommer, M. A. (2012). Neuronal correlates of metacognition in primate frontal cortex. Neuron 75, 517-530. doi: 10.1016/j.neuron.2012.05.028
52. Murphy, F. C., Smith, K. A., Cowen, P. J., Robbins, T. W., and Sahakian, B. J. (2002). The effects of tryptophan depletion on cognitive and affective processing in healthy volunteers. Psychopharmacology 163, 42-53. doi: 10.1007/s00213-002-1128-9
53. Murray, J. D., Anticevic, A., Gancsos, M., Ichinose, M., Corlett, P. R., Krystal, J. H., et al. (2012). Linking microcircuit dysfunction to cognitive impairment: effects of disinhibition associated with schizophrenia in a cortical working memory model. Cereb. Cortex doi: 10.1093/cercor/bhs370. [Epub ahead of print].
54. Nichols, D. E., and Nichols, C. D. (2008). Serotonin receptors. Chem. Rev. 108, 1614-1641. doi: 10.1021/cr078224o
55. Ögren, S. O., Eriksson, T. M., Elvander-Tottie, E., D'Addario, C., Ekström, J. C., Svenningsson, P., et al. (2008). The role of 5-HT1A receptors in learning and memory. Behav. Brain Res. 195, 54-77. doi: 10.1016/j.bbr.2008.02.023
56. Pannu, J. K., Kaszniak, A. W., and Rapcsak, S. Z. (2005). Metamemory for faces following frontal lobe damage. J. Int. Neuropsychol. Soc. 11, 668-676. doi: 10.1017/S1355617705050873
57. Park, S. B., Coull, J. T., McShane, R. H., Young, A. H., Sahakian, B. J., Robbins, T. W., et al. (1994). Tryptophan depletion in normal volunteers produces selective impairments in learning and memory. Neuropharmacology 33, 575-588. doi: 10.1016/0028-3908(94)90089-2
58. Park, S., and Holzman, P. S. (1992). Schizophrenics show spatial working memory deficits. Arch. Gen. Psychiatry 49, 975-982. doi: 10.1001/archpsyc.1992.01820120063009
59. Park, S., Püschel, J., Sauter, B. H., Rentsch, M., and Hell, D. (1999). Spatial working memory deficits and clinical symptoms in schizophrenia: a 4-month follow-up study. Biol. Psychiatry 46, 392-400. doi: 10.1016/S0006-3223(98)00370-9
60. Pasternak, T., and Greenlee, M. W. (2005). Working memory in primate sensory systems. Nat. Rev. Neurosci. 6, 97-107. doi: 10.1038/nrn1603
61. Penetar, D. M., and McDonough, J. H. Jr. (1983). Effects of cholinergic drugs on delayed match-to-sample performance of rhesus monkeys. Pharmacol. Biochem. Behav. 19, 963-967. doi: 10.1016/0091-3057(83)90399-4
62. Pessoa, L., and Ungerleider, L. G. (2004). Neural correlates of change detection and change blindness in a working memory task. Cereb. Cortex 14, 511-520. doi: 10.1093/cercor/bhh013
63. Pompeiano, M., Palacios, J. M., and Mengod, G. (1994). Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res. Mol. Brain Res. 23, 163-178. doi: 10.1016/0169-328X(94)90223-2
64. Porrino, L. J., and Goldman-Rakic, P. S. (1982). Brainstem innervation of prefrontal and anterior cingulate cortex in the rhesus monkey revealed by retrograde transport of HRP. J. Comp. Neurol. 205, 63-76. doi: 10.1002/cne.902050107
65. Puig, M. V., Artigas, F., and Celada, P. (2005). Modulation of the activity of pyramidal neurons in rat prefrontal cortex by raphe stimulation in vivo: involvement of serotonin and GABA. Cereb. Cortex 15, 1-14. doi: 10.1093/cercor/bhh104
66. Puig, M. V., Santana, N., Celada, P., Mengod, G., and Artigas, F. (2004). In vivo excitation of GABA interneurons in the medial prefrontal cortex through 5-HT3 receptors. Cereb. Cortex 14, 1365-1375. doi: 10.1093/cercor/bhh097
67. Puig, M. V., Watakabe, A., Ushimaru, M., Yamamori, T., and Kawaguchi, Y. (2010). Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT1A and 5-HT2A receptors. J. Neurosci. 30, 2211-2222. doi: 10.1523/JNEUROSCI.3335-09.2010
68. Rademaker, R. L., Tredway, C. H., and Tong, F. (2012). Introspective judgments predict the precision and likelihood of successful maintenance of visual working memory. J. Vis. 12, 21. doi: 10.1167/12.13.21
69. Robbins, T., and Roberts, A. (2007). Differential regulation of fronto-executive function by the monoamines and acetylcholine. Cereb. Cortex 17, i151-i160. doi: 10.1093/cercor/bhm066
70. Robbins, T. W., and Arnsten, A. F. T. (2009). The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu. Rev. Neurosci. 32, 267-287. doi: 10.1146/annurev.neuro.051508.135535
71. Robert, P. H., and Benoit, M. (2008). "Neurochemistry of cognition: serotonergic and adrenergic mechanisms, " in Handbook of Clinical Neurology, eds F. B. Michael and J. Aminoff (Elsevier), 31-40. Available online at: http://www.sciencedirect.com/science/article/pii/S007297520788002X
72. Rounis, E., Maniscalco, B., Rothwell, J. C., Passingham, R. E., and Lau, H. (2010). Theta-burst transcranial magnetic stimulation to the prefrontal cortex impairs metacognitive visual awareness. Cogn. Neurosci. 1, 165-175. doi: 10.1080/17588921003632529
73. Santana, N., Bortolozzi, A., Serrats, J., Mengod, G., and Artigas, F. (2004). Expression of serotonin1A and serotonin2A receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb. Cortex 14, 1100-1109. doi: 10.1093/cercor/bhh070
74. Schmitt, J. A. J., Wingen, M., Ramaekers, J. G., Evers, E. A. T., and Riedel, W. J. (2006). Serotonin and human cognitive performance. Curr. Pharm. Des. 12, 2473-2486. doi: 10.2174/138161206777698909
75. Schnyer, D. M., Verfaellie, M., Alexander, M. P., LaFleche, G., Nicholls, L., and Kaszniak, A. W. (2004). A role for right medial prefrontal cortex in accurate feeling-of-knowing judgments: evidence from patients with lesions to frontal cortex. Neuropsychologia 42, 957-966. doi: 10.1016/j.neuropsychologia.2003.11.020
76. 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
77. Silber, B. Y., and Schmitt, J. A. J. (2010). Effects of tryptophan loading on human cognition, mood, and sleep. Neurosci. Biobehav. Rev. 34, 387-407. doi: 10.1016/j.neubiorev.2009.08.005
78. Smith, E. E., and Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science 283, 1657-1661. doi: 10.1126/science.283.5408.1657
79. Van der Stigchel, S., Merten, H., Meeter, M., and Theeuwes, J. (2007). The effects of a task-irrelevant visual event on spatial working memory. Psychon. Bull. Rev. 14, 1066-1071. doi: 10.3758/BF03193092
80. Tanaka, A., and Funahashi, S. (2012). Macaque monkeys exhibit behavioral signs of metamemory in an oculomotor working memory task. Behav. Brain Res. 233, 256-270. doi: 10.1016/j.bbr.2012.05.013
81. Tegnér, J., Compte, A., and Wang, X.-J. (2002). The dynamical stability of reverberatory neural circuits. Biol. Cybern. 87, 471-481. doi: 10.1007/s00422-002-0363-9
82. Tuckwell, H. (1988). Introduction to Theoretical Neurobiology. Cambridge University Press Available online at: http://www.amazon.ca/exec/obidos/redirect?tag=citeulike09-20andpath=ASIN/0521350964
83. 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
84. Villalobos, C., Beique, J.-C., Gingrich, J. A., and Andrade, R. (2005). Serotonergic regulation of calcium-activated potassium currents in rodent prefrontal cortex. Eur. J. Neurosci. 22, 1120-1126. doi: 10.1111/j.1460-9568.2005.04307.x
85. Vollenweider, F., Vollenweider-Scherpenhuyzen, M., Bäbler, A., Vogel, H., and Hell, D. (1998). Psilocybin induces schizophrenia-like psychosis in humans via a serotonin-2 agonist action. Neuroreport 9, 3897. doi: 10.1097/00001756-199812010-00024
86. Wang, X. J. (1998). Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J. Neurophysiol. 79, 1549-1566.
87. Wang, X.-J. (1999). Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J. Neurosci. 19, 9587-9603.
88. Wei, Z., Wang, X.-J., and Wang, D.-H. (2012). From distributed resources to limited slots in multiple-item working memory: a spiking network model with normalization. J. Neurosci. 32, 11228-11240. doi: 10.1523/JNEUROSCI.0735-12.2012
89. Williams, G. V., Rao, S. G., and Goldman-Rakic, P. S. (2002). The physiological role of 5-HT2A receptors in working memory. J. Neurosci. 22, 2843-2854.
90. Wingen, M., Kuypers, K. P. C., and Ramaekers, J. G. (2007). Selective verbal and spatial memory impairment after 5-HT1A and 5-HT2A receptor blockade in healthy volunteers pre-treated with an SSRI. J. Psychopharmacol. 21, 477-485. doi: 10.1177/0269881106072506
91. Wittmann, M., Carter, O., Hasler, F., Cahn, B. R., Grimberg, U., Spring, P., et al. (2007). Effects of psilocybin on time perception and temporal control of behaviour in humans. J. Psychopharmacol. 21, 50-64. doi: 10.1177/0269881106065859
92. 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.
93. 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.
94. Zhang, Z., and Arsenault, D. (2005). Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex. J. Physiol. 566, 379-394. doi: 10.1113/jphysiol.2005.086066