Differential effects of acute serotonin and dopamine depletion on prepulse inhibition and P50 suppression measures of sensorimotor and sensory gating in humans

Neuropsychopharmacology

Volumn 33, Issue 7, 2008, Pages 1653-1666

  Mann, Collette ^a   Croft, Rodney J ^a,c   Scholes, Kirsty E ^b   Dunne, Alan ^c   O'Neill, Barry V ^c   Leung, Sumie ^c   Copolov, David ^a   Phan, K Luan ^a,d   Nathan, Pradeep J ^a,e,f,g  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f GlaxoSimthKline   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Dopamine; P50 suppression; PPI; Schizophrenia; Sensory gating; Serotonin

Indexed keywords

DOPAMINE; PHENYLALANINE; PLACEBO; SEROTONIN; TRYPTOPHAN; TYROSINE;

ADULT; AMINO ACID BLOOD LEVEL; ARTICLE; CATECHOLAMINE DEPLETION; CHANNEL GATING; CONTROLLED STUDY; ELECTROMYOGRAPHY; EVOKED AUDITORY RESPONSE; HUMAN; MALE; MONOAMINE METABOLISM; NEUROTRANSMISSION; NORMAL HUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SEROTONIN RELEASE; STARTLE REFLEX;

ACOUSTIC STIMULATION; ADULT; AFFECT; AMINO ACIDS; CROSS-OVER STUDIES; DOPAMINE; DOUBLE-BLIND METHOD; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS; FOOD, FORMULATED; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; MALE; NEURAL INHIBITION; REACTION TIME; SEROTONIN; STARTLE REACTION;

EID: 43649085353     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301556     Document Type: Article

References (105)

1. Abduljawad KA, Langley RW, Bradshaw CM, Szabadi E (1998). Effects of bromocriptine and haloperidol on prepulse inhibition of the acoustic startle response in man. J Psychopharmacol 12: 239-245.
2. Abduljawad KA, Langley RW, Bradshaw CM, Szabadi E (1999). Effects of bromocriptine and haloperidol on prepulse inhibition of the acoustic startle resposne in man. J Psychopharmacol 12: 239-245.
3. Abel KM, Allin M, van Amelsvoort T, Hemsley D, Geyer MA (2007). The indirect serotonergic agonist d-fenfluramine and prepulse inhibition in healthy men. Neuropharmacology 52: 1088-1094.
4. Adler LE, Cawthra E, Donovan KA, Harris JG, Nagamoto HT, Olincy A et al (2005). Improved P50 auditory gating with odansetron in medicated schizophrenia patients. Am J Psychiat 162: 386-388.
5. Adler LE, Freedman R, Ross RG, Olincy A, Waldo MC (1999). Elementary phenotypes in neurobiological and genetic study of schizophrenia. Biol Psychiatry 46: 8-18.
6. Adler LE, Hoffer LJ, Griffith J, Waldo MC, Freedman R (1992). Normalization by nicotine of deficient auditory sensory gating in the relatives of schizophrenics. Biol Psychiatry 32: 607-616.
7. Adler LE, Olincy A, Cawthra EM, McRae KA, Harris JG, Nagamoto HT et al (2004). Varied effects of atypical neuroleptics on P50 auditory gating in schizophrenia patients. Am J Psychiatry 161: 1822-1828.
8. Adler LE, Pachtman E, Franks RD, Pecevich M, Waldo MC (1982). Neurophysiological evidence for a defect in neuronal mechansims involved in sensory gating in schizophrenia. Biol Psychiatry 17: 639-654.
9. Adler LE, Rose GM, Freedman R (1986). Neurophysiologic studies of sensory gating in rats: effects of amphetamine, phencyclidine and haloperidol. Biol Psychiatry 21: 787-798.
10. Anokhin AP, Heath AC, Myers E, Ralano A, Wood S (2003). Genetic influences on prepulse inhibition of startle reflex in humans. Neurosci Lett 353: 45-48.
11. Arnsten AF, Goldman-Rakic PS (1998). Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for hyperdopaminergic mechanism. Arch Gen Psychiatry 55: 362-368.
12. Balaban MT, Losito BDG, Simons RF, Graham FK (1986). Off-line latency and amplitude scoring of the human reflex eye blink with Fortran IV. Psychophysiology 23: 612.
13. Becker J, Gomes I, Ghisolfi ES, Schuch A, Ramos FL, Ehlers JA et al (2004). Clozapine, but not typical antipsychotics, correct P50 suppression deficit in patients with schizophrenia. Clin Neurophysiol 115: 396-401.
14. Bitsios P, Giakoumaki SG, Frangou S (2005). The effects of dopamine agonists on prepulse inhibition in healthy men depend on baseline PPI values. Psychopharmacology 182: 144-152.
15. Bond A, Lader M (1974). The use of analog scales in rating subjective feelings. Br J Med Psychol 47: 211-218.
16. Boutros NN, Zouridakis G, Overall J (1991). Replication and extension of P50 findings in schizophrenia. Clin Electroencephalogr 22: 40-45.
17. Braff DL (1993). Information processing and attention dysfunctions in schizophrenia. Schizophr Bull 18: 233-259.
18. Braff DL, Geyer M (1990). Sensorimotor gating and schizophrenia: human and animal model studies. Arch Gen Psychiatry 47: 181-188.
19. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups and pharmacological studies. Psychopharmacology 156: 234-258.
20. Braff DL, Light GA, Swerdlow NR (2007). Prepulse inhibition and P50 suppression are both deficient but not correlated in schizophrenia patients. Biol Psychiatry 61: 1204-1207.
21. Brenner CA, Edwards CR, Carroll CA, Kieffaber PD, Hetrick WP (2004). P50 and acoustic startle gating are not related in healthy participants. Psychophysiology 41: 702-708.
22. Cadenhead KS, Braff DL (1999). Schizophrenia spectrum disorders. In: Dawson ME, Schell AM, Bohmelt AH (eds). Startle Modification: Implications for Neuroscience, Cognitive Science, and Clinical Science. Cambridge University Press: USA. pp 231-244.
23. Carpenter LL, Anderson GM, Pelton GH, Gaudin JA, Kirwin PDS, Price LH et al (1998). Tryptophan depletion during continuous CSF sampling in healthy human subjects. Neuropsychopharmacology 19: 26-35.
24. Clementz BA, Geyer MA, Braff DL (1998). Multiple site evaluation of P50 suppression among schizophrenia and normal comparison subjects. Schizophr Res 30: 71-80.
25. Cohen SA (2001). Amino acid analysis using precolumn derivatisation with 6-aminoquino lyl-N-hydroxysuccinimidyl carbamate. In: Cooper C, Packer N, Williams K (eds). Methods in Molecular Biology. Humana Press: New Jersey. pp 39-47.
26. Croft RJ, Dimoska A, Gonsalvez CJ, Clarke AR (2004). Suppression of P50 evoked potential component, schizotypal beliefs and smoking. Psychiatry Res 128: 53-62.
27. Dean B (2003). The cortical serotonin 2A receptor and the pathology of schizophrenia: a likely accomplice. J Neurochem 85: 1-13.
28. Della Casa V, Hofer I, Weiner I, Feldon J (1998). The effects of smoking on acoustic prepulse inhibition in healthy men and women. Psychopharmacology 137: 362-368.
29. Ellis KA, Mehta MA, Naga Venkatesha Murthy PJ, McTavish SF, Nathan PJ, Grasby PM (2007). Tyrosine depletion alters cortical and limbic blood flow but does not modulate spatial working memory performance or task-related blood flow in humans. Hum Brain Mapp [e-pub ahead of print].
30. Freedman R, Coon H, Myles-Worsley M, Orr-Urtreger A, Olincy A, Davis A et al (1997). Linkage of a neurophysiological deficit in schizophrenia to a chromosome 15 locus. Proc Natl Acad Sci USA 94: 587-592.
31. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR (2001). Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 156: 117-154.
32. Giakoumaki SG, Roussos P, Frangou S, Bitsios P (2007). Disruption of prepulse inhibition of the startle reflex by the preferential D(3) agonist ropinirole in healthy males. Psychopharmacology [e-pub ahead of print].
33. Gogos A, Nathan PJ, Guille V, Croft RJ, van den Buuse M (2006). Estrogen prevents 5-HT1A receptor-induced disruptions of prepulse inhibition in healthy women. Neuropsychopharmacology 31: 885-889.
34. Goldman-Rakic PS (1995). Cellular basis of working memory. Neuron 14: 477-485.
35. Gouzoulis-Mayfrank E, Heekeren K, Thelen B, Lindenblatt H, Kovar KA, Sass H et al (1998). Effects of the hallucinogen psilocybin on habituation and prepulse inhibition of the startle reflex in humans. Behav Pharmacol 9: 561-566.
36. Graham F (1975). The more or less startling effects of weak prestimulation. Psychophysiology 12: 238-248.
37. Graham SJ, Langley RW, Bradshaw CM, Szabadi E (2002). Effects of haloperidol and clozapine on prepulse inhibition of the acoustic startle response and the N1/P2 auditory evoked potential in man. J Psychopharmacol 15: 243-250.
38. Hamm A, Weike A, Schupp H (2001). The effect of neuroleptic medication on prepulse inhibition in schizophrenia patients: current status and future issues. Psychopharmacology 156: 259-265.
39. Hammer TB, Oranje B, Glenthoj BY (2007). The effects of imipramine on P50 suppression, prepulse inhibition and habituation of the startle response in humans. Int J Neuropsychopharmacol (in press).
40. Harmer C, McTavish S, Clark L, Goodwin G, Cowen P (2001). Tyrosine depletion attenuates dopamine function in healthy volunteers. Psychopharmacology 133: 329-342.
41. Harrison BJ, Olver JS, Norman TR, Burrows GD, Wesnes KA, Nathan PJ (2004). Selective effects of acute serotonin and catecholamine depletion on memory in healthy women. J Psychopharmacol 18: 32-40.
42. Hashimoto K, Iyo M, Freedman R, Stevens KE (2005). Tropisetron improves deficient inhibitory auditory processing in DBA/2 mice: role of alpha 7 nicotinic acetylcholine receptors. Psychopharmacology 183: 13-19.
43. Hoffman HS, Fleshler M (1963). Startle reaction: modification by background acoustic stimulation. Science 141: 928-930.
44. Hutchison KE, Swift R (1999). Effect of d-amphetamine on prepulse inhibition of the startle reflex in humans. Psychopharmacology 143: 394-400.
45. Ison JR, McAdam DW, Hammond GR (1973). Latency and amplitude changes in the acoutic startle reflex produced by variations in auditory prestimulation. Physiol Behav 10: 1035-1039.
46. Jaskiw GE, Bongiovanni R (2004). Brain tyrosine depletion attenuates haloperidol-induced striatal dopamine release in vivo and augments haloperidol-induced catelepsy in rats. Psychopharmacology 172: 100-107.
47. Jensen KS, Oranje B, Wienberg M, Glenthoj BY (2007). The effects of increased central serotonergic activity on prepulse inhibition and habituation of the human startle response. Neuropsychopharmacology (in press).
48. Kedzior KK, Martin-Iverson MT (2007). Attention-dependent reduction in prepulse inhibition of the startle reflex in cannabis users and schizophrenia patients - a pilot study. Eur J Pharmacology 560: 176-182.
49. Koike K, Hashimoto K, Takai N, Shimizu E, Komatsu N, Watanabe H et al (2005). Tropisetron improves deficits in auditory P50 suppression in schizophrenia. Schizophr Res 76: 67-72.
50. Kumari V, Antonova E, Geyer MA, Ffytche D, Williams SC, Sharma T (2007). A fMRI investigation of startle gating deficits in schizophrenia patients treated with typical or atypical antipsychotics. Int J Neuropsychopharmacol 10: 463-477.
51. Kumari V, Mulligan OF, Cotter PA, Poon L, Toone BK, Checkley SA et al (1998). Effects of single oral administrations of haloperidol and d-amphetamine on prepulse inhibition of the acoustic startle reflex in healthy male volunteers. Behav Pharmacol 9: 567-576.
52. Kumari V, Sharma T (2002). Effects of typical and atypical antipsychotics on prepulse inhibition in schizophrenia: a critical evaluation of current evidence and directions for future research. Psychopharmacology 162: 97-101.
53. Landis C, Hunt WA (1939). The Startle Pattern. Farrar and Rinehart: New York.
54. Laruelle M, Kegeles LS, Abi-Dargham A (2003). Glutamate, dopamine, and schizophrenia: from pathophysiology to treatment. Ann N Y Acad Sci 1003: 138-158.
55. Leyton M, Young SN, Pihl RO, Etezadi S, Lauze C, Blier P, et al (2000). Effects on mood of acute phenylalanine/tyrosine depletion in healthy women. Neuropsychopharmacology 52: 121-217.
56. Liechti ME, Geyer MA, Hell D, Vollenweider FX (2001). Effects of MDMA (ecstasy) on prepulse inhibition and habituation of startle in humans after pretreatment with citalopram, haloperidol, or ketanserin. Neuropsychopharmacology 24: 240-252.
57. Light GA, Geyer M, Clementz BA, Cadenhead K, Braff D (2000). Normal P50 suppression in schizophrenia patients treated with atypical antipsychotic medications. Am J Psychiatry 175: 767-771.
58. Light GA, Malaspina D, Geyer M, Luber BM, Coleman EA, Sackeim HA et al (1999). Amphetamine disrupts P50 suppression in normal subjects. Biol Psychiatry 49: 990-996.
59. Lu BY, Martin KE, Edgar JC, Smith AK, Lewis SF, Escamilla MA et al (2007). Effect of catechol O-methyltransferase Val(158)Met polymorphism on the P50 gating endophenotype in schizophrenia. Biol Psychiatry [e-pub ahead of print].
60. Martin-Iverson MT, Else D (2000). PHNO, a selective dopamine D2 receptor agonist, does not reduce prepulse inhibition of the startle reflex in rats. Psychopharmacology 151: 38-48.
61. Matrenza C, Hughes J, Kemp AH, Wesnes K, Harrison BJ, Nathan PJ (2004). Simultaneous depletion of serotonin and catecholamines impairs sustained attention without affecting learning and memory in humans. J Psychopharmacol 18: 21-31.
62. McGhie A, Chapman J (1961). Disorders of attention and perception in early schizophrenia. Br J Med Psychol 34: 103-116.
63. McTavish SF, Callado L, Cowen PJ, Sharp T (1999b). Comparison of the effects of α-methyl-p-tyrosine and a tyrosine-free amino acid load on extracellular noradrenaline in the rat hippocampus in vivo. J Psychopharmacol (Oxf) 13: 379-384.
64. McTavish SF, Cowen PJ, Sharp T (1999a). The effect of a tyrosine-free amino acid mixture on regional brain catecholamine synthesis and release. Psychopharmacology (Berl) 141: 182-188.
65. McTavish SF, McPerhson MH, Harmer CJ, Clark L, Sharp T, Goodwin GM et al (2001a). Antidopaminergic effects of dietary tyrosine depletion in healthy subjects and patients with manic illness. Br J Psychiatry 179: 356-360.
66. McTavish SF, Raumann B, Cowen PJ, Sharp T (2001b). Tyrosine depletion attenuates the behavioural stimulant effects of amphetamine and cocaine in rats. Eur J Pharmacol 424: 115-119.
67. Mehta MA, Gumaste D, Montgomery AJ, McTavish SF, Grasby PM (2005). The effects of acute tyrosine and phenylalanine depletion on spatial working memory and planning in healthy volunteers are predicted by changes in striatal dopamine levels. Psychopharmacology (Berlin) 26: 56-68.
68. Moja E, Stoff D, Gessa G, Castoldi D, Assereto R, Tofanetti O (1988). Decrease in plasma tryptophan after tryptophan-free amino acid mixtures in man. Life Sci 42: 1551-1556.
69. Montgomery AJ, McTavish SF, Cowen PJ, Grasby PM (2003). Reduction in brain dopamine concentration with dietary tyrosine plus phenylalanine depletion: a raclopride PET study. Am J Psychiatry 10: 1887-1889.
70. Moxon KA, Gerhardt G, Adler LE (2003a). Dopaminergic modulation of the P50 auditory-evoded potential in a computer model of the CA3 region of the hippocampus: its relationship to sensory gating in schizophrenia. Biol Cybern 88: 265-275.
71. Moxon KA, Gerhardt GA, Gulinello M, Adler LE (2003b). Inhibitory control of sensory gating in a computer model of the CA3 region of the hippocampus. Biol Cybern 88: 247-264.
72. Nagamoto HT, Adler LE, Hea RA, Griffith JM, McRae KA, Freedman R (1996). Gating of auditory P50 in schizophrenics: unique effects of clozapine. Biol Psychiatry 40: 181-188.
73. Nagamoto HT, Adler LE, McRae KA, Huettl P, Cawthra E, Gerhardt G et al (1999). Auditory P50 in schizophrenics on clozapine: improved gating parallels clinical improvement and changes in plasma 3-methoxy-4- hydroxyphenylglycol. Neuropsychobiology 39: 10-17.
74. Nagamoto HT, Adler LE, Waldo MC, Griffith J, Freedman R (1991). Gating of auditory response in schizophrenics and normal controls: effects of recording site and stimulation interval on the P50 wave. Schizophr Res 4: 31-40.
75. Nathan PJ, Hughes J, McInerney B, Harrison BJ (2004). Simultaneous depletion of tryptophan, tyrosine and phenylalanine as an experimental method to probe brain monoamine function in humans. Int J Neuropsychopharmacol 7: 171-176.
76. Nishizawa S, Benkelfat C, Young SN, Leyton M, Mzengeza S, De Montigny C et al (1997). Differences between males and females in rates of serotonin synthesis in human brain. Proc Natl Acad Sci USA 94: 5308-5313.
77. Oldendorf WH, Szabo J (1976). Amino acid assignment to one of three blood brain barrier amino acid carriers. Am J Physiol 230: 94-98.
78. Oranje B, Geyer MA, Bocker KBE, Kenemans JL, Verbaten MN (2006). Prepulse inhibition and P50 suppression: commonalities and dissociations. Psychiatry Res 143: 147-158.
79. Oranje B, Verbaten MN, Kemner C, Kahn RS (2004). Modulating sensorimotor gating in healthy volunteers: the effects of desipramine and haloperidol. Psychiatry Res 127: 195-205.
80. Palmour RM, Ervin FR, Baker GB, Young SN (1998). An amino acid mixture deficient in phenylalanine and tyrosine reduces cerebrospinal fluid catecholamine metabolites and alcohol consumption in vervet monkeys. Psychopharmacology 13: 1-7.
81. Phillips MA, Langley RW, Bradshaw CM, Szabadi E (2000b). The effects of some antidepressant drugs on prepulse inhibition of the acoustic startle (eyeblink) response and the N1/P2 auditory evoked response in man. J Psychopharmacol 14: 40-45.
82. Phillips MA, Oxtoby EK, Langley RW, Bradshaw CM, Szabadi E (2000a). Effects of acute tryptophan depletion on prepulse inhibition of the acoustic startle (eyeblink) response and the N1/P2 auditory evoked response in man. J Psychopharmacol 14: 258-265.
83. Prinssen EPM, Assie M, Wouter K, Kleven MS (2002). Depletion of 5-HT disrupts prepulse inhibition in rats: dependence on the magnitude of depletion, and reversal by a 5-HT precursor. Neuropsychopharmacology 26: 340-347.
84. Prosser CL, Hunter WS (1936). The extinction of startle responses and spinal reflexes in the white rat. Am J Physiol 117: 609-618.
85. Reilly JG, McTavish SF, Young AH (1997). Rapid depletion of plasma tryptophan: a review of studies and experimental methodology. J Psychopharmacol 11: 381-392.
86. Riba J, Rodriguez-Fornells A, Barbanoj MJ (2002). Effects of ayahuasca on sensory and sensorimotor gating in himans as measured by P50 suppression and prepulse inhibition of the startle reflex, respectively. Psychopharmacology 165: 18-28.
87. Sambeth A, Blokland A, Harmer CJ, Kilkens TO, Nathan PJ, Porter RJ et al (2007). Sex differences in the effect of acute tryptophan depletion on declarative episodic memory: a pooled analysis of nine studies. Neurosci Biobehav Rev 31: 516-529.
88. Schmitt JA, Jorissen B, Sobezak S, van Boxtel MPJ, Hogervorst E, Deutz NEP et al (2000). Tryptophan depletion impairs memory consolidation but improves focused attention in healthy young volunteers. J Psychopharmacol 14: 21-29.
89. Sobczak S, Riedel WJ, Booij I, Hen Rot MA, Deutz NEP, Honig A (2002). Cognition following acute tryptophan depletion: difference between first degree-degree relatives of bipolar disorder patients and matched healthy control volunteers. Psychol Med 32: 503-515.
90. Swerdlow NR, Auerbach P, Monroe SM, Hartston H, Geyer MA, Braff DL (1993). Men are more inhibited than women by weak prepulses. Biol Psychiatry 34: 253-260.
91. Swerdlow NR, Braff D, Geyer M (2000). Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11: 185-204.
92. Swerdlow NR, Eastvold A, Karban B, Ploum Y, Stephany N, Geyer MA et al (2002a). Dopamine agonist effects on startle and sensorimotor gating in normal male subjects: time course studies. Psychopharmacology 161: 189-201.
93. Swerdlow NR, Geyer MA, Shoemaker JM, Light GA, Braff DL, Stevens KE et al (2006). Convergence and divergence in the neurochemical regulation of prepulse inhibition of startle and N40 suppression in rats. Neuropsychopharmacology 31: 506-515.
94. Swerdlow NR, Hartman PL, Auerbach PP (1997). Changes in sensorimotor inhibition across the menstrual cycle: implications for neuropsychiatric disorders. Biol Psychiatry 41: 452-460.
95. Swerdlow NR, Platten A, Shoemaker J, Pitcher L, Auerbach PP (2001). Effects of pergolide on sensorimotor gating of the startle reflex in rats. Psychopharmacology 158: 230-240.
96. Swerdlow NR, Stephany N, Shoemaker JM, Ross L, Wasserman LC, Talledo J et al (2002b). Effects of amantadine and bromocriptine on startle and sensorimotor gating: parametric studies and cross-species comparisons. Psychopharmacology 164: 82-92.
97. Swerdlow NR, Shoemaker JM, Pitcher L, Platten A, Kuczenski R, Eleey CC et al (2002c). Genetic differences in startle gating-disruptive effects of apomorphine: evidence for central mediation. Behav Neurosci 116: 682-690.
98. Vollenweider FX, Csomor PA, Knappe B, Geyer MA, Quednow BB (2007). The effects of the preferential 5-HT2A agonist psilocybin on prepulse inhibition of startle in healthy human volunteers depend on interstimulus interval. Neuropsychopharmacology 32:1876-1887.
99. Vollenweider FX, Remensberger S, Hell D, Geyer MA (1999). Opposite effects of 3,4-methylenedioxymethamphetamine (MDMA) on sensorimotor gating in rats versus healthy humans. Psychopharmacology 143: 365-372.
100. Ward PB, HOffer LD, Liebert BJ, Catts SV, O'Donnell M, Adler LE (1996). Replication of a P50 auditory gating deficit in Australian patients with schizophrenia. Psychiatry Res 64: 121-135.
101. Weike AI, Bauer U, Hamm AO (2000). Effective neuroleptic medication removes prepulse inhibition deficits in schizophrenia patients. Biol Psychiatry 47: 61-70.
102. Williams GV, Goldman-Rakic PS (1995). Blockade of dopamine D1 receptors enhances memory fields of prefrontal neurons in primate cerebral cortex. Nature 376: 572-575.
103. Williams WA, Shoaf SE, Hommer D, Rawlings R, Linnoila M (1999). Effects of acute Tryptophan depletion on plasma and cerebrospinal fluid tryptophan and 5-hydroxyindoleacetic acid in normal volunteers. J Neurochem 72: 1641-1647.
104. Yee CM, White PM (2001). Experimental modification of P50 suppression. Psychophysiology 38: 531-539.
105. Young SN, Smith SE, Phil RO, Ervin FR (1985). Tryptophan depletion causes rapid lowering of mood in normal males. Psychopharmacology 87: 173-177.