Acute administration of nutritionally sourced tryptophan increases fear recognition
Abstract
Rationale The serotonin precursor tryptophan (TRP) has been widely used as a nutritional supplement and antidepressant. Recently, however, the use of TRP has been severely restricted due to its association with the eosinophilic myalgic syndrome, an autoimmune disorder probably caused by ingestion of a contaminant produced in certain TRP manufacturing processes. Objectives To determine the bioavailability of a nutritional source of TRP obtained from milk protein and to assess whether administration of this material produced neuroendocrine and neuropsychological effects consistent with increased brain serotonin activity. Methods We studied 24 healthy subjects who ingested approximately 1.8 g of nutritionally-sourced TRP or placebo in a double-blind, parallel group, design. We carried out venous sampling for amino acid and hormone estimation and performed a test of emotional processing using a facial expression recognition task. Results The nutritionally-sourced TRP caused a substantial increase in the availability of TRP in plasma. Relative to placebo the TRP material produced some evidence of an increase in plasma cortisol, and enhanced the perception of fearful and happy facial expressions. Conclusions A nutritional source of TRP increased the availability of TRP for brain serotonin synthesis and produced endocrine and neuropsychological changes consistent with increased brain serotonin function. The effect of TRP on emotional processing may be relevant to its reported activi…
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Acutely increasing 5-HT function with a single dose of tryptophan or citalopram increased fear recognition in 4 of 5 studies of healthy volunteers.
“Increasing 5-HT function acutely in 5 studies of healthy volunteers from the same group in Oxford, using a single dose of tryptophan or citalopram, increased fear recognition in 4 studies (Attenburrow et al., 2003;Bhagwagar et al., 2004;Browning et al., 2007;Harmer et al., 2003a) but not in the fifth (Murphy et al., 2009a).”
From Affective Cognition and its Disruption in Mood Disorders (2011) · cites this paper as Attenburrow et al., 2003
In 3 of those studies, there was also an increase in recognition of happiness.
“In 3 of the studies there was also an increase in recognition of happiness (Attenburrow et al., 2003;Harmer et al., 2003a;Murphy et al., 2009a).”
From Affective Cognition and its Disruption in Mood Disorders (2011) · cites this paper as Attenburrow et al., 2003
Cites
Ekman, P. (1976) · Medical Entomology and Zoology · Cited by 4,345 · see citing works
Facial expression megamix: Tests of dimensional and category accounts of emotion recognition
Young, A. W., Rowland, D., Calder, A. J., Etcoff, N. L., Seth, A. K., & Perrett, D. I. (1997) · Cognition · doi:10.1016/s0010-0277(97)00003-6 · Cited by 539 · see citing works
Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys
Raleigh, M. J., McGuire, M. T., Brammer, G. L., Pollack, D. B., & Yuwiler, A. (1991) · Brain Research · doi:10.1016/0006-8993(91)90001-c · Cited by 447 · see citing works
Acute SSRI Administration Affects the Processing of Social Cues in Healthy Volunteers
Harmer, C. J., Bhagwagar, Z., Perrett, D. I., Völlm, B. A., Cowen, P. J., & Goodwin, G. M. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300004 · Cited by 420 · cited 3× · see citing works
“In addition, based on a recent study with acute SSRI treatment, we predicted that acute TRP ingestion would increase the detection of fearful and happy facial expressions (Harmer et al. 2003a).”
BackgroundSelf-citationBiochemistry of tryptophan in health and disease
Bender, D. A. (1983) · Molecular Aspects of Medicine · doi:10.1016/0098-2997(83)90005-5 · Cited by 355 · see citing works
Fürst, P., Pollack, L., Graser, T. A., Godel, H. G., & Stehle, P. (1990) · Journal of Chromatography A · doi:10.1016/s0021-9673(00)97000-6 · Cited by 268 · see citing works
Effects of drugs on the processes regulating the functional activity of brain 5-hydroxytryptamine
Green, A. R., & Grahame‐Smith, D. G. (1976) · Nature · doi:10.1038/260487a0 · Cited by 184 · see citing works
Neuroendocrine probes of serotonergic function: A critical review
Yatham, L. N., & Steiner, M. S. (1993) · Life Sciences · doi:10.1016/0024-3205(93)90696-z · Cited by 164 · see citing works
The Effect of Tryptophan on Social Interaction in Everyday Life A Placebo-Controlled Study
Moskowitz, D. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00219-6 · Cited by 163 · see citing works
Tryptophan depletion decreases the recognition of fear in female volunteers
Harmer, C. J., Rogers, R. D., Tunbridge, E. M., Cowen, P. J., & Goodwin, G. M. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1401-6 · Cited by 162 · see citing works
Self-citationRaleigh, M. J., & McGuire, M. T. (1989) · Animal Behaviour · doi:10.1016/s0003-3472(89)80065-x · Cited by 104 · see citing works
The clinical psychopharmacology of tryptophan
Young, S. N. (1986) · Cited by 93 · see citing works
Serotonin receptor subtypes in depression: evidence from studies in neuroendocrine regulation.
Cowen, P. J. (1993) · PubMed · Cited by 87 · see citing works
Self-citationCowen, P. J., GADHVI, H., Gosden, B., & Kolakowska, T. (1985) · Psychopharmacology · doi:10.1007/bf00431703 · Cited by 74 · see citing works
Self-citationSharp, T., Bramwell, S., & Smith, A. D. (1992) · Life Sciences · doi:10.1016/0024-3205(92)90321-f · Cited by 71 · see citing works
Lehnert, H., & Wurtma, R. J. (2010) · Psychotherapy and Psychosomatics · doi:10.1159/000288676 · Cited by 58 · see citing works
Tryptophan produced by Showa Denko and epidemic eosinophilia-myalgia syndrome.
Kilbourne, E. M., Philen, R. M., Kamb, M. L., & Falk, H. (1996) · PubMed · Cited by 48 · see citing works
Depression and Serotonin Metabolism
Byerley, W., & Risch, S. C. (1985) · Journal of Clinical Psychopharmacology · doi:10.1097/00004714-198508000-00002 · Cited by 32 · see citing works
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Cited by
Sorted by citations
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Affective Cognition and its Disruption in Mood Disorders
Elliott, R., Zahn, R., Deakin, J. F. W., & Anderson, I. M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.77 · Cited by 330 · see citing works
“In 3 of the studies there was also an increase in recognition of happiness (Attenburrow et al., 2003; Harmer et al., 2003a; Murphy et al., 2009a).”
BackgroundMinzenberg, M., Fan, J., New, A. S., Tang, C. Y., & Siever, L. J. (2007) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.03.006 · Cited by 314 · see citing works
“Doubleblind, placebo-controlled studies indicate that serotonergic agents can modulate healthy adults' ability to recognize facial expressions of fear (Harmer et al., 2003, 2004; Attenburrow et al., 2003).”
BackgroundEffect of a single dose of citalopram on amygdala response to emotional faces
Murphy, S. E., Norbury, R., O'Sullivan, U., Cowen, P. J., & Harmer, C. J. (2009) · British Journal of Psychiatry · doi:10.1192/bjp.bp.108.056093 · Cited by 255 · see citing works
“…expected increase in the recognition of happy facial expressions on the behavioural facial expression recognition task but, unlike participants in a number of previous studies of acute serotonergic manipulation, 4,5,36 they did not show an increase in the recognition of fearful facial expressions.”
Self-citationDel-Ben, C. M., Deakin, J. F. W., Mckie, S., Delvai, N. A., Williams, S. R., Elliott, R., Dolan, M., & Anderson, I. M. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300728 · Cited by 260 · see citing works
“Acute modulation of 5-HT function alters facial expression recognition in healthy volunteers (Harmer et al, 2003a, b; Attenburrow et al, 2003), but as yet it is unclear as which to neural substrates mediate this effect.”
BackgroundInfluentialEffects of tryptophan loading on human cognition, mood, and sleep
Silber, B. Y., & Schmitt, J. A. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.005 · Cited by 260 · see citing works
“…levels can increase 5-HT synthesis as much as twofold following 3 g pure Trp load (Young, 1996; Young and Gauthier, 1981), which is significant to modulate mood, cognition and behaviour (Attenburrow et al., 2003; Cunliffe et al., 1998; Marsh et al., 2002; Markus et al., 2008; Yuwiler et al., 1981).”
BackgroundMethodInfluentialBurghardt, N. S., Sullivan, G. M., McEwen, B. S., Gorman, J. M., & LeDoux, J. E. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.02.029 · Cited by 246 · see citing works
A single dose of citalopram increases fear recognition in healthy subjects
Browning, M., Reid, C., Cowen, P. J., Goodwin, G. M., & Harmer, C. J. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881106074062 · Cited by 245 · see citing works
Self-citationTranter, R., Bell, D., Gutting, P., Harmer, C., Healy, D., & Anderson, I. M. (2009) · Journal of Affective Disorders · doi:10.1016/j.jad.2009.01.028 · Cited by 184 · see citing works
Self-citationSocial-emotion recognition in borderline personality disorder
Minzenberg, M., Poole, J. H., & Vinogradov, S. (2006) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2006.03.005 · Cited by 170 · see citing works
“Harmer et al have found that recognition of fearful facial expressions by healthy adults is enhanced with administration of either tryptophan [47] or selective serotonin reuptake inhibitors [48] and decreased with tryptophan depletion [49].”
BackgroundCools, R., Calder, A. J., Lawrence, A. D., Clark, L., Bullmore, E., & Robbins, T. W. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2215-5 · Cited by 161 · see citing works
“Whilst concurring with the present amygdala activation profile, this pattern appears inconsistent with findings from Harmer et al. (2003b) and Attenburrow et al. (2003) who observed, respectively, that acute tryptophan depletion reduced and acute tryptophan loading enhanced fearperceptioninafacialexpressionrecognition…”
ResultCrişan, L. G., Pană, S. E., Vulturar, R., Heilman, R. M., Szekely‐Copîndean, R. D., Drugă, B., Dragoş, N., & Miu, A. C. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp019 · Cited by 164 · see citing works
“In humans, the acute administration of selective 5-HT reuptake inhibitors (SSRIs) or 5-HT precursor tryptophan, both resulting in increased 5-HT availability in the brain, enhance the recognition of fearful faces (Attenburrow et al., 2003; Browning et al., 2007).”
BackgroundA model of differential amygdala activation in psychopathy
Moul, C., Killcross, S., & Dadds, M. R. (2012) · Psychological Review · doi:10.1037/a0029342 · Cited by 159 · see citing works
Passamonti, L., Crockett, M. J., Apergis-Schoute, A. M., Clark, L., Rowe, J. B., Calder, A. J., & Robbins, T. W. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.033 · Cited by 137 · see citing works
Efficacy markers in depression
Harmer, C. J., Cowen, P. J., & Goodwin, G. M. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881110367722 · Cited by 122 · see citing works
Self-citationRoiser, J. P., Rogers, R. D., Cook, L. J., & Sahakian, B. J. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0495-z · Cited by 115 · see citing works
“Consistent with this hypothesis, it was previously reported that acute tryptophan depletion reduces and tryptophan loading increases fear perception in a facial expression recognition task (Attenburrow et al. 2003; Harmer et al. 2003), and that acute tryptophan depletion results in impaired quality of decision-making…”
BackgroundThe effects of serotonin manipulations on emotional information processing and mood
Merens, W., van der Does, W. A. J., & Spinhoven, P. (2007) · Journal of Affective Disorders · doi:10.1016/j.jad.2007.01.032 · Cited by 108 · see citing works
“Attenburrow et al. (2003) investigated the effects of an 80% tryptophan powder derived from milk whey (approximately 1.8 g tryptophan) on facial expression recognition in healthy females.”
BackgroundResultInfluentialLechín, F., van der Dijs, B., & Hernández-Adrián, G. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.11.025 · Cited by 101 · see citing works
“Summarizing, many experimental findings show that 5-HT1A and 5-HT-1B/D agonists inhibit DR and MR serotonergic activities, respectively, when these drugs are systemically administered (Andrade et al., 2004; Attenburrow et al., 2003; Evrard et al., 1999; Lin and Parsons, 2002; Martinez-Price and Geyer, 2002; Newman et…”
BackgroundTryptophan supplementation and serotonin function: genetic variations in behavioural effects
Gibson, E. L. (2018) · Proceedings of The Nutrition Society · doi:10.1017/s0029665117004451 · Cited by 99 · see citing works
The effect of raising and lowering tryptophan levels on human mood and social behaviour
Young, S. N. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0375 · Cited by 100 · see citing works
“Raising tryptophan with alpha-lactalbumin, a protein with high tryptophan levels, enhanced the recognition of both fearful and happy faces in healthy participants [74].”
BackgroundMoul, C., Dobson‐Stone, C., Brennan, J., Hawes, D. J., & Dadds, M. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056619 · Cited by 98 · see citing works
“[14] respectively found that acute administration of a serotonin selective reuptake inhibitor (SSRI) and ingestion of tryptophan (the natural precursor of serotonin) improved recognition of both fear and happiness.”
BackgroundKemp, A. H., Gray, M. A., Silberstein, R. B., Armstrong, S. M., & Nathan, P. J. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.03.022 · Cited by 98 · see citing works
“This finding was replicated in a subsequent study by the same authors after administration of tryptophan (Attenburrow et al., 2003).”
Effects of increasing tryptophan intake on growth and physiological changes in nursery pigs1
Shen, Y. B., Voilqué, G., Kim, J. D., Odle, J., & Kim, S. W. (2012) · Journal of Animal Science · doi:10.2527/jas.2011-4203 · Cited by 97 · see citing works
“Thus, increasing Trp intake has been tested as a nutritional strategy to control stress in humans (Markus et al., 1998; Attenburrow et al., 2003).”
BackgroundOmega-3 fatty acids (fish-oil) and depression-related cognition in healthy volunteers
Antypa, N., van der Does, W. A. J., Smelt, A., & Rogers, R. (2008) · Journal of Psychopharmacology · doi:10.1177/0269881108092120 · Cited by 92 · see citing works
Toward a Neurogenetic Theory of Neuroticism
Canli, T. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1417.022 · Cited by 93 · see citing works
Murphy, S. E., Longhitano, C., Ayres, R. E., Cowen, P. J., & Harmer, C. J. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0401-8 · Cited by 81 · see citing works
“8 g) is sufficient to induce neuropsychological changes in the detection of facial expressions of emotion (Attenburrow et al. 2003) similar to those seen with acute citalopram administration (Harmer et al.”
ResultInfluentialSelf-citationMohajeri, M. H., Wittwer, J., Vargas, K., Hogan, E., Holmes, A., Rogers, P. J., Goralczyk, R., & Gibson, E. L. (2015) · British Journal of Nutrition · doi:10.1017/s0007114514003754 · Cited by 81 · see citing works
“In addition, a-lactalbumin improves the memory of recovered depressives and healthy subjects((6)), and increases the recognition of emotional faces in healthy young women((18)).”
BackgroundA systematic review of the effect of L-tryptophan supplementation on mood and emotional functioning
Kikuchi, A. M., Tanabe, A., & Iwahori, Y. (2020) · Journal of Dietary Supplements · doi:10.1080/19390211.2020.1746725 · Cited by 80 · see citing works
“In a study published in 2003 (Attenburrow et al. 2003), women took 1.8 g IHDB )C(noitingocer noisserpxe laicaF )a( Ta bl e 3.”
BackgroundInfluentialShen, Y. B., Voilqué, G., Odle, J., & Kim, S. W. (2012) · Journal of Nutrition · doi:10.3945/jn.112.163824 · Cited by 73 · see citing works
Forssman, L., Peltola, M. J., Yrttiaho, S., Puura, K., Mononen, N., Lehtimäki, T. J., & Leppänen, J. M. (2013) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12181 · Cited by 71 · see citing works
“Indeed, a randomized controlled study in human adults has shown that increased tryptophan and serotonergic function heightens perceptual sensitivity to fearful facial expressions (Attenburrow et al., 2003).”
BackgroundBooij, L., Merens, W., Markus, C. R., & van der Does, W. A. J. (2006) · Journal of Psychopharmacology · doi:10.1177/0269881105057466 · Cited by 68 · see citing works
Mapping the developmental pathways of child conduct problems through the neurobiology of empathy
Moul, C., Hawes, D. J., & Dadds, M. R. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.016 · Cited by 65 · see citing works
Impaired fear recognition in regular recreational cocaine users
Kemmis, L., Hall, J. K., Kingston, R. A., & Morgan, M. J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0829-5 · Cited by 66 · see citing works
“2003a), and tryptophan supplementation (Attenburrow et al. 2003), and impaired following tryptophan depletion (Harmer et al.”
Murphy, S. E., Longhitano, C., Ayres, R. E., Cowen, P. J., Harmer, C. J., & Rogers, R. D. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21122 · Cited by 60 · see citing works
“in healthy volunteers (Attenburrow et al., 2003; Harmer et al., 2003), and in clinical populations (Kent, Coplan, & Gorman, 1998).”
BackgroundSelf-citationBauman, M. D., & Amaral, D. G. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.040 · Cited by 59 · see citing works
Merens, W., Booij, L., Markus, R., Zitman, F. G., Onkenhout, W., & van der Does, W. A. J. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20051492 · Cited by 59 · see citing works
Labuschagne, I., Jones, R., Callaghan, J., Whitehead, D. L., Dumas, E. M., Say, M. J., Hart, E. P., Justo, D., Coleman, A., Santos, R. C. D., et al. (2012) · Psychiatry Research · doi:10.1016/j.psychres.2012.09.022 · Cited by 57 · see citing works
5HT3 antagonism abolishes the emotion potentiated startle effect in humans
Harmer, C. J., Reid, C. B., Ray, M. K., Goodwin, G. M., & Cowen, P. J. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0337-z · Cited by 57 · see citing works
“Acute administration of agents increasing serotonin function such as the SSRI citalopram (Harmer et al. 2003) or serotonin precursor tryptophan (Attenburrow et al. 2003) increased fearful facial expression recognition in healthy volunteers.”
BackgroundResultSelf-citationMarsh, A. A., Finger, E. C., Buzas, B., Soliman, N., Richell, R. A., Vythilingham, M., Pine, D. S., Goldman, D., & Blair, R. J. R. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0581-2 · Cited by 52 · see citing works
“Our findings are consistent with the findings of other studies that have found no effect of gender on facial expression recognition after serotonergic manipulation (Roiser et al. 2006; Attenburrow et al. 2003; Harmer et al. 2003a,b).”
BackgroundResultFacial expression perception: an objective outcome measure for treatment studies in mood disorders?
Venn, H., Watson, S., Gallagher, P., & Young, A. H. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705006012 · Cited by 51 · see citing works
“Further support for an effect of the 5-HT systems on perception of fear comes from the study by Attenburrow et al. (2003) which found increased fear recognition following acute administration of nutritionally sourced tryptophan (Trp), a precursor to 5- HT, as well as a trend for increased…”
BackgroundTryptophan supplementation modulates social behavior: A review
Steenbergen, L., Jongkees, B. J., Sellaro, R., & Colzato, L. S. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.02.022 · Cited by 50 · see citing works
Food-derived serotonergic modulators: effects on mood and cognition
Hulsken, S., Märtin, A., Mohajeri, M. H., & Homberg, J. R. (2013) · Nutrition Research Reviews · doi:10.1017/s0954422413000164 · Cited by 50 · see citing works
“An oral dose of 1·8 g Trp (600 % increase in TRP:LNAA) increased the recognition of fearful and happy faces in females((95)).”
BackgroundMerens, W., Booij, L., Haffmans, P. J., & van der Does, A. (2008) · Journal of Psychopharmacology · doi:10.1177/0269881107081531 · Cited by 49 · see citing works
Gibson, E. L., Vargas, K., Hogan, E., Holmes, A., Rogers, P. J., Wittwer, J., Kloek, J., Góralczyk, R., & Mohajeri, M. H. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3609-z · Cited by 46 · see citing works
“However, the results have not been entirely consistent; one oral dose of 1.8 g TRP enhanced recognition of both happy and fearful faces (Attenburrow et al. 2003), whereas 3 g/day TRP for 14 days increased recognition of happiness but decreased recognition of disgust expressions, and reduced…”
BackgroundResultInfluentialThe Role of the Amygdala in Anxiety Disorders
Gina, L., Andrew, M., Jamie, L. A., & Michael, J. (2012) · InTech eBooks · doi:10.5772/50323 · Cited by 45 · see citing works
“However, it has been emphasized that the effects of serotonergic challenge on fear recognition and amygdala activation appear to be dependent upon the individual’s baseline sensitivity to threat [212], gender [213] and genotype [214].”
BackgroundPositive and negative affect differentially influence identification of facial emotions
Coupland, N. J., Sustrik, R. A., Ting, P. T., Li, D., Hartfeil, M. A. W., Singh, A. J., & Blair, J. (2004) · Depression and Anxiety · doi:10.1002/da.10136 · Cited by 45 · see citing works
“Recent studies have reported that acute modulation of serotonin function altered the recognition of both happy and fearful faces without affecting the recognition of other emotions [Attenburrow et al., 2003; Harmer et al., 2003a, 2003b].”
BackgroundGood‐quality diet in the early years may have a positive effect on academic achievement
Nyaradi, A., Li, J., Foster, J. K., Hickling, S., Jacques, A., O’Sullivan, T. A., & Oddy, W. H. (2015) · Acta Paediatrica · doi:10.1111/apa.13324 · Cited by 44 · see citing works
“Tryptophan is a precursor to serotonin, which is a neurotransmitter involved in important behavioural and psychological processes (25).”
BackgroundMartin, L., Clair, J., Davis, P. W., O’Ryan, D., Hoshi, R., & Curran, H. V. (2006) · Addiction · doi:10.1111/j.1360-0443.2006.01574.x · Cited by 43 · see citing works
Kerestes, R., Labuschagne, I., Croft, R. J., O’Neill, B. V., Bhagwagar, Z., Phan, K. L., & Nathan, P. J. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1340-3 · Cited by 41 · see citing works
“As both neuroimaging (Del-Ben et al. 2005; Harmer et al. 2006) and behavioural ( Attenburrow et al. 2003 ) studies have shown that prototypical (i.e.”
BackgroundSambeth, A., Riedel, W. J., Tillie, D. E., Blokland, A., Postma, A., & Schmitt, J. A. J. (2008) · Journal of Psychopharmacology · doi:10.1177/0269881108089577 · Cited by 39 · see citing works
Hoshi, R., Bisla, J., & Curran, H. V. (2004) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2004.06.006 · Cited by 38 · see citing works
Blair, K. S., Finger, E. C., Marsh, A. A., Morton, J., Mondillo, K., Buzás, B., Goldman, D. A., Drevets, W. C., & Blair, J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0920-y · Cited by 37 · see citing works
“2003b) while acute administration of tryptophan, by contrast, increases subjects’ ability to recognize fear expressions (Attenburrow et al. 2003).”
BackgroundStudying the neurobiology of human social interaction: Making the case for ecological validity
Hogenelst, K., Schoevers, R. A., & Rot, M. A. H. (2015) · Social Neuroscience · doi:10.1080/17470919.2014.994786 · Cited by 36 · see citing works
“These tasks required participants to indicate the type of emotion expressed in faces briefly presented on a computer screen (Attenburrow et al., 2003; Harmer, Rogers, et al., 2003; Kerestes et al., 2009).”
BackgroundLabuschagne, I., Croft, R. J., Phan, K., & Nathan, P. J. (2008) · Journal of Psychopharmacology · doi:10.1177/0269881108097878 · Cited by 34 · see citing works
Effects of α-lactalbumin on emotional processing in healthy women
Scrutton, H., Carbonnier, A., Cowen, P. J., & Harmer, C. J. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881106075271 · Cited by 34 · see citing works
Self-citationMorandini, L., Ramallo, M. R., Moreira, R. G., Höcht, C., Somoza, G. M., da Silva, A. C. R., & Pandolfi, M. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.10.005 · Cited by 31 · see citing works
Differential effects of tryptophan depletion on emotion processing according to face direction
Williams, J. H. G., Perrett, D. I., Waiter, G. D., & Pechey, S. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm021 · Cited by 30 · see citing works
“Acute administration of tryptophan (the dietary precursor of serotonin) is associated with improved emotion recognition (Attenburrow et al., 2003), whilst acute tryptophan depletion (ATD) is associated with increased errors (Harmer et al., 2003).”
BackgroundHensler, J. G. (2010) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(10)70090-4 · Cited by 30 · see citing works
Daly, E., Deeley, Q., Hallahan, B. P., Craig, M., Brammer, M. J., Lamar, M., Cleare, A. J., Giampietro, V., Ecker, C., Page, L., et al. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1850-7 · Cited by 26 · see citing works
“For example, human studies have shown that manipulation of brain 5-HT levels is associated with effects on recognition of emotional facial expressions (Attenburrow et al. 2003; Browning et al. 2007; Harmer et al. 2003a; Murphy et al. 2006).”
BackgroundSerotonergic modulation of face-emotion recognition
Del‐Ben, C. M., Ferreira, C. A., Alves-Neto, W. C., & Graeff, F. G. (2008) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2008000400002 · Cited by 24 · see citing works
“Of these, ten (15-24) evaluated the effects of acute manipulation of the 5-HT system.”
BackgroundInfluentialBeacher, F. D. C. C., Gray, M. A., Minati, L., Whale, R., Harrison, N. A., & Critchley, H. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1897-5 · Cited by 22 · see citing works
Crespi, F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.05.021 · Cited by 21 · see citing works
Blunted emotion‐modulated startle reflex in anorexia nervosa
Brockmeyer, T., Pellegrino, J., Maier, C., Münch, H. M., Harmer, C. J., Walther, S., Herzog, W., & Friederich, H. (2019) · International Journal of Eating Disorders · doi:10.1002/eat.23022 · Cited by 21 · see citing works
Self-citationdas Neves, M. D. C. L., Trémeau, F., Nicolato, R., Lauar, H., Romano‐Silva, M. A., & Corrêa, H. (2011) · Brazilian Journal of Psychiatry · doi:10.1590/s1516-44462011000300009 · Cited by 20 · see citing works
“Harmer described that 10 micrograms of citalopram improved the recognition of fear, and that the acute depletion of tryptophan worsened the recognition of fear,(38) while dietary tryptophan supplementation seems to improve facial emotion recognition.(39) Battaglia showed that children who have one or two copies of the…”
BackgroundSerra, M., Salgado‐Pineda, P., Delaveau, P., Fakra, É., Gastó, C., & Blin, O. J. (2006) · Clinical Neuropharmacology · doi:10.1097/01.wnf.0000214799.25044.ea · Cited by 18 · see citing works
“This finding was replicated after administration of tryptophan.(75) Effects of Antidepressant Drugs on Emotion CLINICAL NEUROPHARMACOLOGY”
BackgroundSerotonergic Contribution to Boys' Behavioral Regulation
Nantel‐Vivier, A., Pihl, R. O., Young, S. N., Parent, S., Bélanger, S. A., Sutton, R. S., Dubois, M.-E., Tremblay, R. E., & Séguin, J. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020304 · Cited by 18 · see citing works
“Human studies replicated these findings [14,20,29,30], and additionally found positive associations between serotonin and emotion recognition [31–34].”
ResultDu, Y., Wu, B., Xiao, F., Yan, T., Li, Q., Jia, Y., Bi, K., & He, B. (2020) · Journal of Separation Science · doi:10.1002/jssc.201901002 · Cited by 17 · see citing works
das Neves, M. D. C. L., Trémeau, F., Nicolato, R., Lauar, H., Romano‐Silva, M. A., & Corrêa, H. (2011) · Brazilian Journal of Psychiatry · doi:10.1590/s1516-44462011005000018 · Cited by 14 · see citing works
Lee, R., Gill, A. D., Chen, B., McCloskey, M. S., & Coccaro, E. F. (2012) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e31825368b7 · Cited by 14 · see citing works
Tryptophan for the sleeping disorder and mental symptom of new-type drug dependence
Wang, D., Li, W., Xiao, Y., He, W., Wei, W., Yang, L., Yu, J., Song, F., & Wang, Z. (2016) · Medicine · doi:10.1097/md.0000000000004135 · Cited by 12 · see citing works
“The authors have no conflicts of interest to disclose. a Department of Epidemiology and Biostatistics, School of Public Health, Tongji Medic the Prevention and Treatment of Occupational Diseases, c Department of Social Medic Huazhong University of Science and Technology, dCompulsory Residential…”
BackgroundInfluentialGiorgi, R. D., Martens, M., Pesci, N. R., Cowen, P. J., & Harmer, C. J. (2021) · Journal of Psychopharmacology · doi:10.1177/02698811211060307 · Cited by 13 · see citing works
“A similar effect has been seen with acute administration of serotonin precursor, tryptophan (Attenburrow et al., 2003).”
BackgroundSelf-citationMicrodosing psychedelics as cognitive and emotional enhancers.
Rifkin, B. D., Maraver, M. J., & Colzato, L. S. (2020) · Psychology of Consciousness Theory Research and Practice · doi:10.1037/cns0000213 · Cited by 12 · see citing works
The Genetics of Risk Aversion: A Systematic Review
Molins, F., Sahin, F., & Serrano, M. Á. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph192114307 · Cited by 11 · see citing works
“Some previous examples, but not including the genetic part, also suggest this: it seems that the elevated levels of serotonin after the administration of its precursor (tryptophan) or inhibitors of its transporters, facilitate the recognition of threatening faces in humans [72,73], and the acquisition of a conditioned…”
BackgroundRecognizing emotions in faces: effects of acute tryptophan depletion and bright light
Rot, M. A. H., Coupland, N. J., Boivin, D. B., Benkelfat, C., & Young, S. N. (2009) · Journal of Psychopharmacology · doi:10.1177/0269881109348169 · Cited by 11 · see citing works
“Acute increases in brain serotonin function, achieved by means of single-dose administration of the amino acid precursor of serotonin, tryptophan, or the selective serotonin reuptake inhibitor, citalopram, have generally been found to improve the correct recognition of fearful expressions in healthy individuals withou…”
BackgroundReduced emotion recognition from nonverbal cues in anorexia nervosa
Blomberg, M., Schlegel, K., Stoll, L., Febry, H., Wünsch‐Leiteritz, W., Leiteritz, A., & Brockmeyer, T. (2021) · European Eating Disorders Review · doi:10.1002/erv.2860 · Cited by 10 · see citing works
Anti-obesity Drugs: From Animal Models to Clinical Efficacy
Dourish, C. T., Wilding, J. P. H., & Halford, J. C. G. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-373861-5.00028-x · Cited by 10 · see citing works
Mirzai, N., Polet, K., Morisot, A., Hesse, S., Pesce, A., Louchart, S., & Iakimova, G. (2023) · Cognitive and Behavioral Neurology · doi:10.1097/wnn.0000000000000348 · Cited by 9 · see citing works
“Williams et al (2003) also found that individuals with schizophrenia with atypical neuroleptic treatment allocated as much attention to salient features of the face (eyes, nose, and mouth) as controls, whereas typical neuroleptic treatment led to fewer observations of these features.”
BackgroundResultThe role of TPH2 variant rs4570625 in shaping infant attention to social signals
Kataja, E., Leppänen, J. M., Kantojärvi, K., Pelto, J., Häikiö, T., Korja, R., Nolvi, S., Karlsson, H., Paunio, T., & Karlsson, L. (2020) · Infant Behavior and Development · doi:10.1016/j.infbeh.2020.101471 · Cited by 7 · see citing works
Besnier, N., Cassé‐Perrot, C., Jouve, É., Nguyen, N. P. T., Lançon, C., Falissard, B., & Blin, O. J. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1691-4 · Cited by 6 · see citing works
Baldwin, D. S., & Garner, M. J. (2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(07)00018-5 · Cited by 4 · see citing works
Serotonin Disturbance in Mouse Models of Autism Spectrum Disorders
Tamada, K., & Takumi, T. (2014) · Neuromethods · doi:10.1007/978-1-4939-2250-5_9 · Cited by 4 · see citing works
Dietary tryptophan affects group behavior in a social bird
Saldanha, B. C., Beltrão, P., Gomes, A. C. R., Soares, M. C., Cardoso, G. C., & Trigo, S. (2024) · Behavioral Ecology · doi:10.1093/beheco/arae018 · Cited by 2 · see citing works
Patterns and correlates of prosocial behaviour development
Nantel‐Vivier, A. (2010) · eScholarship@McGill (McGill) · doi:10.82308/9475 · Cited by 2 · see citing works
Manipulating serotonin function in depression
Merens, W. (2003) · Leiden Repository (Leiden University)
Zuccolo, P. F., Corchs, F., & Neto, D. M. R. (2017) · Perspectivas em Análise do Comportamento · doi:10.18761/perspectivas.v3i2.229
Thurgood, C. (2005) · Swinburne figshare (Swinburne University of Technology) · doi:10.25916/sut.26261321
Neuropsychopharmacology of appetite in healthy volunteers
Thomas, J. M. (2015) · University of Birmingham Institutional Research Archive (University of Birmingham)
Other Times I Can Barely See: The Effects of Hallucinogens on Vision and Attention
Baggott, M. J. (2010) · eScholarship (California Digital Library)
Current awareness in human psychopharmacology
(2004) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/hup.563
Colzato, L. S., Moratinos, A. B. R., Reuter, M., & Kirsch, P. (2017) · Springer eBooks · doi:10.1007/978-3-319-57505-6_2
RetractedNeural and Behavioral Correlates of PTSD and Alcohol Use
Forster, G. L. (2014) · Defense Technical Information Center (DTIC) · doi:10.21236/ada610004
“However, it has been emphasized that the effects of serotonergic challenge on fear recognition and amygdala activation appear to be dependent upon the individual’s baseline sensitivity to threat [212], gender [213] and genotype [214].”
Backgroundde Sousa, P. S. L., Vasquez, J. J. B., Daza-Cardona, E. A., da Conceição, Y. R. S., & Gouvêia, A. (2025) · Caderno Pedagógico · doi:10.54033/cadpedv22n5-228
Fisher, P. M. (2010) · D-Scholarship@Pitt (University of Pittsburgh)
de Sousa, P. S. L., Buenhombre, J., Daza-Cardona, E. A., Richard, Y., & Gouvêia, A. (2024) · Research Square · doi:10.21203/rs.3.rs-4151627/v1
Zerón-Rugerio, M. F., Parilli‐Moser, I., Gonzalez-Rodriguez, A., Urpí-Sardà, M., Diez-Hernández, M., Ibarra-Picón, A., Barrau-Martínez, B., Pérez-Cano, F. J., Cambras, T., & Izquierdo-Pulido, M. (2026) · Food & Function · doi:10.1039/d6fo00807k
- Authors
- Attenburrow, M.-J., Williams, C., Odontiadis, J., Reed, A., Powell, J., Cowen, P. J., & Harmer, C. J.
- Affiliations
- Warneford Hospital (GB)
- Unilever (United Kingdom) (GB)
- Corresponding author
- Cowen, P. J.
- Venue
- Psychopharmacology
- Published
- 2003-08-01
- Volume
- 169
- Issue
- 1
- Pages
- 104-107
- ISSN
- 0033-3158 (ISSN-L)
- 1432-2072
- OpenAlex
- W2052009832
- Cited by
- 96
- References
- 18
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 4 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 5 · 2014: 3 · 2013: 4 · 2012: 6
- FWCI
- 2.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Psychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Unilever
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- tryptophan, serotonin, facial expression recognition, fear recognition, emotional processing, cortisol, milk protein, neuropsychological outcomes
- MeSH terms
- Adult, Biological Availability, Diet, Double-Blind Method, Facial Expression, Fear, Female, Humans, Hydrocortisone, Middle Aged, Prolactin, Serotonin, Tryptophan, Human Growth Hormone
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