Response properties of human amygdala subregions: evidence based on functional MRI combined with probabilistic anatomical maps
Open accessAbstract
The human amygdala is thought to play a pivotal role in the processing of emotionally significant sensory information. The major subdivisions of the human amygdala-the laterobasal group (LB), the superficial group (SF), and the centromedial group (CM)-have been anatomically delineated, but the functional response properties of these amygdala subregions in humans are still unclear. We combined functional MRI with cyto-architectonically defined probabilistic maps to analyze the response characteristics of amygdala subregions in subjects presented with auditory stimuli. We found positive auditory stimulation-related signal changes predominantly in probabilistically defined LB, and negative responses predominantly in SF and CM. In the left amygdala, mean response magnitude in the core area of LB with 90-100% assignment probability was significantly larger than in the core areas of SF and CM. These differences were observed for pleasant and unpleasant stimuli. Our findings reveal that the probabilistically defined anatomical subregions of the human amygdala show distinctive fMRI response patterns. The stronger auditory responses in LB as compared with SF and CM may reflect a predominance of auditory inputs to human LB, similar to many animal species in which the majority of sensory, including auditory, afferents project to this subdivision of the amygdala. Our study indicates that the intrinsic functional differentiation of the human amygdala may be probed using fMRI combined with probabilistic anatomical maps.
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Males with positive resting-state functional connectivity between parieto-occipital regions and the basolateral amygdala may have memory problems, because the basolateral amygdala is important for memory in addition to emotional processing.
“Although all sub-regions are relevant for emotional processing (Ball et al., 2007, Hurlemann et al., 2008, Bzdok et al., 2013a), BLA is additionally important for memory function (Bzdok et al., 2013a); therefore, males demonstrating positive RSFC between parieto-occipital and BLA may report problems with memory functions.”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Ball et al., 2007
The AM is thought to automatically extract biological significance from the environment.
“This brain region is thought to automatically extract biological significance from the environment (Ball et al. 2007; Sander et al. 2003; Bzdok et al. 2011; Müller et al. 2011).”
From Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy (2012) · cites this paper as Ball et al. 2007
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Cites
The assessment and analysis of handedness: The Edinburgh inventory
Oldfield, R. C. (1971) · Neuropsychologia · doi:10.1016/0028-3932(71)90067-4 · Cited by 35,900 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles, K. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.034 · Cited by 4,033 · see citing works
Self-citationContributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · see citing works
Blood, A. J., & Zatorre, R. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191355898 · Cited by 2,814 · see citing works
Both of Us Disgusted in My Insula
Wicker, B., Keysers, C., Plailly, J., Royet, J.-P., Gallese, V., & Rizzolatti, G. (2003) · Neuron · doi:10.1016/s0896-6273(03)00679-2 · Cited by 2,185 · see citing works
How brains beware: neural mechanisms of emotional attention
Vuilleumier, P. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.10.011 · Cited by 2,162 · see citing works
The Amygdaloid Complex: Anatomy and Physiology
SAH, P., FABER, E. S. L., LOPEZ DE ARMENTIA, M., & POWER, J. (2003) · Physiological Reviews · doi:10.1152/physrev.00002.2003 · Cited by 1,745 · see citing works
Neurobiology of emotion perception II: implications for major psychiatric disorders
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00171-9 · Cited by 1,736 · see citing works
Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression
Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., & Rosen, B. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80219-6 · Cited by 1,711 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
Cognitive Neuroscience of Emotion
(1999) · doi:10.1093/oso/9780195118889.001.0001 · Cited by 1,288 · see citing works
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., & Zilles, K. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0025-5 · Cited by 1,264 · see citing works
Blood, A. J., Zatorre, R. J., Bermudez, P., & Evans, A. C. (1999) · Nature Neuroscience · doi:10.1038/7299 · Cited by 1,097 · see citing works
The human amygdala and the emotional evaluation of sensory stimuli
Zald, D. H. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00248-5 · Cited by 1,062 · see citing works
The rewards of music listening: Response and physiological connectivity of the mesolimbic system
Menon, V., & Levitin, D. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.05.053 · Cited by 1,059 · see citing works
Dissociated neural representations of intensity and valence in human olfaction
Anderson, A. K., Christoff, K., Stappen, I., Panitz, D., Ghahremani, D. G., Glover, G., Gabrieli, J. D. E., & Sobel, N. (2003) · Nature Neuroscience · doi:10.1038/nn1001 · Cited by 1,054 · see citing works
Investigating emotion with music: An fMRI study
Koelsch, S., Fritz, T., v. Cramon, D. Y., Müller, K., & Friederici, A. D. (2006) · Human Brain Mapping · doi:10.1002/hbm.20180 · Cited by 1,037 · see citing works
Pitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980 · see citing works
The Human Amygdala: An Evolved System for Relevance Detection
Sander, D., Grafman, J., & Zalla, T. (2003) · Reviews in the Neurosciences · doi:10.1515/revneuro.2003.14.4.303 · Cited by 944 · cited 1× · see citing works
“The challenge of unraveling the function of the human amygdala is attracting great interest [1–5].”
BackgroundNeuropsychology of fear and loathing
Calder, A. J., Lawrence, A. D., & Young, A. W. (2001) · Nature reviews. Neuroscience · doi:10.1038/35072584 · Cited by 927 · see citing works
Shmuel, A., Augath, M., Oeltermann, A., & Logothetis, N. K. (2006) · Nature Neuroscience · doi:10.1038/nn1675 · Cited by 898 · see citing works
Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation
Small, D. M., Gregory, M. D., Mak, Y. E., Gitelman, D. R., Mesulam, M. M., & Parrish, T. B. (2003) · Neuron · doi:10.1016/s0896-6273(03)00467-7 · Cited by 789 · see citing works
Deficient Fear Conditioning in Psychopathy
Birbaumer, N., Veit, R., Lotze, M., Erb, M., Hermann, C., Grodd, W., & Flor, H. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.7.799 · Cited by 706 · see citing works
A functional MRI study of human amygdala responses to facial expressions of fear versus anger.
Whalen, P. J., Shin, L. M., McInerney, S. C., Fischer, H., Wright, C. I., & Rauch, S. L. (2001) · Emotion · doi:10.1037/1528-3542.1.1.70 · Cited by 660 · see citing works
Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli
Wright, C. I., Fischer, H., Whalen, P. J., McInerney, S. C., Shin, L. M., & Rauch, S. L. (2001) · Neuroreport · doi:10.1097/00001756-200102120-00039 · Cited by 533 · see citing works
Lateralization of amygdala activation: a systematic review of functional neuroimaging studies
Baas, D., Aleman, A., & Kahn, R. S. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.02.004 · Cited by 509 · see citing works
Passive music listening spontaneously engages limbic and paralimbic systems
Brown, S., Martinez, M. J., & Parsons, L. M. (2004) · NeuroReport · doi:10.1097/00001756-200409150-00008 · Cited by 468 · see citing works
Comparative aspects of amygdala connectivity
PRICE, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07070.x · Cited by 442 · see citing works
fMRI reveals amygdala activation to human faces in social phobics
Birbaumer, N., Grodd, W., Diedrich, O., Klose, U., Erb, M., Lotze, M., Schneider, F., Weiss, U., & Flor, H. (1998) · NeuroReport · doi:10.1097/00001756-199804200-00048 · Cited by 390 · see citing works
Contextual modulation of amygdala responsivity to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Polis, S., Alexander, A. L., Shin, L. M., & Whalen, P. J. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042947865 · Cited by 389 · see citing works
Brain circuits involved in emotional learning in antisocial behavior and social phobia in humans
Veit, R., Flor, H., Erb, M., Hermann, C., Lotze, M., Grodd, W., & Birbaumer, N. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00519-0 · Cited by 377 · see citing works
Seifritz, E., Esposito, F., Neuhoff, J. G., Lüthi, A., Mustovic, H., Dammann, G., von Bardeleben, U., Radue, E. W., Cirillo, S., Tedeschi, G., et al. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00697-8 · Cited by 373 · see citing works
Turner, R. (2002) · NeuroImage · doi:10.1006/nimg.2002.1082 · Cited by 365 · see citing works
Inverse amygdala and medial prefrontal cortex responses to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2003) · NeuroReport · doi:10.1097/00001756-200312190-00006 · Cited by 359 · see citing works
Zaitsev, M., Hennig, J., & Speck, O. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20261 · Cited by 350 · see citing works
Self-citationIntegrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala
Winston, J. S., Gottfried, J. A., Kilner, J. M., & Dolan, R. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1569-05.2005 · Cited by 287 · see citing works
Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study
Fischer, H., Wright, C. I., Whalen, P. J., McInerney, S. C., Shin, L. M., & Rauch, S. L. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00940-1 · Cited by 250 · see citing works
Bordi, F., & LeDoux, J. E. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02493.1992 · Cited by 218 · see citing works
Morris, J. S., Büchel, C., & Dolan, R. J. (2001) · NeuroImage · doi:10.1006/nimg.2000.0721 · Cited by 212 · see citing works
Cognitive-Emotional Interactions: Listen to the Brain
LeDoux, J. E. (1999) · doi:10.1093/oso/9780195118889.003.0007 · Cited by 210 · see citing works
Extended Amygdala and Emotional Salience: A PET Activation Study of Positive and Negative Affect
Liberzon, I., Phan, K. L., Decker, L. R., & Taylor, S. F. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300113 · Cited by 189 · see citing works
Is There an Amygdala and How Far Does It Extend?
McDonald, A. J. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07067.x · Cited by 169 · see citing works
Functional MRI of the Human Amygdala?
Merboldt, K., Fransson, P., Bruhn, H., & Frahm, J. (2001) · NeuroImage · doi:10.1006/nimg.2001.0802 · Cited by 162 · see citing works
Brain regions involved in the recognition of happiness and sadness in music
Khalfa, S. P., Schön, D., Anton, J., & Liégeois‐Chauvel, C. (2005) · Neuroreport · doi:10.1097/00001756-200512190-00002 · Cited by 154 · see citing works
The Role of the Amygdala in Primate Social Cognition
Emery, N. J., & Amaral, D. G. (1999) · doi:10.1093/oso/9780195118889.003.0008 · Cited by 141 · see citing works
Optimized 3 T EPI of the amygdalae
Robinson, S., Windischberger, C., Rauscher, A., & Moser, E. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.12.048 · Cited by 133 · see citing works
The human basal forebrain. Part II
Heimer, L., de Olmos, J. S., Alheid, G. F., Pearson, J., Sakamoto, N., Shinoda, K., Marksteiner, J., & Switzer, R. C. (1999) · Handbook of Chemical Neuroanatomy · doi:10.1016/s0924-8196(99)80024-4 · Cited by 125 · see citing works
Left Auditory Cortex and Amygdala, but Right Insula Dominance for Human Laughing and Crying
Sander, K., & Scheich, H. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/089892905774597227 · Cited by 93 · see citing works
Gonzalez-Lima, F., & Scheich, H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91009-7 · Cited by 76 · see citing works
Reciprocal Changes in the Firing Probability of Lateral and Central Medial Amygdala Neurons
Collins, D. R., & Paré, D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-02-00836.1999 · Cited by 70 · see citing works
Krishnan, S., Slavin, M. J., Tran, T.-T. T., Doraiswamy, P. M., & Petrella, J. R. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.12.061 · Cited by 34 · see citing works
Integrated volume visualization of functional image data and anatomical surfaces using normal fusion
Stokking, R., Zuiderveld, K. J., & Viergever, M. A. (2001) · Human Brain Mapping · doi:10.1002/1097-0193(200104)12:4 · Cited by 24 · see citing works
Blood supply of the rat amygdala.
Merksz, M., Ambach, G., & Palkovits, M. (1978) · PubMed · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
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Functional connectivity of the human amygdala using resting state fMRI
Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Gotimer, K., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.11.030 · Cited by 749 · see citing works
Bzdok, D., Schilbach, L., Vogeley, K., Schneider, K., Laird, A. R., Langner, R., & Eickhoff, S. B. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0380-y · Cited by 653 · see citing works
Self-citationTowards a neural basis of music-evoked emotions
Koelsch, S. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.01.002 · Cited by 651 · see citing works
A neuroscientific perspective on music therapy
Koelsch, S. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04592.x · Cited by 387 · see citing works
Gabard-Durnam, L. J., Flannery, J., Goff, B., Gee, D. G., Humphreys, K. L., Telzer, E., Hare, T., & Tottenham, N. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.038 · Cited by 372 · see citing works
Di Martino, A., Zuo, X.-N., Kelly, C., Grzadzinski, R., Mennes, M., Schvarcz, A., Rodman, J., Lord, C., Castellanos, F. X., & Milham, M. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.02.011 · Cited by 345 · see citing works
Chase, H. W., Eickhoff, S. B., Laird, A. R., & Hogarth, L. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.025 · Cited by 316 · see citing works
Self-citationThe role of the amygdala in atypical gaze on emotional faces in autism spectrum disorders
Kliemann, D., Dziobek, I., Hatri, A., Baudewig, J., & Heekeren, H. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5294-11.2012 · Cited by 183 · see citing works
ALE meta-analysis on facial judgments of trustworthiness and attractiveness
Bzdok, D., Langner, R., Caspers, S., Kurth, F., Habel, U., Zilles, K., Laird, A., & Eickhoff, S. B. (2011) · Brain Structure and Function · doi:10.1007/s00429-010-0287-4 · Cited by 183 · see citing works
Self-citationSelective processing of social stimuli in the superficial amygdala
Goossens, L., Kukolja, J., Onur, O. A., Fink, G. R., Maier, W., Griez, E., Schruers, K., & Hurlemann, R. (2009) · Human Brain Mapping · doi:10.1002/hbm.20755 · Cited by 132 · see citing works
Amygdala hyperreactivity in restrictive anorexia nervosa
Joos, A. A. B., Saum, B., van Elst, L. T., Perlov, E., Glauche, V., Hartmann, A., Freyer, T., Tüscher, O., & Zeeck, A. (2011) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2010.11.008 · Cited by 124 · see citing works
Developmental sex differences in resting state functional connectivity of amygdala sub-regions
Alarcón, G., Cservenka, A., Rudolph, M. D., Fair, D. A., & Nagel, B. J. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.04.013 · Cited by 105 · see citing works
Neural correlates of prenatal stress in young women
Favaro, A., Tenconi, E., Degortes, D., Manara, R., & Santonastaso, P. (2015) · Psychological Medicine · doi:10.1017/s003329171500046x · Cited by 51 · see citing works
Hurlemann, R., Rehme, A. K., Diessel, M., Kukolja, J., Maier, W., Walter, H., & Cohen, M. X. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.04.004 · Cited by 51 · see citing works
Current emotion research in behavioral neuroscience: the role(s) of the amygdala
Armony, J. L. (2013) · Emotion Review · doi:10.1177/1754073912457208 · Cited by 44 · see citing works
Sex differences in amygdala subregions: evidence from subregional shape analysis
Kim, H. J., Kim, N., Kim, S., Hong, S., Park, K., Lim, S., Park, J.-M., Na, B., Chae, Y., Lee, J., et al. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.02.025 · Cited by 40 · see citing works
Frontocingular Dysfunction in Bulimia Nervosa when Confronted with Disease‐specific Stimuli
Joos, A. A. B., Saum, B., Zeeck, A., Perlov, E., Glauche, V., Hartmann, A., Freyer, T., Sandholz, A., Unterbrink, T., van Elst, L. T., et al. (2011) · European Eating Disorders Review · doi:10.1002/erv.1150 · Cited by 35 · see citing works
Neumeister, P., Feldker, K., Heitmann, C. Y., Buff, C., Brinkmann, L., Bruchmann, M., & Straube, T. (2018) · Psychological Medicine · doi:10.1017/s0033291717002513 · Cited by 28 · see citing works
Kim, N., Kim, H. J., Hwang, J., Yoon, S. J., Cho, H. B., Renshaw, P. F., Lyoo, I. K., & Kim, J. E. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2010.11.005 · Cited by 11 · see citing works
- Authors
- Ball, T., Rahm, B., Eickhoff, S. B., Schulze-Bonhage, A., Speck, O., & Mutschler, I.
- Affiliations
- Goethe University Frankfurt (DE)
- Forschungszentrum Jülich (DE)
- University Medical Center Freiburg (DE)
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-03-21
- Volume
- 2
- Issue
- 3
- Pages
- e307
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC1819558
- OpenAlex
- W1998410431
- Cited by
- 176
- References
- 54
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 4 · 2023: 14 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 9 · 2018: 8 · 2017: 18 · 2016: 14 · 2015: 10 · 2014: 15 · 2013: 14 · 2012: 10
- FWCI
- 5.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- edoc (University of Basel) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- JuSER (Forschungszentrum Jülich) (submittedVersion)
- Publication Server of Goethe University Frankfurt am Main (Goethe University Frankfurt) (submittedVersion, cc-by)
- edoc (University of Basel)
- Funders
- Albert-Ludwigs-Universität Freiburg
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- human amygdala, amygdala subregions, superficial amygdala, centromedial amygdala, auditory stimulation, emotional processing, cytoarchitecture, auditory afferents, emotional valence
- MeSH terms
- Acoustic Stimulation, Adult, Amygdala, Anatomy, Depression, Emotions, Facial Expression, Humans, Functional Laterality, Magnetic Resonance Imaging, Motivation, Music, Probability, Surveys and Questionnaires, Young Adult
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