Role of the hippocampus and orbitofrontal cortex during the disambiguation of social cues in working memory
Open accessAbstract
Human social interactions are complex behaviors requiring the concerted effort of multiple neural systems to track and monitor the individuals around us. Cognitively, adjusting our behavior on the basis of changing social cues such as facial expressions relies on working memory and the ability to disambiguate, or separate, the representations of overlapping stimuli resulting from viewing the same individual with different facial expressions. We conducted an fMRI experiment examining the brain regions contributing to the encoding, maintenance, and retrieval of overlapping identity information during working memory using a delayed match-to-sample task. In the overlapping condition, two faces from the same individual with different facial expressions were presented at sample. In the nonoverlapping condition, the two sample faces were from two different individuals with different expressions. fMRI activity was assessed by contrasting the overlapping and nonoverlapping conditions at sample, delay, and test. The lateral orbitofrontal cortex showed increased fMRI signal in the overlapping condition in all three phases of the delayed match-to-sample task and increased functional connectivity with the hippocampus when encoding overlapping stimuli. The hippocampus showed increased fMRI signal at test. These data suggest that lateral orbitofrontal cortex helps encode and maintain representations of overlapping stimuli in working memory, whereas the orbitofrontal cortex and hippocampus contribute to the successful retrieval of overlapping stimuli. We suggest that the lateral orbitofrontal cortex and hippocampus play a role in encoding, maintaining, and retrieving social cues, especially when multiple interactions with an individual need to be disambiguated in a rapidly changing social context in order to make appropriate social responses.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The hippocampal-orbitofrontal cortex-amygdala neural network has been implicated in cognitive processes related to social memory.
“This neural network has been implicated in the cognitive processes related to social memory [139]”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [139]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Ekman, P. (1976) · Medical Entomology and Zoology · Cited by 4,345 · see citing works
Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1
Boynton, G., Engel, S., Glover, G., & Heeger, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-13-04207.1996 · Cited by 2,522 · see citing works
Coding facial expressions with Gabor wavelets
Lyons, M. J., Akamatsu, S., Kamachi, M., & Gyoba, J. (2002) · International Conference on Automatic Face and Gesture Recognition · doi:10.1109/afgr.1998.670949 · Cited by 2,214 · see citing works
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
The functions of the orbitofrontal cortex
Rolls, E. T. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00277-x · Cited by 1,327 · see citing works
Lateral prefrontal cortex: architectonic and functional organization
Petrides, M. (2005) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2005.1631 · Cited by 1,212 · see citing works
Web-Based Database for Facial Expression Analysis
Pantić, M., Valstar, M., Rademaker, R. M., & Maat, L. (2005) · IEEE International Conference on Multimedia and Expo (ICME) · doi:10.1109/icme.2005.1521424 · Cited by 1,099 · see citing works
Wood, E. R., Dudchenko, P. A., Robitsek, R. J., & Eichenbaum, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)00071-4 · Cited by 992 · see citing works
Architectonic subdivision of the human orbital and medial prefrontal cortex
Öngür, D., Ferry, A. T., & Price, J. L. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10609 · Cited by 944 · see citing works
The Anatomical Connections of the Macaque Monkey Orbitofrontal Cortex. A Review
Cavada, C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.220 · Cited by 917 · see citing works
Measuring functional connectivity during distinct stages of a cognitive task
Rissman, J., Gazzaley, A. H., & D’Esposito, M. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.06.035 · Cited by 894 · see citing works
Object and Spatial Visual Working Memory Activate Separate Neural Systems in Human Cortex
Courtney, S. M., Ungerleider, L. G., Keil, K., & Haxby, J. V. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.1.39 · Cited by 891 · see citing works
Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes
Slotnick, S. D., Moo, L. R., Segal, J. B., & Hart, J. (2003) · Cognitive Brain Research · doi:10.1016/s0926-6410(03)00082-x · Cited by 654 · see citing works
Gur, R. C., Šára, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., Turner, T. H., Bajcsy, R., Posner, A., & Gur, R. E. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00006-7 · Cited by 647 · see citing works
Fellows, L. K. (2003) · Brain · doi:10.1093/brain/awg180 · Cited by 631 · see citing works
Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat
McAlonan, K., & Brown, V. J. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.019 · Cited by 618 · see citing works
Hornak, J., O'Doherty, J., Bramham, J., Rolls, E. T., Morris, R. G., Bullock, P. R., & Polkey, C. E. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/089892904322926791 · Cited by 603 · see citing works
Chudasama, Y., & Robbins, T. W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08771.2003 · Cited by 543 · see citing works
Berlin, H. A. (2004) · Brain · doi:10.1093/brain/awh135 · Cited by 541 · see citing works
Integrating Memories in the Human Brain: Hippocampal-Midbrain Encoding of Overlapping Events
Daphna Shohamy, A., & Wagner, A. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.023 · Cited by 525 · see citing works
Barbas, H., & Blatt, G. J. (1995) · Hippocampus · doi:10.1002/hipo.450050604 · Cited by 453 · see citing works
The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags
Hannula, D. E., Tranel, D., & Cohen, N. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5222-05.2006 · Cited by 436 · see citing works
Walton, M. E., Behrens, T. E. J., Buckley, M. J., Rudebeck, P. H., & Rushworth, M. F. S. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.027 · Cited by 397 · see citing works
Working Memory for Conjunctions Relies on the Medial Temporal Lobe
Olson, I. R., Page, K., Moore, K. S., Chatterjee, A. K., & Verfaellie, M. H. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1923-05.2006 · Cited by 395 · see citing works
Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information
Charan Ranganath, A., & D’Esposito, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00411-1 · Cited by 391 · see citing works
The hippocampus is required for short‐term topographical memory in humans
Hartley, T., Bird, C. M., Chan, D., Cipolotti, L., Husain, M., Vargha‐Khadem, F., & Burgess, N. (2006) · Hippocampus · doi:10.1002/hipo.20240 · Cited by 349 · see citing works
Meunier, M. (1997) · Neuropsychologia · doi:10.1016/s0028-3932(97)00027-4 · Cited by 348 · see citing works
Otto, T., & Eichenbaum, H. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.5.762 · Cited by 343 · see citing works
Scheperjans, F., Eickhoff, S. B., Hömke, L., Mohlberg, H., Hermann, K., Amunts, K., & Zilles, K. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm241 · Cited by 336 · see citing works
Human Brain Anatomy in Computerized Images
Damásio, H. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195165616.001.0001 · Cited by 333 · see citing works
Otto, T., & Eichenbaum, H. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.5.762 · Cited by 317 · see citing works
Schoenbaum, G., Setlow, B., Nugent, S. L., Saddoris, M. P., & Gallagher, M. (2003) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.55203 · Cited by 317 · see citing works
Neural correlates of rapid reversal learning in a simple model of human social interaction
Kringelbach, M. L., & Rolls, E. T. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00393-8 · Cited by 306 · see citing works
Haxby, J. V., Petit, L., Ungerleider, L. G., & Courtney, S. M. (2000) · NeuroImage · doi:10.1006/nimg.2000.0592 · Cited by 300 · see citing works
Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence
Charan Ranganath, A., Cohen, M. X., & Brozinsky, C. J. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929054475118 · Cited by 294 · see citing works
Match–Mismatch Processes Underlie Human Hippocampal Responses to Associative Novelty
Kumaran, D., & Maguire, E. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1677-07.2007 · Cited by 264 · see citing works
Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli
Stern, C. E., Sherman, S. J., Kirchhoff, B. A., & Hasselmo, M. E. (2001) · Hippocampus · doi:10.1002/hipo.1048 · Cited by 244 · see citing works
Self-citationThe Hippocampus and Disambiguation of Overlapping Sequences
Agster, K. L., Fortin, N. J., & Eichenbaum, H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05760.2002 · Cited by 231 · see citing works
Visual Working Memory Is Impaired when the Medial Temporal Lobe Is Damaged
Olson, I. R., Moore, K. S., Stark, M., & Chatterjee, A. K. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.7.1087 · Cited by 221 · see citing works
Schon, K., Hasselmo, M. E., LoPresti, M. L., Tricarico, M. D., & Stern, C. E. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3807-04.2004 · Cited by 191 · see citing works
Self-citationSala, J. B., Pia Rämä, A., & Courtney, S. M. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00166-5 · Cited by 191 · see citing works
Tsuchida, A., Doll, B. B., & Fellows, L. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1958-10.2010 · Cited by 188 · cited 3× · see citing works
“Additionally, the orbitofrontal cortex is critical for making correct decisions in reversal-learning tasks (Berlin et al., 2004; Chudasama & Robbins, 2003; Fellows & Farah, 2003; Hornak et al., 2004; McAlonan & Brown, 2003; Meunier et al., 1997; Rudebeck & Murray, 2008; Schoenbaum et al., 2003; Tsuchida et al., 2010).”
Roberts, A., Tomic, D. L., Parkinson, C. H., Roeling, T. A. P., Cutter, D. J., Robbins, T. W., & Everitt, B. J. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21300 · Cited by 181 · see citing works
Nichols, E. A., Kao, Y.-C., Verfaellie, M. H., & Gabrieli, J. D. E. (2006) · Hippocampus · doi:10.1002/hipo.20190 · Cited by 180 · see citing works
Schluppeck, D., Curtis, C. E., Glimcher, P. W., & Heeger, D. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5330-05.2006 · Cited by 171 · see citing works
The representation of information about faces in the temporal and frontal lobes
Rolls, E. T. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.04.019 · Cited by 152 · see citing works
Rudebeck, P. H., & Murray, E. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2272-08.2008 · Cited by 148 · see citing works
Insausti, R., & Muñoz, M. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01662.x · Cited by 146 · see citing works
Changes in Limbic and Prefrontal Functional Interactions in a Working Memory Task for Faces
McIntosh, A. R., Grady, C. L., Haxby, J. V., Ungerrleider, L. G., & Horwitz, B. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.4.571 · Cited by 140 · see citing works
Schon, K., Atri, A., Hasselmo, M. E., Tricarico, M. D., LoPresti, M. L., & Stern, C. E. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1982-05.2005 · Cited by 132 · see citing works
Self-citationBrown, T. I., Ross, R. S., Keller, J. B., Hasselmo, M. E., & Stern, C. E. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6021-09.2010 · Cited by 130 · see citing works
Self-citationBower, M. R., Euston, D. R., & McNaughton, B. L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2901-04.2005 · Cited by 124 · see citing works
Working Memory and the Organization of Brain Systems
Shrager, Y., Levy, D. A., Hopkins, R. O., & Squire, L. R. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0710-08.2008 · Cited by 123 · see citing works
The Dynamics of Hippocampal Activation during Encoding of Overlapping Sequences
Kumaran, D., & Maguire, E. A. (2006) · Neuron · doi:10.1016/j.neuron.2005.12.024 · Cited by 120 · see citing works
Intact Working Memory for Relational Information after Medial Temporal Lobe Damage
Jeneson, A., Mauldin, K. N., & Squire, L. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2895-10.2010 · Cited by 109 · see citing works
Olsen, R. K., Nichols, E. A., Chen, J., Hunt, J. F. V., Glover, G. H., Gabrieli, J. D. E., & Wagner, A. D. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2245-09.2009 · Cited by 103 · see citing works
LoPresti, M., Schon, K., Tricarico, M. D., Swisher, J., Celone, K. A., & Stern, C. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0464-08.2008 · Cited by 87 · see citing works
Self-citationCooperative interactions between hippocampal and striatal systems support flexible navigation
Brown, T. I., Ross, R. S., Tobyne, S. M., & Stern, C. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.046 · Cited by 86 · see citing works
Self-citationThe retrieval of learned sequences engages the hippocampus: Evidence from fMRI
Ross, R. S., Brown, T. I., & Stern, C. E. (2009) · Hippocampus · doi:10.1002/hipo.20558 · Cited by 82 · see citing works
Self-citationThe human hippocampal formation mediates short-term memory of colour–location associations
Finke, C., Braun, M., Ostendorf, F., Lehmann, T., Hoffmann, K., Kopp, U. A., & Ploner, C. J. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.10.004 · Cited by 79 · see citing works
Tabbert, K., Stark, R. M., Kirsch, P., & Vaitl, D. (2005) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.01.007 · Cited by 76 · see citing works
Working Memory-Related Hippocampal Deactivation Interferes with Long-Term Memory Formation
Axmacher, N., Elger, C. E., & Fell, J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5277-08.2009 · Cited by 68 · see citing works
Greater Working Memory Load Results in Greater Medial Temporal Activity at Retrieval
Schön, K., Quiroz, Y. T., Hasselmo, M. E., & Stern, C. E. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp006 · Cited by 67 · see citing works
Self-citationHippocampal Neurons Encode Different Episodes in an Overlapping Sequence of Odors Task
Ginther, M. R., Walsh, D. F., & Ramus, S. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3413-10.2011 · Cited by 54 · see citing works
Newmark, R. E., Schön, K., Ross, R. S., & Stern, C. E. (2013) · Hippocampus · doi:10.1002/hipo.22106 · Cited by 51 · see citing works
Self-citationRoss, R. S., Sherrill, K. R., & Stern, C. E. (2011) · Brain Research · doi:10.1016/j.brainres.2011.09.038 · Cited by 39 · see citing works
Self-citationSchön, K., Tinaz, S., Somers, D. C., & Stern, C. E. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.09.023 · Cited by 39 · see citing works
Self-citationTwo Distinct Functional Networks for Successful Resolution of Proactive Interference
Caplan, J. B., McIntosh, A. R., & Rosa, E. D. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl076 · Cited by 37 · see citing works
Schön, K., Ross, R. S., Hasselmo, M. E., & Stern, C. E. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12062 · Cited by 17 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Neural circuits regulating prosocial behaviors
Walsh, J. J., Christoffel, D. J., & Malenka, R. C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-022-01348-8 · Cited by 72 · see citing works
Bristow, G. C., Thomson, D. M., Openshaw, R. L., Mitchell, E. J., Pratt, J. A., Dawson, N., & Morris, B. J. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107536 · Cited by 36 · see citing works
- Authors
- Ross, R. S., LoPresti, M. L., Schon, K., & Stern, C. E.
- Affiliations
- Boston University (US)
- Corresponding author
- Ross, Robert S.
- Venue
- Cognitive, Affective, & Behavioral Neuroscience
- Published
- 2013-05-03
- Volume
- 13
- Issue
- 4
- Pages
- 900-915
- ISSN
- 1530-7026 (ISSN-L)
- 1531-135X
- PMC
- PMC3796192
- OpenAlex
- W2032951281
- Cited by
- 28
- References
- 69
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 3 · 2018: 1 · 2017: 3 · 2016: 1 · 2014: 1
- FWCI
- 0.37
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cognitive Affective & Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- University of New Hampshire Scholars Repository (University of New Hampshire at Manchester) (submittedVersion)
- Funders
- National Institutes of Health (1s10rr021110-01a1)
- National Institute of Mental Health (P50MH071702)
- National Center for Research Resources (P41-RR-14075, P41RR014075, S10‐RR‐021110)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampus, orbitofrontal cortex, working memory, facial expressions, delayed matching-to-sample, functional connectivity, social cognition, face recognition (cognition)
- MeSH terms
- Adolescent, Cues, Discrimination Learning, Facial Expression, Female, Hippocampus, Humans, Image Processing, Computer-Assisted, Male, Memory, Short-Term, Oxygen, Pattern Recognition, Visual, Photic Stimulation, Reaction Time, Linear Models, Prefrontal Cortex, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review