Distinct contributions of frontal areas to emotion and social behaviour in the rat
Open accessAbstract
Although the lesions of patients with impaired social behaviour encompass both orbitofrontal and anterior cingulate cortex (OFC and ACC), attempts to model such impairments in animals have focused on the OFC. However, recent neuroimaging attempts to identify the neural correlates of social interaction have emphasized the relative importance of ACC. Here we report the effect of circumscribed excitotoxic lesions of either OFC or ACC on ethological, unconditioned tests of emotion and social behaviour in the Lister hooded rat. OFC lesions altered emotional responsiveness to stimuli in non‐social, fear‐inducing situations (hyponeophagia test), and produced a small but statistically significant increase in aggression to other rats, but did not compromise other aspects of social interaction and appraisal. ACC lesions did, however, affect the utilization of social information. Specifically, ACC lesions diminished interest in other individuals and caused a relative reduction in memory for social stimuli. Whereas normal animals habituated to repeated presentations of the same individual, the poor performance of ACC animals entailed continued higher levels of responsiveness to repeated presentations of the same individual. The ACC impairment cannot simply be attributed to a general reduction in arousal, or a general impairment in recognition memory. Neither lesion affected anxiety per se (successive alleys test). Further analyses were conducted to investigate whether the changes in aggressive and social behaviour were related to different aspects of decision‐making. Although the relationship between changes in social interaction and decision‐making after ACC lesions is unclear, OFC impairments in emotionality were correlated with increased impulsive choice.
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?
Anterior cingulate lesions can decrease social responsiveness and the memory of social stimuli in rats.
“Further, evidence that anterior cingulate lesions can decrease social responsiveness and the memory of social stimuli in rats (Rudebeck et al., 2007) points to the likely involvement of the bundle.”
From The cingulum bundle: Anatomy, function, and dysfunction (2018) · cites this paper as Rudebeck et al., 2007
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
Meeting of minds: the medial frontal cortex and social cognition
Amodio, D. M., & Frith, C. D. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1884 · Cited by 3,782 · see citing works
Fehr, E., & Fischbacher, U. (2003) · Nature · doi:10.1038/nature02043 · Cited by 3,475 · cited 1× · see citing works
“Cooperation in such tasks is more stable when participants have the opportunity to find out about each other (Fehr & Fischbacher, 2003).”
BackgroundPrefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers
Gabbott, P. L. A., Warner, T. A., Jays, P. R. L., Salway, P., & Busby, S. J. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20738 · Cited by 1,227 · see citing works
Rolls, E. T., Hornak, J., Wade, D., & McGrath, J. (1994) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.57.12.1518 · Cited by 1,005 · see citing works
Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices
Hornak, J. (2003) · Brain · doi:10.1093/brain/awg168 · Cited by 725 · see citing works
Ennaceur, A., Neave, N., & Aggleton, J. P. (1997) · Experimental Brain Research · doi:10.1007/pl00005603 · Cited by 670 · see citing works
Separate neural pathways process different decision costs
Rudebeck, P. H., Walton, M. E., Smyth, A. N., Bannerman, D. M., & Rushworth, M. F. S. (2006) · Nature Neuroscience · doi:10.1038/nn1756 · Cited by 580 · see citing works
Self-citationAmygdala and Ventral Hippocampus Contribute Differentially to Mechanisms of Fear and Anxiety.
McHugh, S. B., Deacon, R. M. J., Rawlins, J. N. P., & Bannerman, D. M. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.63 · Cited by 384 · cited 4× · see citing works
“Journal Compilation ª Federation of European Neuroscience Societies and Blackwell Publishing Ltd unconditioned tests of social interaction and emotionality (Bannerman et al., 2002b; McHugh et al., 2004).”
BackgroundMethodInfluentialSelf-citationA Role for the Macaque Anterior Cingulate Gyrus in Social Valuation
Rudebeck, P. H., Buckley, M. J., Walton, M. E., & Rushworth, M. F. S. (2006) · Science · doi:10.1126/science.1128197 · Cited by 312 · see citing works
Self-citationEncoding of Time-Discounted Rewards in Orbitofrontal Cortex Is Independent of Value Representation
Roesch, M. R., Taylor, A. R., & Schoenbaum, G. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.027 · Cited by 297 · see citing works
Izquierdo, A., Suda, R. K., & Murray, E. A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1232-05.2005 · Cited by 186 · see citing works
Flagged first, then by citations
Research works printed but not linked: 33
- Bannerman DM Deacon RM Offen S Friswell J Grubb M Rawlins JN Double dissociation of function within the hippocampus: spatial memory and hyponeophagia Behav. Neurosci. 2002a 116 884 901 12369808
- Bannerman DM Lemaire M Beggs S Rawlins JN Iversen SD Cytotoxic lesions of the hippocampus increase social investigation but do not impair social-recognition memory Exp. Brain Res. 2001 138 100 109 11374076
- Bannerman DM Lemaire M Yee BK Iversen SD Oswald CJ Good MA Rawlins JN Selective cytotoxic lesions of the retrohippocampal region produce a mild deficit in social recognition memory Exp. Brain Res. 2002b 142 395 401 11819048
- Baxter MG Parker A Lindner CC Izquierdo AD Murray EA Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex J. Neurosci. 2000 20 4311 4319 10818166 PMC6772657
- Bechara A Damasio H Damasio AR Emotion, decision making and the orbitofrontal cortex Cereb. Cortex 2000 10 295 307 10731224
- de Bruin JP van Oyen HG Van de Poll N Behavioural changes following lesions of the orbital prefrontal cortex in male rats Behav. Brain Res. 1983 10 209 232 6686460
- Burns SM Wyss JM The involvement of the anterior cingulate cortex in blood pressure control Brain Res. 1985 340 71 77 4027647
- Butter CM Snyder DR McDonald JA Effects of orbital frontal lesions on aversive and aggressive behaviors in rhesus monkeys J. Comp. Physiol. Psychol. 1970 72 132 144 4987458
- Chudasama Y Robbins TW Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex J. Neurosci. 2003 23 8771 8780 14507977 PMC6740430
- Cummings JL Frontal-subcortical circuits and human behavior Arch. Neurol. 1993 50 873 880 8352676
- Floyd NS Price JL Ferry AT Keay KA Bandler R Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat J. Comp. Neurol. 2000 422 556 578 10861526
- Galef BG Heyes C Galef BG Social enhancement of food preference in Norway rats: a brief review Social Learning in Animals: the Roots of Culture 1986 Burlington, MA Academic Press 49 64
- Hadland KA Rushworth MF Gaffan D Passingham RE The effect of cingulate lesions on social behaviour and emotion Neuropsychologia 2003 41 919 931 12667528
- Izquierdo A Suda RK Murray EA Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency J. Neurosci. 2004 24 7540 7548 15329401 PMC6729636
- Kennerley SW Walton ME Behrens TE Buckley MJ Rushworth MF Optimal decision making and the anterior cingulate cortex Nat. Neurosci. 2006 9 940 947 16783368
- King-Casas B Tomlin D Anen C Camerer CF Quartz SR Montague PR Getting to know you: reputation and trust in a two-person economic exchange Science 2005 308 78 83 15802598
- Kolb B Social behavior of rats with chronic prefrontal lesions J. Comp. Physiol. Psychol. 1974 87 466 474 4472309
- Machado CJ Bachevalier J The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta) Behav. Neurosci. 2006 120 761 786 16893284
- Mitchell JP Macrae CN Banaji MR Encoding-specific effects of social cognition on the neural correlates of subsequent memory J. Neurosci. 2004 24 4912 4917 15163682 PMC6729362
- Mobini S Body S Ho MY Bradshaw CM Szabadi E Deakin JF Anderson IM Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement Psychopharmacology (Berl.) 2002 160 290 298 11889498
- Paxinos G Watson C The Rat Brain in Stereotaxic Coordinates 1998 San Diego Academic Press
- Rilling J Gutman D Zeh T Pagnoni G Berns G Kilts C A neural basis for social cooperation Neuron 2002 35 395 405 12160756
- Rilling JK Sanfey AG Aronson JA Nystrom LE Cohen JD The neural correlates of theory of mind within interpersonal interactions Neuroimage 2004 22 1694 1703 15275925
- Roesch MR Olson CR Neuronal activity related to reward value and motivation in primate frontal cortex Science 2004 304 307 310 15073380
- Rolls ET The Brain and Emotion 1999 Oxford Oxford University Press
- Ross RS McGaughy J Eichenbaum H Acetylcholine in the orbitofrontal cortex is necessary for the acquisition of a socially transmitted food preference Learn. Mem. 2005 12 302 306 15897258 PMC1142459
- Shah AA Treit D Excitotoxic lesions of the medial prefrontal cortex attenuate fear responses in the elevated-plus maze, social interaction and shock probe burying tests Brain Res. 2003 969 183 194 12676379
- Shidara M Richmond BJ Anterior cingulate: single neuronal signals related to degree of reward expectancy Science 2002 296 1709 1711 12040201
- Somerville LH Heatherton TF Kelley WM Anterior cingulate cortex responds differentially to expectancy violation and social rejection Nat. Neurosci. 2006 9 1007 1008 16819523
- Tomlin D Kayali MA King-Casas B Anen C Camerer CF Quartz SR Montague PR Agent-specific responses in the cingulate cortex during economic exchanges Science 2006 312 1047 1050 16709783
- Vogt BA Peters A Form and distribution of neurons in rat cingulate cortex: areas 32, 24, and 29 J. Comp. Neurol. 1981 195 603 625 7462444
- Walton ME Bannerman DM Alterescu K Rushworth MF Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions J. Neurosci. 2003 23 6475 6479 12878688 PMC6740644
- Yee BK Cytotoxic lesion of the medial prefrontal cortex abolishes the partial reinforcement extinction effect, attenuates prepulse inhibition of the acoustic startle reflex and induces transient hyperlocomotion, while sparing spontaneous object recognition memory in the rat Neuroscience 2000 95 675 689 10670435
Cited by
Sorted by citations
Choice, uncertainty and value in prefrontal and cingulate cortex
Rushworth, M. F. S., & Behrens, T. E. J. (2008) · Nature Neuroscience · doi:10.1038/nn2066 · Cited by 866 · see citing works
Self-citationThe cingulum bundle: Anatomy, function, and dysfunction
Bubb, E. J., Metzler-Baddeley, C., & Aggleton, J. P. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.008 · Cited by 740 · see citing works
“Further, evidence that anterior cingulate lesions can decrease social responsiveness and the memory of social stimuli in rats (Rudebeck et al., 2007) points to the likely involvement of the bundle.”
The Anterior Cingulate Gyrus and Social Cognition: Tracking the Motivation of Others
Apps, M. A. J., Rushworth, M. F. S., & Chang, S. W. C. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.018 · Cited by 559 · see citing works
Self-citationClan mentality: evidence that the medial prefrontal cortex responds to close others
Krienen, F. M., Tu, P.-C., & Buckner, R. L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2180-10.2010 · Cited by 256 · see citing works
“…interactions (Glees et al., 1950; Eslinger and Damasio, 1985; Damasio et al., 1990; Rolls et al., 1994; Stone et al., 1998; Anderson et al., 1999; Hadland et al., 2003; Mah et al., 2005; Rudebeck et al., 2006, 2007) [for review, see Damasio et al. (1996), Stuss (2002), and Adolphs (2003, 2009)].”
Barch, D. M., Pagliaccio, D., & Luking, K. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_376 · Cited by 218 · see citing works
How good is the macaque monkey model of the human brain?
Passingham, R. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.01.002 · Cited by 181 · see citing works
Advances in understanding neural mechanisms of social dominance
Zhou, T., Sandi, C., & Hu, H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.006 · Cited by 133 · see citing works
Sex differences in social interaction in rats: role of the immediate-early gene Zif268
Stack, A., Carrier, N., Dietz, D., Hollis, F., Sorenson, J., & Kabbaj, M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.163 · Cited by 113 · see citing works
Prefrontal Regulation of Threat-Elicited Behaviors: A Pathway to Translation
Roberts, A. C. (2020) · Annual Review of Psychology · doi:10.1146/annurev-psych-010419-050905 · Cited by 50 · see citing works
Reichelt, A. C., Loughman, A., Bernard, A., Raipuria, M., Abbott, K. N., Dachtler, J., Van, T. T. H., & Moore, R. J. (2020) · Nutritional Neuroscience · doi:10.1080/1028415x.2018.1537169 · Cited by 49 · see citing works
Kuniishi, H., Ichisaka, S., Matsuda, S., Futora, E., Harada, R., & Hata, Y. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00250 · Cited by 34 · see citing works
Cholinergic transmission from the basal forebrain modulates social memory in male mice
Kljakic, O., Al‐Onaizi, M., Janíčková, H., Chen, K. S., Guzman, M. S., Prado, M. A. M., & Prado, V. F. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15400 · Cited by 22 · see citing works
Turano, A., McAuley, E. M., Muench, M. C., & Schwarz, J. M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113449 · Cited by 11 · see citing works
- Authors
- Rudebeck, P. H., Walton, M. E., Millette, B. H. P., Shirley, E., Rushworth, M. F. S., & Bannerman, D. M.
- Affiliations
- University of Oxford (GB)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2007-10
- Volume
- 26
- Issue
- 8
- Pages
- 2315-2326
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC2228395
- OpenAlex
- W1518543521
- Cited by
- 139
- References
- 11
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 7 · 2023: 9 · 2022: 6 · 2021: 14 · 2020: 13 · 2019: 2 · 2018: 5 · 2017: 9 · 2016: 6 · 2015: 9 · 2014: 11 · 2013: 9 · 2012: 6
- FWCI
- 2.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (087736)
- Royal Society
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- orbitofrontal cortex, anterior cingulate cortex, social behavior, emotions, excitotoxic lesions, aggression, social recognition memory, impulsive choice, decision-making, anxiety, Lister hooded rats
- MeSH terms
- Analysis of Variance, Animals, Behavior, Animal, Brain Mapping, Discrimination, Psychological, Emotions, Frontal Lobe, Memory, Reaction Time, Smell, Social Behavior, Rats
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
