Hippocampal lesions in rhesus monkeys disrupt emotional responses but not reinforcer devaluation effects
Abstract
Background Although the role of the hippocampus in emotional behavior has long been recognized, the extent to which the hippocampus plays a role in the regulation and expression of emotion in rhesus monkeys has not been systematically explored.Methods Rhesus monkeys (Macaca mulatta) with excitotoxic lesions of the hippocampal formation and unoperated control animals were assessed on two different types of emotional processing: defensive reactions to a potential predator (experiment 1) and ability to update the value of positive reinforcers, in this case food (experiment 2). Monkeys with aspiration lesions of the perirhinal cortex were also included in this study as an operated control group.Results In experiment 1, whereas both operated groups showed reduced latencies to retrieve food located near an innately fear-provoking stimulus, a fake snake, only monkeys with hippocampal lesions displayed reduced defensive reactions to the snake. In experiment 2, both operated groups performed as well as control animals when choosing objects flexibly based on the current value of a food.Conclusions These findings dissociate the hippocampus and perirhinal cortex in fear expression and specifically implicate the hippocampal formation in generating responses to stimuli that are potentially threatening.
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Damage to regions near the amygdala, such as entorhinal cortex, perirhinal cortex, or hippocampus, has no effect on the devaluation task.
“Likewise, damage to regions near the amygdala, such as the entorhinal cortex, perirhinal cortex, or hippocampus, have no effect (81, 82).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [81]
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“On this view, amygdala damage disrupts so-called devaluation effects because of its influence on processing of internal context, which is needed for the “value-updating” function.”
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“This can be investigated in tests that extend approach– avoidance conflict over time with no incentive to act quickly, such that approach latency has a different meaning than in our task (Chudasama et al., 2008, 2009).”
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“However, these findings conflict with studies of nonanxious rodents in which reductions in vHipp glutamate function are anxiolytic in ethological tests of anxiety (Barkus et al., 2010) and the anxiolytic effects of hippocampal lesions in nonanxious primates (Chudasama et al., 2008, 2009).”
BackgroundResultNeonatal hippocampal damage impairs specific food/place associations in adult macaques.
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“Repeated encounters with a threat stimulus in the absence of aversive outcomes typically leads to extinction of these defensive responses (Nelson et al., 2003; Izquierdo and Murray, 2004; Izquierdo et al., 2005; Chudasama et al., 2008), demonstrating adaptability in the face of threat versus safety.”
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BackgroundSelf-citationBahrami, S., Nordengen, K., Shadrin, A. A., Frei, O., van der Meer, D., Dale, A. M., Westlye, L. T., Andreassen, O. A., & Kaufmann, T. (2022) · Nature Communications · doi:10.1038/s41467-022-31086-w · Cited by 25 · see citing works
Incubation of food craving is independent of macronutrient composition
Darling, R. A., Dingess, P. M., Schlidt, K. C., Smith, E. M., & Brown, T. E. (2016) · Scientific Reports · doi:10.1038/srep30900 · Cited by 23 · see citing works
Pena, R. R., Medeiros, D. D. C., Guarnieri, L. D. O., GUERRA, J. B., Carvalho, V. R., Mendes, E. M. A. M., Pereira, G. S., & Moraes, M. F. D. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.08.058 · Cited by 21 · see citing works
“, 2004), the ventral 466 hippocampus is associated to a variety of emotional behaviors (Bannerman et 467 al., 2002; Chudasama et al., 2008; Kjelstrup et al., 2002; McHugh et al., 2004; 468 Pentkowski et al., 2006).”
BackgroundRaper, J., Wilson, M., Sánchez, M. M., Payne, C. D., & Bachevalier, J. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.11.018 · Cited by 21 · see citing works
“When faced with a potential threat, adult rodents and primates with hippocampal lesions exhibit less freezing/fear and more anxiety-like behaviors (Phillips & LeDoux, 1992; Chudasama, et al., 2008, 2009; Machado & Bachevalier, 2008; Buchanan, et al., 2009; Wang et al., 2013).”
BackgroundResultA role for hippocampal adult neurogenesis in shifting attention toward novel stimuli
Weeden, C. S. S., Mercurio, J. C., & Cameron, H. A. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112152 · Cited by 17 · see citing works
“Work in monkeys has shown that hippocampal lesions result in a general lack of interest in innately fear-provoking objects and decreased distraction by these objects when reaching over them for rewards [51,52].”
BackgroundYang, T., Bavley, R. L., Fomalont, K., Blomstrom, K. J., Mitz, A. R., Turchi, J. N., Rudebeck, P. H., & Murray, E. A. (2014) · Hippocampus · doi:10.1002/hipo.22294 · Cited by 14 · see citing works
“In addition, monkeys with excitotoxic lesions of the hippocampus were not impaired on VML, despite the same group being impaired in another domain (Chudasama et al., 2008).”
BackgroundSelf-citationKelly, S. J., Bernard, K., Muñoz, C., Lawrence, R. C., Thacker, J. S., Grillo, C. A., Piroli, G. G., & Reagan, L. P. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1301-x · Cited by 12 · see citing works
“…in cognitive tasks that are dependent upon the hippocampus (Beracochea et al. 2007), reinforcer devaluation and agerelated enhancement of taste aversion learning have both been suggested to be independent of hippocampal function (Chudasama et al. 2008; Manrique et al. 2007; Pickens et al. 2003).”
BackgroundScarf, D., Millar, J., Pow, N., & Colombo, M. (2014) · Behavioral Neuroscience · doi:10.1037/a0035487 · Cited by 11 · see citing works
“This finding is consistent with previous work demonstrating deficits in response inhibition in mammals after hippocampal lesions (Bannerman et al., 2002, 2003, 1999; Cheung & Cardinal, 2005; Chudasama et al., 2009, 2008; Richmond et al., 1999).”
ResultCharbonneau, J. A., Amaral, D. G., & Bliss‐Moreau, E. (2022) · Scientific Reports · doi:10.1038/s41598-022-08077-4 · Cited by 10 · see citing works
“, [1]) or the pharmacological blockade or activation of particular receptors (e.”
BackgroundThe role of puberty on physical and brain development: A longitudinal study in male Rhesus Macaques
Kovacs-Balint, Z. A., Raper, J., Richardson, R., Gopakumar, A., Kettimuthu, K., Higgins, M. K., Feczko, E., Earl, E., Ethun, K. F., Li, L., et al. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2023.101237 · Cited by 11 · see citing works
“cesses -amygdala (AMY), hippocampus (HIPPO), prefrontal cortex (PFC), and their functional connectivity (FC)- (Maren and Fanselow, 1997; Meunier et al., 1999; Ledoux, 2000; Izquierdo and Murray, 2004; Kalin et al., 2004; Phelps and Ledoux, 2005; Chudasama et al., 2008; Machado and Bachevalier, 2008; Brenhouse and Ande…”
Macaques fail to develop habit responses during extended training on a reinforcer devaluation task.
LaFlamme, E. M., Ahmed, F., Forcelli, P. A., & Málková, L. (2022) · Behavioral Neuroscience · doi:10.1037/bne0000503 · Cited by 9 · see citing works
Banik, S. P., Bagchi, D., Banerjee, P., Chakraborty, S., Bagchi, M., Bose, C., De, D., Saha, S., & Chakraborty, S. (2025) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2025.1603364 · Cited by 8 · see citing works
Busse, S., & Schwarting, R. K. W. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00118 · Cited by 8 · see citing works
Vicario-Feliciano, R. M., Murray, E. A., & Averbeck, B. B. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000211 · Cited by 9 · see citing works
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Neonatal perirhinal cortex lesions impair monkeys’ ability to modulate their emotional responses.
Ahlgrim, N. S., Raper, J., Johnson, E. C., & Bachevalier, J. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000208 · Cited by 6 · see citing works
“However, no correlation was found between a lack of habituation and memory performance (Chudasama et al., 2008).”
BackgroundEffects of systemic cholinergic antagonism on reinforcer devaluation in macaques
Waguespack, H. F., Málková, L., Forcelli, P. A., & Turchi, J. N. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.05.003 · Cited by 7 · see citing works
Neural signatures of experience-based improvements in deterministic decision-making
Tremel, J. J., Laurent, P. A., Wolk, D. A., Wheeler, M. E., & Fiez, J. A. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.08.023 · Cited by 8 · see citing works
Tremel, J. J., Ortiz, D. M., & Fiez, J. A. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.04.023 · Cited by 7 · see citing works
Duc, W. L., Butler, C., Argyropoulos, G. P. D., Chu, S., Hutcherson, C. A. C., Ruocco, A. C., Ito, R., & Lee, A. C. H. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003033 · Cited by 6 · see citing works
Schoenfeld, T. J., Smith, J. A., Sonti, A. N., & Cameron, H. A. (2020) · Hippocampus · doi:10.1002/hipo.23267 · Cited by 6 · see citing works
Amygdala lesions in rhesus monkeys fail to disrupt object choices based on internal context.
Rhodes, S. E. V., Charles, D. P., Howland, E. J., & Murray, E. A. (2012) · Behavioral Neuroscience · doi:10.1037/a0027229 · Cited by 5 · see citing works
Self-citationBusse, S., & Schwarting, R. K. W. (2015) · Neurotoxicity Research · doi:10.1007/s12640-015-9551-y · Cited by 4 · see citing works
Conway, P. B., Autore, L., Zamora, A. M., Harel, A., Wang, Z., Tavallaei, A. A., Winston, S. M., Luis, C. O. S., O’Leary, J. D., Brimble, M. A., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003391 · Cited by 3 · see citing works
Zinc function in childhood brain
Asindi, A. A., & Torty, C. (2022) · Nigerian Journal of Paediatrics · doi:10.4314/njp.v49i1.3 · Cited by 2 · see citing works
The role of orbitofrontal cortex in economic choice behavior
Padoa‐Schioppa, C., & Shi, W. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-820480-1.00046-2
- Authors
- Chudasama, Y., Wright, K. S., & Murray, E. A.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Chudasama, Yogita
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2008-06
- Volume
- 63
- Issue
- 11
- Pages
- 1084-1091
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W1986764568
- Cited by
- 65
- References
- 46
- Citations by year
- 2025: 3 · 2023: 3 · 2022: 6 · 2021: 2 · 2020: 3 · 2019: 5 · 2018: 2 · 2017: 4 · 2016: 6 · 2015: 2 · 2014: 4 · 2013: 4 · 2012: 2
- FWCI
- 2.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- hippocampus, hippocampal lesions, emotional behavior, fear expression, defensive reactions, perirhinal cortex, reinforcer devaluation, excitotoxic lesions, rhesus monkeys, threat detection
- MeSH terms
- Affective Symptoms, Animals, Behavior, Animal, Conditioning, Operant, Discrimination Learning, Hippocampus, Macaca mulatta, Male, Reaction Time, Reinforcement, Psychology, Reversal Learning, Satiation, Reproducibility of Results, Excitatory Amino Acid Agonists
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