Cited by 384Memory and Neural MechanismsStress Responses and CortisolAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

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Amygdala and Ventral Hippocampus Contribute Differentially to Mechanisms of Fear and Anxiety.

McHugh, S. B., Deacon, R. M. J., Rawlins, J. N. P., Bannerman, David M.·2004·Behavioral Neuroscience

DOI 10.1037/0735-7044.118.1.63

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Abstract

Cytotoxic ventral hippocampal lesions produced anxiolytic effects on 4 ethologically based, unconditioned tests of anxiety in the rat (hyponeophagia, black/white 2-compartment box test, a successive alleys test that represents a modified version of the elevated plus-maze, and a social interaction test). Dorsal hippocampal lesions did not produce anxiolytic effects on these tests, suggesting a distinct specialization of function within the hippocampus. Furthermore, the effects of ventral hippocampal lesions were also distinct from those of amygdala lesions. This suggests that the effects of ventral hippocampal lesions are not simply due to direct or indirect effects on the amygdala, and that these 2 brain areas contribute differentially to a brain system (or systems) associated with the processing of fearful and/or anxiogenic stimuli.

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Anxiolytic effects of Enterococcus faecalis 2001 on a mouse model of colitis
Takahashi, K., Tsuji, M., Nakagawasai, O., Miyagawa, K., Kurokawa, K., Mochida-Saito, A., Iwasa, M., Iwasa, H., Suzuki, S., Takeda, H., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-62309-3 · Cited by 11
Specific sub-regions along the longitudinal axis of the hippocampus mediate antidepressant-like behavioral effects
Levone, B. R., Moloney, G. M., Cryan, J. F., & O’Leary, O. F. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100331 · Cited by 10
Stressor-Induced Increases in Circulating, but Not Colonic, Cytokines Are Related to Anxiety-like Behavior and Hippocampal Inflammation in a Murine Colitis Model
Maltz, R. M., Marte-Ortiz, P., Rajasekera, T. A., Loman, B. R., Gur, T., & Bailey, M. T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042000 · Cited by 10
“In addition to its roles in the intestine, IL-17 can also affect the brain and behavior [23,24,29,30].”
Background
Role of the glycoprotein thorns in anxious effects of rabies virus: Evidence from an animal study
Ghassemi, S., Pourbadie, H. G., Prehaud, C. J. N., Lafon, M., & Sayyah, M. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.05.001 · Cited by 10
Neural correlates of learning and memory are altered by early-life stress
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“…in excitatory/inhibitory balance remains to be studied but could be important for maintaining the sparsity of the engram (Chen et al., 2022; Guo et al., 2018; Pignatelli et al., 2019; Ramsaran et al., 2023), a key property of these memory ensembles (Josselyn et al., 2015; Tonegawa et al., 2015).”
Effects of early noise exposure on hippocampal-dependent behaviors during adolescence in male rats: influence of different housing conditions
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Paraoxon-induced damage in rat hippocampus is associated with alterations in the expression of apoptosis-related proteins
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Regional dissociation of paradigm-specific synapse remodeling during memory consolidation in the adult rat dentate gyrus
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Measures of anxiety, amygdala volumes, and hippocampal scopolamine phMRI response in elderly female rhesus macaques
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“Consistent with differential roles of the amygdala and hippocampus in regulation of anxiety, hippocampal and amygdala lesions in rodents and nonhuman primates caused distinct alterations in measures of anxiety (Machado and Bachevalier, 2008; McHugh et al., 2004).”
Complexity of Compensatory Effects in Nrf1 Knockdown: Linking Undeveloped Anxiety-Like Behavior to Prevented Mitochondrial Dysfunction and Oxidative Stress
Khalifeh, S., Oryan, S., Khodagholi, F., Digaleh, H., Shaerzadeh, F., Maghsoudi, N., & Zarrindast, M. (2015) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-015-0236-0 · Cited by 9
The entorhinal cortex, but not the dorsal hippocampus, is necessary for single‐cue latent learning
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“This supports previous research, which demonstrate that a functional VH is necessary for the use of internal motivational states to express appropriate behaviors (Bannerman et al., 2002, 2003; Kjelstrup et al., 2002; McHugh et al., 2004; Trivedi and Coover, 2004).”
Result
Neonatal amphetamine exposure and hippocampus-mediated behaviors
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Septotemporal variation in modulation of synaptic transmission, paired-pulse ratio and frequency facilitation/depression by adenosine and GABA B receptors in the rat hippocampus
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“…al., 1994; Maurer et al., 2005; Moser et al., 1993), while the ventral hippocampus has been linked to anxiety-related behaviors (Bannerman et al., 2002; Kjelstrup et al., 2002; Pentkowski et al., 2006), stress-induced disfunctions and social interactions (McHugh et al., 2004; Okuyama et al., 2016).”
Background
Effects of hypomagnetic field on adult hippocampal neurogenic niche and neurogenesis in mice
Luo, Y., Zhan, A., Fan, Y., & Tian, L. (2022) · Frontiers in Physics · doi:10.3389/fphy.2022.1075198 · Cited by 8
Morphine improved stress-induced amnesia and anxiety through interacting with the ventral hippocampal endocannabinoid system in rats
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Beta-band modulation in the human hippocampus during a conflict response task
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Hypo-Anxious Phenotype of Adolescent Offspring Prenatally Exposed to LPS Is Associated with Reduced mGluR5 Expression in Hippocampus
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“An excitotoxic lesion in one of these two cerebral structures produces anxiolytic effects [35].”
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Neonatal amygdala lesions: Co-occuring impact on social/fear-related behavior and cocaine sensitization in adult rats.
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Adolescent methamphetamine exposure drives neuroinflammation and aberrant neurogenesis linked to anxiety and cognitive impairments in adult mice
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Translocator protein ligand, YL-IPA08, attenuates lipopolysaccharide-induced depression-like behavior by promoting neural regeneration
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Alterations between high and low-avoidance lines of Hatano rats in learning behaviors, ultrasonic vocalizations, and histological characteristics in hippocampus and amygdala
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Effects of 2.45 GHz Non-Ionizing Radiation on Anxiety-Like Behavior, Gene Expression, and Corticosterone Level in Male Rats
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Over-expression of δC-DCLK-short in mouse brain results in a more anxious behavioral phenotype
Schenk, G. J., Veldhuisen, B., Wedemeier, O., McGown, C. C., Schouten, T. G., Oitzl, M. S., de Kloet, E. R., & Vreugdenhil, E. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.002 · Cited by 7
Some Biobehavioral Insights into Persistent Effects of Emotional Trauma
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Hippocampal damage disrupts the latent decision-making processes underlying approach-avoidance conflict processing in humans
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Laterality dissociation of ventral hippocampus inhibition in learning and memory, glial activation and neural arborization in response to chronic stress in male Wistar rats
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Memantine Disrupts Motor Coordination through Anxiety-like Behavior in CD1 Mice
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Short photoperiod modulates behavior, cognition and hippocampal neurogenesis in male Japanese quail
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Excess cerebellar granule neurons induced by the absence of p75NTR during development elicit social behavior deficits in mice
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“The hippocampus and the cerebellum are both involved in anxiety behaviors (Bannerman et al., 2004; McHugh et al., 2004; Engin and Treit, 2007; Phillips, 2015; MorenoRius, 2018), therefore the elevated anxiety observed only in the conditional p75Atoh1-Cre might be due to developmental defects in the hippocampus induced…”
Background
Molecular mechanisms of D-cycloserine in facilitating fear extinction: insights from RNAseq
Malan‐Müller, S., Fairbairn, L., Daniels, W. M. U., Dashti, M. J. S., Oakeley, E. J., Altorfer, M., Kidd, M., Seedat, S., Gamieldien, J., & Hemmings, S. M. J. (2015) · Metabolic Brain Disease · doi:10.1007/s11011-015-9727-4 · Cited by 5
“1976; Quirk andMueller 2008) and processing of emotional behaviour (Kjelstrup et al. 2002; Bannerman et al. 2004;McHugh et al. 2004).”
BackgroundMethod
Effects of spontaneous recurrent seizures on cognitive function via modulation of SNAREs expression
Yu, H., Yang, X., Tang, X. W., & Tang, R. (2017) · International Journal of Neuroscience · doi:10.1080/00207454.2017.1387115 · Cited by 6
Inactivation of the ventral hippocampus facilitates the attenuation of odor neophobia in rats
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The role of microRNAs in the therapeutic action of D-cycloserine in a post-traumatic stress disorder animal model
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“The hippocampus also contains high levels of NMDARs and plays a pivotal role in fear extinction retention processes (Fredrikson et al., 1976; Quirk and Mueller 2008) and processing of emotional behaviour (Kjelstrup et al., 2002; Bannerman et al., 2004; McHugh et al., 2004).”
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Traumatic brain injury-induced anxiety: Injury and plasticity of the central noradrenergic system
Tsuda, S., Hou, J., Thompson, F. J., & Bose, P. (2025) · Experimental Neurology · doi:10.1016/j.expneurol.2025.115182 · Cited by 6
The Role of Neurogenesis in Anxiety Disorders
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Development of a Minipig Model of BINT From Blast Exposure Using a Repeatable Mobile Shock Expansion Tube
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Distinct effects of AMPAR subunit depletion on spatial memory
Eltokhi, A., Bertocchi, I., Rozov, A. V., Jensen, V., Borchardt, T., Taylor, A. M., Proenca, C. C., Rawlins, J. N. P., Bannerman, D. M., & Sprengel, R. (2023) · iScience · doi:10.1016/j.isci.2023.108116 · Cited by 6
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The effect of 5-HT4 serotonin receptors in the CA3 hippocampal region on D-AP5-induced anxiolytic-like effects: Isobolographic analyses
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“, 2006), social interactions, stress-induced disfunctions (McHugh et al., 2004; Okuyama et al., 2016), but also with positive emotions (Yang and Wang, 2017).”
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Effects of two selective 5-HT2C receptor-acting compounds into the ventral hippocampus of rats exposed to the elevated plus-maze.
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BMAL1-mediated circadian–ferroptosis crosstalk drives neuronal vulnerability after TBI
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Induced expression of rabies glycoprotein in the dorsal hippocampus enhances hippocampal dependent memory in a rat model of Alzheimer’s disease
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Authors: McHugh, S. B., Deacon, R. M. J., Rawlins, J. N. P., & Bannerman, D. M.
Affiliations: University of Oxford (GB)
ORCID: McHugh, S. B.
Bannerman, David M.
Venue: Behavioral Neuroscience
Publisher: American Psychological Association (APA)
Published: 2004
Volume: 118
Issue: 1
Pages: 63-78
ISSN: 0735-7044 (ISSN-L)
1939-0084
DOI: 10.1037/0735-7044.118.1.63
OpenAlex: W2076874426
Cited by: 384
References: 106
Citations by year: 2026: 10 · 2025: 9 · 2024: 17 · 2023: 8 · 2022: 19 · 2021: 27 · 2020: 17 · 2019: 12 · 2018: 21 · 2017: 30 · 2016: 11 · 2015: 24 · 2014: 22 · 2013: 18 · 2012: 21
FWCI: 8.95
Type: journal article
Language: en
Open access: closed
Locations: Behavioral Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (087736)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
Keywords: amygdala, ventral hippocampus, dorsal hippocampus, fear, anxiety, anxiolytic effects, lesion studies, elevated plus maze, social interaction
MeSH terms: Amygdala, Animals, Anxiety, Fear, Hippocampus, Male, Rats

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Amygdala and Ventral Hippocampus Contribute Differentially to Mechanisms of Fear and Anxiety.

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