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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Schmidt‐Daffy, M. (2012) · Transportation Research Part F Traffic Psychology and Behaviour · doi:10.1016/j.trf.2012.07.002 · Cited by 90
Examining the Role of the Human Hippocampus in Approach–Avoidance Decision Making Using a Novel Conflict Paradigm and Multivariate Functional Magnetic Resonance Imaging
O’Neil, E. B., Newsome, R. N., Li, I. H. N., Thavabalasingam, S., Ito, R., & Lee, A. C. H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1915-15.2015 · Cited by 88
“For example, converging lesion and electrophysiological evidence has revealed ventral HC involvement in ethological tests of anxiety such as the elevated plus maze, light/dark box, and open field, in which an animal is faced with a decision to explore a potentially dangerous or rewarding environment (Bannerman et al.,…”
Background
Hippocampal regulation of aversive memories
Goosens, K. A. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.04.003 · Cited by 96
“For example, hippocampal lesions reduce anxiety on tasks involving a choice between “safe” dark high-walled arms, or “risky” well-lit open arms [7,8,10,11].”
Persistent Adult Neuroimmune Activation and Loss of Hippocampal Neurogenesis Following Adolescent Ethanol Exposure: Blockade by Exercise and the Anti-inflammatory Drug Indomethacin
Vetreno, R. P., Lawrimore, C. J., Rowsey, P. J., & Crews, F. T. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00200 · Cited by 93
“Although not the focus of the current study, hippocampal neurogenesis is critically involved in cognitive and emotive function (Madsen et al., 2003; McHugh et al., 2004; Revest et al., 2009), and the loss of neurogenesis following AIE is associated with behavioral deficits in adulthood (Ehlers et…”
Background
Insulin-Like Growth Factor II Targets the mTOR Pathway to Reverse Autism-Like Phenotypes in Mice
Steinmetz, A. B., Stern, S. A., Kohtz, A. S., Descalzi, G., & Alberini, C. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2010-17.2017 · Cited by 90
“Thus, in line with a role of the hippocampus in social novelty memory but not in social interaction (McHugh et al., 2004; Felix-Ortiz and Tye, 2014; Hitti and Siegelbaum, 2014), the IGF-II effect only on social novelty memory required the selective role of hippocampal IGF-IIR but not IGF-IR.”
Background
Oxytocin and vasopressin in the rodent hippocampus
Cilz, N. I., Cymerblit‐Sabba, A., & Young, W. S. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12535 · Cited by 92
Sex Differences in the Development of the Rodent Corticolimbic System
Premachandran, H., Zhao, M., & Arruda-Carvalho, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.583477 · Cited by 96
Endocannabinoids, cannabinoids and the regulation of anxiety
Petrie, G. N., Nastase, A. S., Aukema, R. J., & Hill, M. N. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108626 · Cited by 91
Dorsal hippocampus involvement in delay fear conditioning depends upon the strength of the tone‐footshock association
Quinn, J. J., Wied, H. M., Ma, Q. D., Tinsley, M. R., & Fanselow, M. S. (2008) · Hippocampus · doi:10.1002/hipo.20424 · Cited by 84
“Similarly, McHugh et al. (2004) tested animals with either VH or DH lesions on a number of unconditional tests of anxiety.”
Molecular heterogeneity along the dorsal–ventral axis of the murine hippocampal CA1 field: a microarray analysis of gene expression
Leonardo, E. D., Richardson-Jones, J. W., Sibille, E. L., Kottman, A., & Hen, R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.082 · Cited by 84
Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety
McHugh, S. B., Fillenz, M., Lowry, J. P., Rawlins, J. N. P., & Bannerman, D. M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07497.x · Cited by 86
“Benzodiazepines reduce latency to enter the white section of the black ⁄ white alley (McHugh et al., 2004) and latency to eat in the neophobia test (Shephard & Estall, 1984).”
BackgroundMethodResultInfluentialSelf-citation
State-Dependent Alterations in Hippocampal Oscillations in Serotonin 1A Receptor-Deficient Mice
Gordon, J. A., Lacefield, C., Kentros, C. G., & Hen, R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1211-05.2005 · Cited by 81
“Recent studies have generally shown that the anxiety phenotype arises specifically from ventral hippocampal lesions (Kjelstrup et al., 2002; Bannerman et al., 2003; McHugh et al., 2004).”
Background
The role of the ventral dentate gyrus in anxiety-based behaviors
Weeden, C. S. S., Roberts, J. M., Kamm, A. M., & Kesner, R. P. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.12.002 · Cited by 80
Impaired spatial memory and enhanced long-term potentiation in mice with forebrain-specific ablation of the Stim genes
García-Alvarez, G., Shetty, M. S., Lu, B., Yap, K. A. F., Oh‐hora, M., Sajikumar, S., Bichler, Z., & Fivaz, M. L. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00180 · Cited by 79
“…mouse strains, also report clear dissociation of LTP and memory, thereby challenging the causal relationship between these two processes (Meiri et al., 1998; Migaud et al., 1998; Zamanillo et al., 1999; Pineda et al., 2004; Rutten et al., 2008; Kim et al., 2009; Dilekoz et al., 2015).”
Background
The anxiolytic-like effects of allopregnanolone vary as a function of intracerebral microinfusion site: the amygdala, medial prefrontal cortex, or hippocampus
Engin, E., & Treit, D. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282d28f6f · Cited by 83
Cross-species anxiety tests in psychiatry: pitfalls and promises
Bach, D. R. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01299-4 · Cited by 79
The ventral hippocampus, but not the dorsal hippocampus is critical for learned approach‐avoidance decision making
Schumacher, A., Vlassov, E., & Ito, R. (2015) · Hippocampus · doi:10.1002/hipo.22542 · Cited by 76
“…the elevated plus maze, light/dark box, successive alley and hyponeophagia (Bannerman et al., 2002; Kjelstrup et al., 2002; Bannerman et al., 2003; McHugh et al., 2004; Trivedi and Coover, 2004), and reduce unconditioned defensive behaviors induced by predatory odour stimuli (Pentkowski et al.,…”
Background
Exposure to an open-field arena increases c-Fos expression in a distributed anxiety-related system projecting to the basolateral amygdaloid complex
Hale, M. W., Hay-Schmidt, A., Mikkelsen, J. D., Poulsen, B. C., Shekhar, A., & Lowry, C. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.054 · Cited by 83
The Avian Hippocampal Formation and the Stress Response
Smulders, T. V. (2017) · Brain Behavior and Evolution · doi:10.1159/000477654 · Cited by 77
“Lesions of the temporal (but not the septal) hippocampus also have an anxiolytic effect [McHugh et al., 2004], although it depends on how anxiety is measured [Degroot and Treit, 2004].”
Background
Corticotropin releasing factor induces anxiogenic locomotion in trout and alters serotonergic and dopaminergic activity
Carpenter, R. E., Watt, M. J., Forster, G. L., Øverli, Ø., Bockholt, C., Renner, K. J., & Summers, C. H. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.07.012 · Cited by 74
“Together, these transmitters shape behavioral responses driven by anxiety primarily through action in limbic regions of the mammalian brain (Bannerman et al., 2003; Kalin et al., 2004; McHugh et al., 2004; Schweimer et al., 2005).”
Background
The expression of non-clustered protocadherins in adult rat hippocampal formation and the connecting brain regions
Kim, S., Mo, J., Han, S. B., Choi, S. Y., Han, S. B., Moon, B.-K., Rhyu, I. J., Sun, W., & Kim, H. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.027 · Cited by 76
Flexible spatial learning requires both the dorsal and ventral hippocampus and their functional interactions with the prefrontal cortex
Avigan, P. D., Cammack, K., & Shapiro, M. L. (2020) · Hippocampus · doi:10.1002/hipo.23198 · Cited by 73
Simvastatin prevents β-amyloid25–35-impaired neurogenesis in hippocampal dentate gyrus through α7nAChR-dependent cascading PI3K-Akt and increasing BDNF via reduction of farnesyl pyrophosphate
Wang, C., Chen, T., Li, G., Zhou, L., Sha, S., & Chen, L. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.05.020 · Cited by 75
Distinct ventral and dorsal hippocampus AP5 anxiolytic effects revealed in the elevated plus-maze task in rats
Häckl, L. P. N., & Carobrez, A. P. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.007 · Cited by 73
Dorsal hippocampal N-methyl-d-aspartate receptors underlie spatial working memory performance during non-matching to place testing on the T-maze
McHugh, S. B., Niewoehner, B., Rawlins, J. N. P., & Bannerman, D. M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.07.021 · Cited by 72
Self-citation
Levels of neurotrophic factors in the hippocampus and amygdala correlate with anxiety- and fear-related behaviour in C57BL6 mice
Yee, B. K., Zhu, S., Mohammed, A. H., & Feldon, J. (2006) · Journal of Neural Transmission · doi:10.1007/s00702-006-0548-9 · Cited by 77
“Second, the selective involvement of dorsal hippocampus seems contrary to the hypothesis that ventral hippocampus is preferentially involved in anxiety-related behaviour in the rat (Kjelstrup et al., 2003; Bannerman et al., 2004; McHugh et al., 2004).”
BackgroundMethodResult
Hippocampal neurogenesis: a biomarker for depression or antidepressant effects? Methodological considerations and perspectives for future research
Tanti, A., & Belzung, C. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1612-z · Cited by 75
“Moreover, in cases of a specific lesion of the ventral subregion, the lesion elicits modified anxiety-like behaviour in various situations such as novelty suppression of feeding (Bannerman et al. 2002; Burns et al. 1996; McHugh et al. 2004), exposure to predator-related stimuli (Blanchard et al.”
Background
Dissociable effects of hippocampus lesions on expression of fear and trace fear conditioning memories in rats
Burman, M. A., Starr, M. J., & Gewirtz, J. C. (2005) · Hippocampus · doi:10.1002/hipo.20137 · Cited by 69
Amygdala Lesions Reduce Anxiety-like Behavior in a Human Benzodiazepine-Sensitive Approach–Avoidance Conflict Test
Korn, C. W., Vunder, J., Miró, J., Fuentemilla, L., Hurlemann, R., & Bach, D. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.01.018 · Cited by 60
“However, rodent amygdala lesions did not affect innate anxiety-like behaviors and rendered behavior in AAC with overt rewards more cautious rather than less cautious (23).”
Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning
Kenney, J. W., Raybuck, J. D., & Gould, T. J. (2012) · Hippocampus · doi:10.1002/hipo.22003 · Cited by 70
“anxiolytic, whereas lesions of the dorsal hippocampus tend to be without effect on measures of anxiety (Bannerman et al., 2002, 2003; Kjelstrup et al., 2002; McHugh et al., 2004).”
Excitotoxic lesions in the central nucleus of the amygdala attenuate stress-induced anxiety behavior
Ventura‐Silva, A. P., Melo, A., Ferreira, A. C., Carvalho, M. M., Campos, F. L., Sousa, N., & Pêgo, J. M. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00032 · Cited by 66
“In further support of this hypothesis is the fact that a lesion in CeA did not affect anxiety-behavior in baseline conditions, which is in line with previous observations by other labs (Möller et al., 1997; McHugh et al., 2004; Cai et al., 2012).”
Result
Opposing alterations in anxiety and species-typical behaviours in serotonin transporter overexpressor and knockout mice
Line, S. J., Barkus, C., Coyle, C., Jennings, K. A., Deacon, R. M. J., Lesch, K., Sharp, T., & Bannerman, D. M. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2010.08.005 · Cited by 65
“Despite this, it is notable that all the anxiety tasks described here are sensitive to lesions of the ventral hippocampus (Bannerman et al., 2003; Bannerman et al., 2004; McHugh et al., 2004), whereas they are not affected by amygdala lesions (Treit et al.”
Self-citation
A role for dorsal and ventral hippocampus in inter-temporal choice cost-benefit decision making.
McHugh, S. B., Campbell, T. G., Taylor, A. M., Rawlins, J. N. P., & Bannerman, D. M. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.1.1 · Cited by 64
“Complete (cHPC), dorsal (dHPC), and ventral (vHPC) hippocampal lesions were highly reproducible and highly selective and consistent with previous studies in this laboratory (Bannerman, Grubb, Deacon, Yee, Feldon, & Rawlins, 2003; Bannerman, et al. 1999; Deacon et al., 2002; McHugh et al., 2004).”
BackgroundResultInfluentialSelf-citation
Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamstersPreprint
Markham, C. M., Taylor, S. L., & Huhman, K. L. (2010) · Learning & Memory · doi:10.1101/lm.1633710 · Cited by 65
“behaviors in a social interaction test (McHugh et al. 2004), and an impairment of risk assessment behaviors (a behavioral index of anxiety) in rats confronted with an ethologically relevant threat stimulus (Pentkowski et al.”
Background
The role of antioxidant properties of Nardostachys jatamansi in alleviation of the symptoms of the chronic fatigue syndrome
Lyle, N., Gomes, A., Sur, T. K., Munshi, S., Paul, S., Chatterjee, S., & Bhattacharyya, D. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.005 · Cited by 64
Remembering Preservation in Hippocampal Amnesia
Clark, I. A., & Maguire, E. A. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033739 · Cited by 68
“…patients accords with findings described in the animal literature, suggesting a distinction between the brain circuitry involved in fear, which is thought to be processed by the amygdala, and anxiety, which is thought to be mediated by the hippocampus (Gray & McNaughton 2003, McHugh et al. 2004).”
Bone Morphogenetic Protein Signaling in the Developing Telencephalon Controls Formation of the Hippocampal Dentate Gyrus and Modifies Fear-Related Behavior
Caronia, G., Wilcoxon, J., Feldman, P., & Grove, E. A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0550-10.2010 · Cited by 63
“General activity levels were tested first because the shortened digits of double mutant mice could affect locomotion and because neonatal hippocampal ablation may cause hyperactivity (McHugh et al., 2004).”
Background
Environmental enrichment induces neuroplastic changes in middle age female BalbC mice and increases the hippocampal levels of BDNF, p-Akt and p-MAPK1/2
Ramírez-Rodríguez, G. B., Ocaña-Fernández, M. D. Á., Vega‐Rivera, N. M., Torres-Pérez, O. M., Gómez‐Sánchez, A., Estrada-Camarena, E. M., & Ortiz-López, L. I. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.026 · Cited by 64

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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