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.

doi:10.1037/0735-7044.118.1.63

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

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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Neurobiology of Affiliative Behavior in Nonhuman Primates**Partial support for this research has been obtained from the Research Council, Rutgers University; Veterans Administration Research funds; the Harry Frank Guggenheim Foundation, New York; and The Epilepsy Foundation of America. We thank Dr. M.J. Raleigh for commenting on an earlier version of this chapter and Ms. Sylva Grossman for typing the manuscript.
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The Professions
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(1998) · doi:10.1002/(sici)1098-1063(1998)8:6

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Regional dissociations within the hippocampus-memory and anxiety
Bannerman, D. M., Rawlins, J. N. P., McHugh, S. B., Deacon, R. M. J., Yee, B. K., Bast, T., Zhang, W.-N., Pothuizen, H. H. J., & Feldon, J. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.03.004 · Cited by 1,462 · see citing works
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Adult hippocampal neurogenesis in depression
Sahay, A., & Hen, R. (2007) · Nature Neuroscience · doi:10.1038/nn1969 · Cited by 1,206 · see citing works
“, whereas those of the ventral hippocampus affect anxiety and have no effect on spatial learnin”
Background
Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear
Sierra-Mercado, D., Padilla-Coreano, N., & Quirk, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.184 · Cited by 1,190 · see citing works
“It has been previously shown that vHPC lesions reduce anxiety (McHugh et al., 2004), but this is unlikely to explain reduced freezing given that we observed no effect of vHPC inactivation in our measure of anxiety.”
Hippocampal synaptic plasticity, spatial memory and anxiety
Bannerman, D. M., Sprengel, R., Sanderson, D. J., McHugh, S. B., Rawlins, J. N. P., Monyer, H., & Seeburg, P. H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3677 · Cited by 688 · see citing works
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Alcohol: Effects on Neurobehavioral Functions and the Brain
Oscar-Berman, M., & Marinković, K. (2007) · Neuropsychology Review · doi:10.1007/s11065-007-9038-6 · Cited by 619 · see citing works
“2002; Gray and McNaughton 2000), there is mounting evidence that the ventral hippocampus is part of a brain system associated with fear and/or anxiety (Bannerman et al. 2004; Kjelstrup et al. 2002; McHugh et al. 2004).”
Background
BLA to vHPC inputs modulate anxiety-related behaviors
Felix-Ortiz, A. C., Beyeler, A., Seo, C., Leppla, C. A., Wildes, C. P., & Tye, K. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.016 · Cited by 592 · see citing works
“One distal amygdalar projection target implicated in anxietyrelated behaviors is the ventral hippocampus (vHPC; File and Gonzalez, 1996; McHugh et al., 2004; Richardson et al., 2004).”
Background
Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior
Felix-Ortiz, A. C., & Tye, K. M. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4257-13.2014 · Cited by 473 · see citing works
“Lesion studies provided the first evidence of an involvement of the vHPC in social interaction (Cadogan et al., 1994; Deacon et al., 2002; McHugh et al., 2004) and defensive behaviors (Pentkowski et al.”
Background
Antidepressant Drug Treatment Modifies the Neural Processing of Nonconscious Threat Cues
Harmer, C. J., Mackay, C. E., Reid, C. B., Cowen, P. J., & Goodwin, G. M. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.015 · Cited by 450 · see citing works
Are There Neural Gender Differences in Online Trust? An fMRI Study on the Perceived Trustworthiness of eBay Offers1
Riedl, Hubert, M., & Kenning, P. (2010) · MIS Quarterly · doi:10.2307/20721434 · Cited by 354 · see citing works
Hippocampal Cytogenesis Correlates to Escitalopram-Mediated Recovery in a Chronic Mild Stress Rat Model of Depression
Jayatissa, M. N., Bisgaard, C. F., Tingström, A., Papp, M., & Wiborg, O. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301041 · Cited by 348 · see citing works
“Rat studies indicate that the ventral hippocampal formation is involved in anxiety (Alves et al, 2004) and that the ventral hippocampal formation and amygdala contribute distinctly to brain systems processing anxiety and/or fear (Mchugh et al, 2004).”
Background
Adult microbiota‐deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus
Luczynski, P., Whelan, S. O., O'SULLIVAN, C. T. D., Clarke, G. A., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13291 · Cited by 345 · see citing works
“In addition to its role in anxiety (Deacon et al., 2002; Kjelstrup et al., 2002; Bannerman et al., 2004; McHugh et al., 2004), the ventral hippocampus is involved in sociability, with hippocampal lesions leading to abnormal responses engagement in social situations (Cadogan et al., 1994; Machado &…”
Background
Prenatal Restraint Stress Generates Two Distinct Behavioral and Neurochemical Profiles in Male and Female Rats
Zuena, A. R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G., Morley‐Fletcher, S., Chiodi, V., Spagnoli, L. G., Gradini, R., Catalani, A., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002170 · Cited by 339 · see citing works
Hippocampal NMDA receptors and anxiety: At the interface between cognition and emotion
Barkus, C., McHugh, S. B., Sprengel, R., Seeburg, P. H., Rawlins, J. N. P., & Bannerman, D. M. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.10.014 · Cited by 328 · see citing works
Self-citation
Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior
Crews, F. T., Vetreno, R. P., Broadwater, M., & Robinson, D. L. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.012138 · Cited by 332 · see citing works
Adult Neurogenesis: Beyond Learning and Memory
Cameron, H. A., & Glover, L. R. (2014) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015006 · Cited by 302 · see citing works
Neurogenesis and affective disorders
Samuels, B. A., & Hen, R. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07614.x · Cited by 286 · see citing works
“have supported this hypothesis (Moser et al., 1993, 1995; Kjelstrup et al., 2002; McHugh et al., 2004).”
Result
The role of hippocampus in anxiety: intracerebral infusion studies
Engin, E., & Treit, D. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282de7929 · Cited by 267 · see citing works
“…weak anxiolytic-like effects on animals’ untrained anxiety reactions, compared with lesions of the ventral hippocampus, which produce relatively robust anxiolytic-like effects (Kjelstrup et al., 2002; Degroot and Treit, 2004; McHugh et al., 2004; Bertoglio et al., 2006; Pentkowski et al., 2006).”
Background
Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats
Pentkowski, N. S., Blanchard, D. C., Lever, C., Litvin, Y., & Blanchard, R. J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04754.x · Cited by 244 · see citing works
“…in variations of the EPM, SPBT, social interaction and hyponeophagia tests (Kjelstrup et al., 2002; Bannerman et al., 2003; Degroot & Treit, 2004; McHugh et al., 2004; Trivedi & Coover, 2004), with these effects resembling the anxiolytic effects induced by benzodiazepines on many of the same…”
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Bidirectional Control of Anxiety-Related Behaviors in Mice: Role of Inputs Arising from the Ventral Hippocampus to the Lateral Septum and Medial Prefrontal Cortex
Parfitt, G. M., Nguyen, R., Bang, J. Y., Aqrabawi, A. J., Tran, M. M., Seo, D. K., Richards, B. A., & Kim, J. C. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.56 · Cited by 229 · see citing works
“The successive alleys (SUA) apparatus consists of four successive linearly connected alleys (alley 1–4) (Deacon, 2013; McHugh et al, 2004).”
Background
Hippocampal—diencephalic—cingulate networks for memory and emotion: an anatomical guide
Bubb, E. J., Kinnavane, L., & Aggleton, J. P. (2017) · Brain and Neuroscience Advances · doi:10.1177/2398212817723443 · Cited by 234 · see citing works
“…it is supposed that the functions of the anterior hippocampus are biased towards emotional states, including anxiety, while the posterior hippocampus is more critical for mnemonic functions (Aggleton, 2012; McHugh et al., 2004; O’Mara et al., 2001; Ranganath and Ritchey, 2012; Small et al., 2011).”
Contribution of Hippocampal and Extra-Hippocampal NR2B-Containing NMDA Receptors to Performance on Spatial Learning Tasks
von Engelhardt, J., Doganci, B., Jensen, V., Hvalby, Ø., Göngrich, C., Taylor, A., Barkus, C., Sanderson, D. J., Rawlins, J. N. P., Seeburg, P. H., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.039 · Cited by 250 · see citing works
Self-citation
Lesions to the <scp>CA</scp>2 region of the hippocampus impair social memory in mice
Stevenson, E. L., & Caldwell, H. K. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12689 · Cited by 222 · see citing works
“…of the hippocampus is important for normal social behaviors, including social memory, in animal models (Ely et al., 1977; Maaswinkel et al., 1996; McHugh et al., 2004; Uekita & Okanoya, 2011; Hitti & Siegelbaum, 2014; Pagani et al., 2014), and may be important across species, including humans.”
Influential
Anxiety, memory impairment, and locomotor dysfunction caused by a mutant thyroid hormone receptor α1 can be ameliorated by T3 treatmentPreprint
Venero, C., Guadaño‐Ferraz, A., Herrero, A. I., Nordström, K., Manzano, J., de Escobar, G. M., Bernal, J., & Vennström, B. (2005) · Genes & Development · doi:10.1101/gad.346105 · Cited by 222 · see citing works
“The hippocampus is well known to play a role in emotion and fearor anxiety-related behavior (LeDoux 2000; McHugh et al. 2004).”
Background
The Distribution of Toxoplasma gondii Cysts in the Brain of a Mouse with Latent Toxoplasmosis: Implications for the Behavioral Manipulation Hypothesis
Berenreiterová, M., Jaroslav Flegr, A., Kuběna, A. A., & Němec, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028925 · Cited by 216 · see citing works
“, [72–74]), importantly including cat-odor exposure [75].”
Neurogenesis along the septo-temporal axis of the hippocampus: Are depression and the action of antidepressants region-specific?
Tanti, A., & Belzung, C. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.017 · Cited by 220 · see citing works
Neuroanatomical Substrates of Rodent Social Behavior: The Medial Prefrontal Cortex and Its Projection Patterns
Ko, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00041 · Cited by 212 · see citing works
“The vHPC also has robust and reciprocal connections with the amygdala that are important for the expression of social behaviors in rodents (Cadogan et al., 1994; Deacon et al., 2002; Kjelstrup et al., 2002; Bannerman et al., 2004b; McHugh et al., 2004; Kheirbek et al., 2013).”
Background
Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus
Niewoehner, B., Single, F. N., Hvalby, Ø., Jensen, V., Borgloh, S. M. Z. A., SEEBURG, P. H., Rawlins, J. N. P., Sprengel, R., & Bannerman, D. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05312.x · Cited by 209 · see citing works
“…of the hippocampus, particularly its ventral portion, in anxiety (Richmond et al., 1999; Gray & McNaughton, 2000; Kjelstrup et al., 2002; Bannerman et al., 2004; McHugh et al., 2004), although this reduced anxiety phenotype was not observed on the other tests of emotionality that were conducted.”
BackgroundSelf-citation
Amygdalar and hippocampal substrates of anxious temperament differ in their heritability
Oler, J. A., Fox, A. S., Shelton, S. E., Rogers, J., Dyer, T. D., Davidson, R. J., Shelledy, W., Oakes, T. R., Blangero, J., & Kalin, N. H. (2010) · Nature · doi:10.1038/nature09282 · Cited by 208 · see citing works
Ventral hippocampal muscimol disrupts context‐specific fear memory retrieval after extinction in rats
Hobin, J. A., Ji, J.-Z., & Maren, S. (2006) · Hippocampus · doi:10.1002/hipo.20144 · Cited by 211 · see citing works
“While data do not speak directly to the role of the ventral hippocampus in grooming, data do show an increase in measures of social interaction, which include social grooming (Bannerman et al., 2002; McHugh et al., 2004).”
Background
Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study
Bergström, A., Jayatissa, M. N., Mørk, A., & Wiborg, O. (2007) · Brain Research · doi:10.1016/j.brainres.2007.12.025 · Cited by 196 · see citing works
Hippocampal lesions, species-typical behaviours and anxiety in mice
Deacon, R. M. J., & Rawlins, J. N. P. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.027 · Cited by 193 · see citing works
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Human Hippocampus Arbitrates Approach-Avoidance Conflict
Bach, D. R., Guitart‐Masip, M., Packard, P. A., Miró, J., Falip, M., Fuentemilla, L., & Dolan, R. J. (2014) · Current Biology · doi:10.1016/j.cub.2014.01.046 · Cited by 179 · see citing works
“In these, a key behavioral assay comprises passive avoidance of potential threat and inhibition, both thought to be controlled by ventral hippocampus [2–6].”
Anxiety and Alzheimer’s disease: Behavioral analysis and neural basis in rodent models of Alzheimer’s-related neuropathology
Pentkowski, N. S., Rogge-Obando, K., Donaldson, T. N., Bouquin, S. J., & Clark, B. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.005 · Cited by 169 · see citing works
Testosterone's Analgesic, Anxiolytic, and Cognitive-Enhancing Effects May Be Due in Part to Actions of Its 5α-Reduced Metabolites in the Hippocampus.
Edinger, K. L., & Frye, C. A. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1352 · Cited by 175 · see citing works
Conceptual framework for the etiology of alcoholism: a “kindling”/stress hypothesis
Breese, G. R., Overstreet, D. H., & Knapp, D. J. (2005) · Psychopharmacology · doi:10.1007/s00213-004-2016-2 · Cited by 167 · see citing works
“Therefore, the conditioned fear inferred from the CER study may not share overlapping sensitization with brain circuits/regions supporting anxiety (McHugh et al. 2004; Walker et al. 2003).”
Background
The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making
Rudebeck, P. H., Bannerman, D. M., & Rushworth, M. F. S. (2008) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.8.4.485 · Cited by 172 · see citing works
“When presented with this situation, control rats usually spend a large amount of time socially interacting, exploring, and sniffing the other rat, whereas aggressive behaviors, such as biting and upright boxing, account for only a small amount of the time spent (Bannerman et al., 2002; McHugh, Deacon, Rawlins, & Banne…”
BackgroundSelf-citation
The role of the hippocampus in approach-avoidance conflict decision-making: Evidence from rodent and human studies
Ito, R., & Lee, A. C. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.07.039 · Cited by 173 · see citing works
The role of interleukin (IL)‐17 in anxiety and depression of patients with rheumatoid arthritis
Yang, L. I. U., Ho, R., & Mak, A. (2011) · International Journal of Rheumatic Diseases · doi:10.1111/j.1756-185x.2011.01673.x · Cited by 167 · see citing works
Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning
Vetreno, R. P., & Crews, F. T. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00035 · Cited by 166 · see citing works
Testosterone's anti-anxiety and analgesic effects may be due in part to actions of its 5α-reduced metabolites in the hippocampus
Edinger, K. L., & Frye, C. A. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.11.001 · Cited by 152 · see citing works
Building and Burying Fear Memories in the Brain
Maren, S. (2005) · The Neuroscientist · doi:10.1177/1073858404269232 · Cited by 160 · see citing works
Algorithms for survival: a comparative perspective on emotions
Bach, D. R., & Dayan, P. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.35 · Cited by 144 · see citing works
Optogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150 · see citing works
The Ventral Hippocampus Supports a Memory Representation of Context and Contextual Fear Conditioning: Implications for a Unitary Function of the Hippocampus.
Rudy, J. W., & Matus-Amat, P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.154 · Cited by 147 · see citing works
Distinct contributions of frontal areas to emotion and social behaviour in the rat
Rudebeck, P. H., Walton, M. E., Millette, B. H. P., Shirley, E., Rushworth, M. F. S., & Bannerman, D. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05844.x · Cited by 139 · 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-citation
Optogenetic dissection of neural circuits underlying emotional valence and motivated behaviors
Nieh, E. H., Kim, S., Namburi, P., & Tye, K. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.11.001 · Cited by 129 · see citing works
“While both the prefrontal cortex and the hippocampus are reciprocally connected with the amygdala, they have been noted to have distinct functions (Kim et al., 1993; Garcia et al., 1999, 1999; Frankland et al., 2004; McHugh et al., 2004; Frankland and Bontempi, 2005; Herry et al., 2008).”
Background
Animal to human translational paradigms relevant for approach avoidance conflict decision making
Kirlić, N., Young, J. W., & Aupperle, R. L. (2017) · Behaviour Research and Therapy · doi:10.1016/j.brat.2017.04.010 · Cited by 128 · see citing works
Further evidence that anxiety and memory are regionally dissociated within the hippocampus
Bertoglio, L. J., Joca, S. R. L., & Guimarães, F. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.021 · Cited by 128 · see citing works
Serotonin receptor expression along the dorsal–ventral axis of mouse hippocampus
Tanaka, K. F., Samuels, B. A., & Hen, R. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0038 · Cited by 124 · see citing works
Opposite monosynaptic scaling of BLP–vCA1 inputs governs hopefulness- and helplessness-modulated spatial learning and memory
Yang, Y., Wang, Z.-H., Jin, S., Gao, D., Liu, N., Chen, S., Zhang, S., Liu, Q., Liu, E., Wang, X., et al. (2016) · Nature Communications · doi:10.1038/ncomms11935 · Cited by 111 · see citing works
“Although the ventral hippocampus seems more concerned with emotions, such as anxiety and fear 44 , studies also show its involvement in learning and memory.”
Inflammation and vascular remodeling in the ventral hippocampus contributes to vulnerability to stress
Pearson-Leary, J., Eacret, D., Chen, R. J., Takano, H., Nicholas, B., & Bhatnagar, S. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.122 · Cited by 114 · see citing works
Impulsive choice in hippocampal but not orbitofrontal cortex‐lesioned rats on a nonspatial decision‐making maze task
Mariano, T. Y., Bannerman, D. M., McHugh, S. B., Preston, T. J., Rudebeck, P. H., Rudebeck, S. R., Rawlins, J. N. P., Walton, M. E., Rushworth, M. F. S., Baxter, M. G., et al. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06837.x · Cited by 107 · see citing works
“Previous studies in the laboratory have shown that both HPC-lesioned (Bannerman et al., 2002, 2003; Deacon et al., 2002; McHugh et al., 2004), and OFC-lesioned (Rudebeck et al., 2007) rats are quicker to eat the food in these tests than are controls.”
ResultSelf-citation
Thymoquinone produced antianxiety-like effects in mice through modulation of GABA and NO levels
Gilhotra, N., & Dhingra, D. (2011) · Pharmacological Reports · doi:10.1016/s1734-1140(11)70577-1 · Cited by 109 · see citing works
“Nitric oxide synthase (NOS) is localized in brain regions involved with anxiety, such as hypothalamus, amygdala and hippocampus [37, 38, 56].”
Background
Ventral Hippocampal CA1 and CA3 Differentially Mediate Learned Approach-Avoidance Conflict Processing
Schumacher, A., Villaruel, F. R., Ussling, A., Riaz, S., Lee, A. C. H., & Ito, R. (2018) · Current Biology · doi:10.1016/j.cub.2018.03.012 · Cited by 101 · see citing works
Slow escape decisions are swayed by trait anxiety
Fung, B. J., Qi, S., Hassabis, D., Daw, N. D., & Mobbs, D. (2019) · Nature Human Behaviour · doi:10.1038/s41562-019-0595-5 · Cited by 102 · see citing works
Acute and chronic effects of selective serotonin reuptake inhibitor treatment on fear conditioning: Implications for underlying fear circuits
Burghardt, N. S., & Bauer, E. P. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.050 · Cited by 101 · see citing works
Global and gene-specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment
Doherty, T. S., Forster, A., & Roth, T. L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.05.028 · Cited by 100 · see citing works
Medial Septal Lesions Mimic Effects of Both Selective Dorsal and Ventral Hippocampal Lesions.
Bannerman, D. M., Matthews, P. M., Deacon, R. M. J., & Rawlins, J. N. P. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.5.1033 · Cited by 98 · see citing works
Self-citation
Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning
Esclassan, F., Coutureau, É., Scala, G. D., & Marchand, A. R. (2008) · Hippocampus · doi:10.1002/hipo.20473 · Cited by 92 · see citing works
“It has thus been suggested that this region plays a general role in the expression of anxietyrelated behaviors (Richmond et al., 1999; Bannerman et al., 2004; Degroot and Treit, 2004; McHugh et al., 2004).”
Dorsal versus ventral hippocampal contributions to trace and contextual conditioning: Differential effects of regionally selective nmda receptor antagonism on acquisition and expression
Czerniawski, J. L., Ree, F., Chia, C., & Otto, T. (2011) · Hippocampus · doi:10.1002/hipo.20992 · Cited by 91 · see citing works
“Consistent with this notion, several laboratories have reported that amygdala and VH play critical but dissociable roles in fear and anxiety, respectively (Phillips and LeDoux, 1992; Bannerman et al., 2004; McHugh et al., 2004).”
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Dorsal and ventral hippocampal adult-born neurons contribute to context fear memory
Huckleberry, K. A., Shue, F., Copeland, T., Chitwood, R. A., Yin, W., & Drew, M. R. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0109-6 · Cited by 91 · see citing works
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“…in the dorsal hippocampus all decreased unconditioned fear reactions in the elevated plus-maze and social interaction tests (Liberato et al., 2006; Rezayat et al., 2005; Kjelstrup et al., 2002; Bannerman et al., 2002; McHugh et al., 2004; Degroot and Treit, 2004; Menard and Treit, 2001; Table 7).”
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Fear and anxiety while driving: Differential impact of task demands, speed and motivation
Schmidt‐Daffy, M. (2012) · Transportation Research Part F Traffic Psychology and Behaviour · doi:10.1016/j.trf.2012.07.002 · Cited by 90 · see citing works
Examining the Role of the Human Hippocampus in Approach–Avoidance Decision Making Using a Novel Conflict Paradigm and Multivariate Functional Magnetic Resonance Imaging
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“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 95 · see citing works
“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 89 · see citing works
“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 85 · see citing works
“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.”
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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 88 · see citing works
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 89 · see citing works
Endocannabinoids, cannabinoids and the regulation of anxiety
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Dorsal hippocampus involvement in delay fear conditioning depends upon the strength of the tone‐footshock association
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“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
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Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety
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“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).”
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State-Dependent Alterations in Hippocampal Oscillations in Serotonin 1A Receptor-Deficient Mice
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“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).”
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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 · see citing works
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 75 · see citing works
“…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).”
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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 78 · see citing works
Cross-species anxiety tests in psychiatry: pitfalls and promises
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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 · see citing works
“…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 77 · see citing works
The Avian Hippocampal Formation and the Stress Response
Smulders, T. V. (2017) · Brain Behavior and Evolution · doi:10.1159/000477654 · Cited by 74 · see citing works
“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].”
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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 · see citing works
“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).”
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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 74 · see citing works
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 · see citing works
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 73 · see citing works
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 · see citing works
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 · see citing works
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 72 · see citing works
“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 71 · see citing works
“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 · see citing works
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. R. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.01.018 · Cited by 67 · see citing works
“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 65 · see citing works
“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 · see citing works
“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 · see citing works
“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 · see citing works
“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 · see citing works
“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.”
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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 · see citing works
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 60 · see citing works
“…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 · see citing works
“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 62 · see citing works

Ventral hippocampal lesions affect anxiety but not spatial learning
Bannerman, D. M., Grubb, M., Deacon, R. M. J., Yee, B. K., Feldon, J., & Rawlins, J. N. P. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00268-1 · Cited by 530 · see citing works
Self-citation
Dissociations among the anxiolytic effects of septal, hippocampal, and amygdaloid lesions.
Treit, D., & Menard, J. L. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.3.653 · Cited by 128 · see citing works
Dissociating the anti-fear effects of septal and amygdaloid lesions using two pharmacologically validated models of rat anxiety.
Treit, D., Pesold, C., & Rotzinger, S. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.5.770 · Cited by 137 · see citing works
Regional dissociations within the hippocampus-memory and anxiety
Bannerman, D. M., Rawlins, J. N. P., McHugh, S. B., Deacon, R. M. J., Yee, B. K., Bast, T., Zhang, W.-N., Pothuizen, H. H. J., & Feldon, J. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.03.004 · Cited by 1,462 · see citing works
Self-citation
Lesions of the ventral hippocampus, but not the dorsal hippocampus, impair conditioned fear expression and inhibitory avoidance on the elevated T-maze
Trivedi, M. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.02.005 · Cited by 179 · see citing works

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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