Developmental rodent models of fear and anxiety: from neurobiology to pharmacology

Ganella, Despina E; Kim, Jee Hyun

doi:10.1111/bph.12643

Cited by 107Memory and Neural MechanismsStress Responses and CortisolNeurotransmitter Receptor Influence on Behavior

Developmental rodent models of fear and anxiety: from neurobiology to pharmacology

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Ganella, Despina E, Kim, Jee Hyun·2014·British Journal of Pharmacology

DOI 10.1111/bph.12643PMC PMC4209932

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Abstract

Anxiety disorders pose one of the biggest threats to mental health in the world, and they predominantly emerge early in life. However, research of anxiety disorders and fear-related memories during development has been largely neglected, and existing treatments have been developed based on adult models of anxiety. The present review describes animal models of anxiety disorders across development and what is currently known of their pharmacology. To summarize, the underlying mechanisms of intrinsic 'unlearned' fear are poorly understood, especially beyond the period of infancy. Models using 'learned' fear reveal that through development, rats exhibit a stress hyporesponsive period before postnatal day 10, where they paradoxically form odour-shock preferences, and then switch to more adult-like conditioned fear responses. Juvenile rats appear to forget these aversive associations more easily, as is observed with the phenomenon of infantile amnesia. Juvenile rats also undergo more robust extinction, until adolescence where they display increased resistance to extinction. Maturation of brain structures, such as the amygdala, prefrontal cortex and hippocampus, along with the different temporal recruitment and involvement of various neurotransmitter systems (including NMDA, GABA, corticosterone and opioids) are responsible for these developmental changes. Taken together, the studies described in this review highlight that there is a period early in development where rats appear to be more robust in overcoming adverse early life experience. We need to understand the fundamental pharmacological processes underlying anxiety early in life in order to take advantage of this period for the treatment of anxiety disorders.

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Early memories contribute to anxiety disorders.
“This notion that early memories contribute to anxiety disorders is still widely held [review in Ref. (96)] and is a component of the present explanatory framework for nightmares.”
From The Stress Acceleration Hypothesis of Nightmares (2017) · cites this paper as [96]

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Freud S, Breuer J (1893) On the psychical mechanism of hysterical phenomena: preliminary communications. In: Strachey J, Strachey A (eds). Studies in hysteria. Harmonsworth Penguin: London, 1974, pp. 53-69.

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Sensitive periods of substance abuse: Early risk for the transition to dependence
Jordan, C. J., & Andersen, S. L. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.10.004 · Cited by 455 · see citing works
“Individual stress reactivity can be quantified as a risk factor for SUD by assessing emotional dysregulation, startle and other physiological responses, and in open-field and elevated plus maze tests (Connor-Smith et al., 2000; Ganella and Kim, 2014; Kalinichev et al., 2002; Quas et al., 2014).”
Avoidance and its bi-directional relationship with conditioned fear: Mechanisms, moderators, and clinical implications
Pittig, A., Wong, A. H. K., Glück, V. M., & Boschet, J. M. (2020) · Behaviour Research and Therapy · doi:10.1016/j.brat.2020.103550 · Cited by 148 · see citing works
Ontogeny of memory: an update on 40 years of work on infantile amnesia
Madsen, H. B., & Kim, J. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.07.030 · Cited by 92 · see citing works
Self-citation
Age Differences in the Neural Correlates of Anxiety Disorders: An fMRI Study of Response to Learned Threat
Gold, A. L., Abend, R., Britton, J. C., Behrens, B., Farber, M. J., Ronkin, E. G., Chen, G., Leibenluft, E., & Pine, D. S. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.19060650 · Cited by 80 · see citing works
The Effectiveness of Psychological Therapies for Anxiety Disorders in Adolescents: A Meta-Analysis
Baker, H. J., Lawrence, P. J., Karalus, J., Creswell, C., & Waite, P. (2021) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-021-00364-2 · Cited by 75 · see citing works
Common neurocircuitry mediating drug and fear relapse in preclinical models
Goode, T. D., & Maren, S. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5024-3 · Cited by 72 · see citing works
Anxiety-like behaviour increases safety from fish predation in an amphipod crustacea
Perrot‐Minnot, M., Banchetry, L., & Cézilly, F. (2017) · Royal Society Open Science · doi:10.1098/rsos.171558 · Cited by 72 · see citing works
The Stress Acceleration Hypothesis of Nightmares
Nielsen, T. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00201 · Cited by 63 · see citing works
“(96)] and is a component of the present explanatory framework for nightmares.”
Background
Assessment of conditioned fear extinction in male and female adolescent rats
Perry, C. J., Ganella, D. E., Nguyen, L. D., Du, X., Drummond, K. D., Whittle, S., Pang, T. Y., & Kim, J. H. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104670 · Cited by 47 · see citing works
A Baldwin interpretation of adult hippocampal neurogenesis: from functional relevance to physiopathology
Abrous, D. N., Koehl, M., & Lemoine, M. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01172-4 · Cited by 45 · see citing works
Emotional learning, stress, and development: An ever-changing landscape shaped by early-life experience
Pattwell, S. S., & Bath, K. G. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.04.014 · Cited by 46 · see citing works
Adolescent alcohol exposure produces sex differences in negative affect-like behavior and group I mGluR BNST plasticity
Kasten, C. R., Carzoli, K. L., Sharfman, N. M., Henderson, T., Holmgren, E. B., Lerner, M. R., Miller, M. C., & Wills, T. A. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0670-7 · Cited by 43 · see citing works
The effects of environmental enrichment and social isolation and their reversion on anxiety and fear conditioning
Mora-Gallegos, A., & Fornaguera, J. (2018) · Behavioural Processes · doi:10.1016/j.beproc.2018.10.022 · Cited by 42 · see citing works
The role of prefrontal–subcortical circuitry in negative bias in anxiety: Translational, developmental and treatment perspectives
Carlisi, C. O., & Robinson, O. J. (2018) · Brain and Neuroscience Advances · doi:10.1177/2398212818774223 · Cited by 42 · see citing works
Effects of paternal and peripubertal stress on aggression, anxiety, and metabolic alterations in the lateral septum
Cordero, M. I., Just, N., Poirier, G. L., & Sandi, C. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.017 · Cited by 38 · see citing works
Role of Dopamine 2 Receptor in Impaired Drug-Cue Extinction in Adolescent Rats
Zbukvic, I., Ganella, D. E., Perry, C. J., Madsen, H. B., Bye, C. R., Lawrence, A. J., & Kim, J. H. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw051 · Cited by 37 · see citing works
Juvenile female rats, but not male rats, show renewal, reinstatement, and spontaneous recovery following extinction of conditioned fearPreprint
Park, C. H. J., Ganella, D. E., & Kim, J. H. (2017) · Learning & Memory · doi:10.1101/lm.045831.117 · Cited by 37 · see citing works
Formyl Peptide Receptor as a Novel Therapeutic Target for Anxiety-Related Disorders
Irene, G., Rattazzi, L., Piras, G., Gobbetti, T., Panza, E., Perretti, M., Dalley, J. W., & D’Acquisto, F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0114626 · Cited by 35 · see citing works
Exposure to a maternal cafeteria diet changes open‐field behaviour in the developing offspring
Speight, A., Davey, W. G., McKenna, E., & Voigt, J. W. (2016) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2016.12.005 · Cited by 36 · see citing works
Differential effects of adolescent and adult-initiated voluntary exercise on context and cued fear conditioning
O’Leary, J. D., Hoban, A. E., Cryan, J. F., O’Leary, O. F., & Nolan, Y. M. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.05.007 · Cited by 38 · see citing works
Postnatal development of neurotransmitter systems and their relevance to extinction of conditioned fear
Kim, J. H., Perry, C. J., Ganella, D. E., & Madsen, H. B. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.10.018 · Cited by 35 · see citing works
Tinbergen’s challenge for the neuroscience of behavior
Pfaff, D. W., Tabansky, I., & Haubensak, W. E. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903589116 · Cited by 32 · see citing works
Early adolescent stress‐induced changes in prefrontal cortex miRNA‐135a and hippocampal miRNA‐16 in male rats
Liu, Y., Liu, D., Xu, J., Jiang, H., & Pan, F. (2017) · Developmental Psychobiology · doi:10.1002/dev.21558 · Cited by 32 · see citing works
Clarifying the neural substrates of threat and safety reversal learning in humans
Savage, H. S., Davey, C. G., Fullana, M. A., & Harrison, B. J. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116427 · Cited by 30 · see citing works
Environmental enrichment decreases anxiety‐like behavior in zebrafish larvae
Gatto, E., Dadda, M., Bruzzone, M., Chiarello, E., Russi, G. D., Maschio, M. D., Bisazza, A., & Lucon‐Xiccato, T. (2022) · Developmental Psychobiology · doi:10.1002/dev.22255 · Cited by 31 · see citing works
Unconventional anxiety pharmacology in zebrafish: Drugs beyond traditional anxiogenic and anxiolytic spectra
de Abreu, M. S., Giacomini, A. C. V. V., Demin, K. A., Galstyan, D. S., Zabegalov, K. N., Kolesnikova, T. O., Amstislavskaya, T. G., Strekalova, T. V., Petersen, E. V., & Kalueff, A. V. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173205 · Cited by 31 · see citing works
Dissociated roles of dorsal and ventral hippocampus in recall and extinction of conditioned fear in male and female juvenile rats
Park, C. H. J., Ganella, D. E., Perry, C. J., & Kim, J. H. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113306 · Cited by 28 · see citing works
Early Development of the GABAergic System and the Associated Risks of Neonatal Anesthesia
Gascoigne, D. A., Serdyukova, N. A., & Aksenov, D. P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312951 · Cited by 28 · see citing works
A dissociation between renewal and contextual fear conditioning in juvenile rats
Park, C. H. J., Ganella, D. E., & Kim, J. H. (2017) · Developmental Psychobiology · doi:10.1002/dev.21516 · Cited by 25 · see citing works
Impact of anesthesia exposure in early development on learning and sensory functions
Aksenov, D. P., Miller, M. J., Dixon, C. J., & Drobyshevsky, A. (2020) · Developmental Psychobiology · doi:10.1002/dev.21963 · Cited by 24 · see citing works
Optimising Exposure for Children and Adolescents with Anxiety, OCD and PTSD: A Systematic Review
Plaisted, H., Waite, P., Gordon, K., & Creswell, C. (2021) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-020-00335-z · Cited by 25 · see citing works
Cafeteria diet administered from lactation to adulthood promotes a change in risperidone sensitivity on anxiety, locomotion, memory, and social interaction of Wistar rats
Teixeira, A. E., Rocha‐Gomes, A., dos Santos, T. P., Amaral, B. L. S., da Silva, A. A., Malagutti, A. R., Leite, F. R. F., Stuckert-Seixas, S. R., & Riul, T. R. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112874 · Cited by 21 · see citing works
The impact of early postnatal environmental enrichment on maternal care and offspring behaviour following weaning
Li, K. A., Lund, E. T., & Voigt, J. W. (2015) · Behavioural Processes · doi:10.1016/j.beproc.2015.11.008 · Cited by 21 · see citing works
A Review of Preclinical Studies to Understand Fear During Adolescence
Kim, J. H., & Ganella, D. E. (2015) · Australian Psychologist · doi:10.1111/ap.12066 · Cited by 20 · see citing works
Epigenetic mechanisms involved in the effects of stress exposure: focus on 5-hydroxymethylcytosine: Table 1:
Hack, L. M., Dick, A. L. W., & Provençal, N. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvw016 · Cited by 18 · see citing works
Behavioral Effects of Buspirone in Juvenile Zebrafish of Two Different Genetic Backgrounds
Abozaid, A., & Gerlai, R. T. (2022) · Toxics · doi:10.3390/toxics10010022 · Cited by 18 · see citing works
Neurocircuitry of fear extinction in adult and juvenile rats
Ganella, D. E., Nguyen, L. D., Lee-Kardashyan, L., Kim, L. E., Paolini, A. G., & Kim, J. H. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.001 · Cited by 18 · see citing works
Diazepam effects on anxiety-related defensive behavior of male and female high and low open‐field activity inbred mouse strains
Mehrhoff, E. A., Booher, W. C., Hutchinson, J., Schumacher, G., Borski, C., Lowry, C. A., Hoeffer, C. A., & Ehringer, M. A. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114343 · Cited by 17 · see citing works
Eternal sunshine of the neuromodulated mind: Altering fear memories through neuromodulation
Tan, S. Z. K., Sheng, V., Chan, Y., & Lim, L. W. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.01.004 · Cited by 17 · see citing works
Cardinal role of the environment in stress induced changes across life stages and generations
Pang, T. Y., Yaeger, J. D. W., Summers, C. H., & Mitra, R. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.012 · Cited by 16 · see citing works
Thin graphene oxide nanoflakes modulate glutamatergic synapses in the amygdala cultured circuits: Exploiting synaptic approaches to anxiety disorders
Secomandi, N., Biagioni, A. F., Kostarelos, K., Cellot, G., & Ballerini, L. (2020) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2020.102174 · Cited by 16 · see citing works
Contextual fear memory modulates PSD95 phosphorylation, AMPAr subunits, PKMζ and PI3K differentially between adult and juvenile rats
Zanca, R. M., Sanay, S., Avila, J. A., Rodriguez, E., Shair, H. N., & Serrano, P. A. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.11.002 · Cited by 15 · see citing works
Effects of Methamphetamine Exposure on Fear Learning and Memory in Adult and Adolescent Rats
Luikinga, S. J., Perry, C. J., Madsen, H. B., Lawrence, A. J., & Kim, J. H. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02845-x · Cited by 15 · see citing works
BNST specific mGlu5 receptor knockdown regulates sex-dependent expression of negative affect produced by adolescent ethanol exposure and adult stress
Kasten, C. R., Holmgren, E. B., Lerner, M. R., & Wills, T. A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01285-y · Cited by 15 · see citing works
Prelimbic cortical stimulation disrupts fear memory consolidation through ventral hippocampal dopamine D2 receptors
Tan, S. Z. K., Poon, C. H., Chan, Y., & Lim, L. W. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15505 · Cited by 14 · see citing works
Basolateral Amygdala Hyperexcitability Is Associated with Precocious Developmental Emergence of Fear-Learning in Fragile X Syndrome
Svalina, M. N., Rio, C. A. C.-D., Kushner, J. K., Levy, A., Baca, S. M., Guthman, E. M., Opendak, M. M., Sullivan, R. M., Restrepo, D., & Huntsman, M. M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1776-21.2022 · Cited by 13 · see citing works
Contributions of human amygdala nuclei to resting-state networks
Elvira, U. K., Seoane, S., Janssen, J., & Janssen, N. (2022) · PLoS ONE · doi:10.1371/journal.pone.0278962 · Cited by 13 · see citing works
A dissociation between recognition and reactivation: The renewal effect at 3 months of age
Cuevas, K., Learmonth, A. E., & Rovee‐Collier, C. (2015) · Developmental Psychobiology · doi:10.1002/dev.21357 · Cited by 13 · see citing works
Sex-dependent effects of chronic exercise on cognitive flexibility but not hippocampal Bdnf in aging mice
Short, A. K., Bui, V., Zbukvic, I., Hannan, A. J., Pang, T. Y., & Kim, J. H. (2021) · Neuronal Signaling · doi:10.1042/ns20210053 · Cited by 13 · see citing works
Human fear neurobiology reimagined: Can brain-derived biotypes predict fear-based disorders after trauma?
France, J. M., & Jovanović, T. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104988 · Cited by 11 · see citing works
Sex-dependent effects of chronic exercise on cognitive flexibility but not hippocampal Bdnf in aging mice
Short, A. K., Bui, M. V., Zbukvic, I., Hannan, A. J., Pang, T. Y., & Kim, J. H. (2022) · Own your potential (DEAKIN) · Cited by 11 · see citing works
Age-specific sex effects in extinction of conditioned fear in rodents
Malik, S., Park, C. H. J., & Kim, J. H. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1298164 · Cited by 11 · see citing works
Context fear learning and renewal of extinguished fear are dissociated in juvenile female rats
Park, C. H. J., Ganella, D. E., & Kim, J. H. (2019) · Developmental Psychobiology · doi:10.1002/dev.21888 · Cited by 12 · see citing works
The outcome of early life status epilepticus—lessons from laboratory animals
Kubová, H., Mikulecká, A., & Mareš, P. (2022) · Epilepsia Open · doi:10.1002/epi4.12664 · Cited by 11 · see citing works
Moderators of cognitive and behaviour therapies for prevention and treatment of anxiety disorders in children and adolescents: A systematic review and meta-analysis
Zhou, S., Creswell, C., Košir, U., & Reardon, T. C. (2025) · Clinical Psychology Review · doi:10.1016/j.cpr.2025.102548 · Cited by 9 · see citing works
Initial evidence for pharmacological modulation of observational threat learning by the GABAergic, but not the noradrenergic system in humans
Esser, R. W., Fuß, J., & Haaker, J. (2020) · Behaviour Research and Therapy · doi:10.1016/j.brat.2020.103605 · Cited by 9 · see citing works
Puzzle feeder as a cognitive enrichment strategy determines long-term welfare improvements in a teleost fish
Gatto, E., Varracchio, C., Bertolucci, C., & Lucon‐Xiccato, T. (2024) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2024.106401 · Cited by 8 · see citing works
A novel discovery platform for targeted drug repurposing: application for psychiatric disorders
Berk, M., Kim, J. H., Williams, L. J., Liu, Z. S.-J., Siskind, D. J., Panizzutti, B., Yung, A. R., & Walder, K. R. (2025) · The Lancet Psychiatry · doi:10.1016/s2215-0366(25)00066-5 · Cited by 8 · see citing works
Function and development of interneurons involved in brain tissue oxygen regulation
Aksenov, D. P., Gascoigne, D. A., Duan, J., & Drobyshevsky, A. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1069496 · Cited by 8 · see citing works
Optimising exposure for adolescents with public speaking anxiety: Affect labelling or positive coping statements?
Plaisted, H., Waite, P., & Creswell, C. (2021) · Behaviour Research and Therapy · doi:10.1016/j.brat.2021.103997 · Cited by 10 · see citing works
Reducing Fear During Childhood to Prevent Anxiety Disorders Later: Insights From Developmental Psychobiology
Kim, J. H. (2017) · Policy Insights from the Behavioral and Brain Sciences · doi:10.1177/2372732217719544 · Cited by 7 · see citing works
A Window on the Study of Aversive Instrumental Learning: Strains, Performance, Neuroendocrine, and Immunologic Systems
de Oliveira, C. C., Gouveia, F. V., de Castro, M. C., Kuroki, M. A., dos Santos, L. C. T., Fonoff, E. T., Teixeira, M. J., Otoch, J. P., & Martinez, R. C. R. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00162 · Cited by 7 · see citing works
Enduring Neural and Behavioral Effects of Early Life Adversity in Infancy: Consequences of Maternal Abuse and Neglect, Trauma and Fear
Boulanger-Bertolus, J., White, A. M., & Dębiec, J. (2017) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-017-0112-y · Cited by 7 · see citing works
GABA Receptors in the Modulation of Fear Memory Extinction
Dubrovina, N. I. (2017) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-017-0438-7 · Cited by 6 · see citing works
Chlordiazepoxide reduces anxiety-like behavior in the adolescent mouse elevated plus maze: A pharmacological validation study
Themann, A., Rodriguez, M., Reyes-Arce, J., & Iñiguez, S. D. (2024) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2024.173819 · Cited by 6 · see citing works
Modelos animales de miedo y ansiedad: descripciones neuro-conductuales
Mora-Gallegos, A., & Castillo, S. S. (2014) · Actualidades en Psicología · doi:10.15517/ap.v28i117.14595 · Cited by 6 · see citing works
Youth is not wasted on the young: Commentary on a BBR themed issue on developmental regulation of memory in anxiety and addiction
Kim, J. H. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.043 · Cited by 6 · see citing works
Mild daily stressors in adulthood may counteract behavioural effects after constant presence of mother during early life
Mrdalj, J., Murison, R. C. C., Soule, J. D., Rød, A. M. K., Milde, A. M., Pallesen, S., & Grønli, J. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.08.018 · Cited by 6 · see citing works
Anxiolytic-like effect of a novel peptide isolated from the venom of the social wasp Synoeca surinama
Gomes, F. M. M., Paniago, C. K., Freire, D. O., de Souza, A. C. B., Lima, M. R., Oliveira-Júnior, N. G., Franco, O. L., & Mortari, M. R. (2016) · Toxicon · doi:10.1016/j.toxicon.2016.09.015 · Cited by 6 · see citing works
Loss of the neuronal kinase DCLK3 leads to anxiety-like behaviour and memory deficits
de Longprez, L., Gaillard, M., Decraene, C., Pérot, J., Keime, C., Nadkarni, N. A., Louçã, M., Jan, C., Liot, G., Aurégan, G., et al. (2025) · Brain · doi:10.1093/brain/awaf042 · Cited by 5 · see citing works
mGlu5: A double-edged sword for aversive learning related therapeutics
Tan, S., & Kim, J. (2021) · Neuroanatomy and Behaviour · doi:10.35430/nab.2021.e16 · Cited by 4 · see citing works
Auditory fear conditioning alters neural gain in the cochlear nucleus: a wireless neural recording study in freely behaving rats
Paolini, A. G., Morgan, S. J., & Kim, J. H. (2020) · Neuronal Signaling · doi:10.1042/ns20200009 · Cited by 5 · see citing works
Impacto y calidad de la productividad académica de los investigadores en Colombia en neurociencia comportamental utilizando modelos animales
Robayo-Castro, B. H., Rico, J. L., Hurtado‐Parrado, C., & Ortega, L. A. (2017) · Universitas Psychologica · doi:10.11144/javeriana.upsy15-5.icpa · Cited by 4 · see citing works
Conditioned Anxiety Mechanism as a Basis for a Procedure of Control Module of an Autonomous Robot
Bielecki, A., Bielecka, M., & Bielecki, P. (2017) · Lecture notes in computer science · doi:10.1007/978-3-319-59060-8_35 · Cited by 4 · see citing works
The pathophysiology of rhabdomyolysis in ungulates and rats: towards the development of a rodent model of capture myopathy
Lubbe, C., Meyer, L. C. R., Kohn, T. A., Harvey, B. H., & Wolmarans, D. W. (2022) · Veterinary Research Communications · doi:10.1007/s11259-022-10030-9 · Cited by 4 · see citing works
Hippocampus-dependent learning in SKAP-HOM deficient mice
Fiedler, A., Grecksch, G., Reinhold, A., Schraven, B. L., & Becker, A. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.051 · Cited by 4 · see citing works
Ameliorative Effect of Moringa oleifera Against CUMS-Induced Anxiety in Rats: β-Catenin and 5-HT1 A Crosstalk
El‐Kadi, R. A., Sedeek, M. S., Abdelkader, N. F., Zaki, H. F., & Kamel, A. S. E. D. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04911-8 · Cited by 4 · see citing works
Periadolescent Social Isolation Effects on Extinction of Conditioned Fear
Drummond, K. D., & Kim, J. H. (2023) · Neuromethods · doi:10.1007/978-1-0716-3218-5_2 · Cited by 3 · see citing works
Adolescent rats show estrous cycle-mediated sex-differences in extinction of conditioned fearPreprint
Perry, C. J., Ganella, D. E., Nguyen, L. D., Du, X., Drummond, K. D., Whittle, S., Pang, T. Y., & Kim, J. H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.31.019273 · Cited by 3 · see citing works
Frontal cortex norepinephrine, serotonin, and dopamine dynamics in an innate fear-reward behavioral modelPreprint
Yang, J.-H., Burke, E. L., Basu, A., Liu, R.-J., Staszko, S. M., Yu, A. L., Rondeau, J., Glaeser-Khan, S., Zhuo, Y., Feng, J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.27.568929 · Cited by 4 · see citing works
Minimizing Variability in Developmental Fear Studies in Mice: Toward Improved Replicability in the Field
Premachandran, H., Wilkin, J., & Arruda-Carvalho, M. (2024) · Current Protocols · doi:10.1002/cpz1.1040 · Cited by 2 · see citing works
Sex-specific vulnerability to single prolonged stress: behavioral alterations and redox imbalance in the developing brain
Cesare, B. D., Mancini, G. F., Lisiola, J. M., Pisaneschi, A., Sikora, V., Morena, M., Caraci, F., Riva, M. A., Schiavone, S., & Campolongo, P. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.117413 · Cited by 2 · see citing works
Automated Synthesis of [18F]Flumazenil Application in GABAA Receptor Neuroimaging Availability for Rat Model of Anxiety
Farn, S., Cheng, K.-H., Huang, Y.-R., Lee, S.-Y., Chen, J.-T., & Chang, K. (2023) · Pharmaceuticals · doi:10.3390/ph16030417 · Cited by 2 · see citing works
Modeling Anger-Like Responses in Animals: Denial of Food in Sight
Subhedar, N. K., Dudhabhate, B. B., & Kokare, D. M. (2023) · Springer eBooks · doi:10.1007/978-3-031-31547-3_143 · Cited by 2 · see citing works
Maternal Separation Exhibits a Sex Dimorphism in Memory Impairments in Adolescent Rats: Acute Methylphenidate Administration as a Treatment
Borzadaran, F. M., Rezakhani, S., Kamali, R., & Esmaeilpour, K. (2025) · Birth Defects Research · doi:10.1002/bdr2.2441 · Cited by 2 · see citing works
Adult Health and Early Life Adversity: Behind the Curtains of Maternal Care Research
Dumas, T. C. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.804239 · Cited by 3 · see citing works
Behavioral comorbidities of early-life seizures: Insights from developmental studies in rats
Grígelová, A., Mikulecká, A., & Kubová, H. (2025) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2025.110307 · Cited by 1 · see citing works
Understanding adolescent anxiety through a neurodevelopmental lens: A comparative review of rodents and humans
Cody, C. R., Hennessy, R. R., Brenhouse, H. C., & Davidow, J. Y. (2025) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2025.101620 · Cited by 1 · see citing works
Generalization and Extinction of Conditioned Fear in Adolescents and Adults: Objective, Subjective, and Neural Outcomes
McCallum, M., Hallford, D. J., & Kim, J. H. (2026) · Depression and Anxiety · doi:10.1155/da/6001839 · Cited by 1 · see citing works
Modeling Anger-Like Responses in Animals: Denial of Food in Sight
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Authors: Ganella, D. E., & Kim, J. H.
Affiliations: The University of Melbourne (AU)
Corresponding author: Kim, Jee Hyun
ORCID: Kim, Jee Hyun
Venue: British Journal of Pharmacology
Publisher: Wiley
Published: 2014-07
Volume: 171
Issue: 20
Pages: 4556-4574
ISSN: 0007-1188 (ISSN-L)
1476-5381
DOI: 10.1111/bph.12643
PMC: PMC4209932
OpenAlex: W1490288863
Cited by: 107
References: 232
Citations by year: 2026: 5 · 2025: 11 · 2024: 6 · 2023: 6 · 2022: 13 · 2021: 11 · 2020: 13 · 2019: 6 · 2018: 6 · 2017: 12 · 2016: 8 · 2015: 6 · 2014: 4
FWCI: 0.97
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: British Journal of Pharmacology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Figshare (submittedVersion, cc-by)
Funders: Australian Research Council (DE120100110)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: anxiety disorders, fear, learned fear, infantile amnesia, fear extinction, stress hyporesponsive period, prefrontal cortex, hippocampus, NMDA receptor, GABA, corticosterone, opioids, early life experience, adolescence
MeSH terms: Animals, Anxiety, Avoidance Learning, Brain, Disease Models, Animal, Fear, Humans, Synaptic Transmission, Reflex, Startle, Vocalization, Animal

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