Extinction (psychology)

Extinction is a behavioral phenomenon observed in both operantly conditioned and classically conditioned behavior, which manifests itself by fading of non-reinforced conditioned response over time. When operant behavior that has been previously reinforced no longer produces reinforcing consequences, the behavior gradually returns to operant levels (to the frequency of the behavior previous to learning, which may or may not be zero)^[1].^[2] In classical conditioning, when a conditioned stimulus is presented alone, so that it no longer predicts the coming of the unconditioned stimulus, conditioned responding gradually stops. For example, after Pavlov's dog was conditioned to salivate at the sound of a metronome, it eventually stopped salivating to the metronome after the metronome had been sounded repeatedly but no food came. Many anxiety disorders such as post-traumatic stress disorder are believed to reflect, at least in part, a failure to extinguish conditioned fear.^[3]

Theories

The dominant account of extinction involves associative models. However, there is debate over whether extinction involves simply "unlearning" the unconditional stimulus (US) – Conditional stimulus (CS) association (e.g., the Rescorla–Wagner account) or, alternatively, a "new learning" of an inhibitory association that masks the original excitatory association (e.g., Konorski, Pearce and Hall account). A third account concerns non-associative mechanisms such as habituation, modulation and response fatigue. Myers & Davis review fear extinction in rodents and suggested that multiple mechanisms may be at work depending on the timing and circumstances in which the extinction occurs.^[4]

Given the competing views and difficult observations for the various accounts researchers have turned to investigations at the cellular level (most often in rodents) to tease apart the specific brain mechanisms of extinction, in particular the role of the brain structures (amygdala, hippocampus, the prefrontal cortex), and specific neurotransmitter systems (e.g., GABA, NMDA).^[4] A recent study in rodents by Amano, Unal and Paré published in Nature Neuroscience found that extinction of a conditioned fear response is correlated with synaptic inhibition in the fear output neurons of the central amygdala that project to the periaqueductal gray that controls freezing behavior. They infer that inhibition derives from the ventromedial prefrontal cortex and suggest promising targets at the cellular level for new treatments of anxiety.^[5]

Classical conditioning

Learning extinction can also occur in a classical conditioning paradigm. In this model, a neutral cue or context can come to elicit a conditioned response when it is paired with an unconditioned stimulus. An unconditioned stimulus is one that naturally and automatically triggers a certain behavioral response. A certain stimulus or environment can become a conditioned cue or a conditioned context, respectively, when paired with an unconditioned stimulus. An example of this process is a fear conditioning paradigm using a mouse. In this instance, a tone paired with a mild footshock can become a conditioned cue, eliciting a fear response when presented alone in the future. In the same way, the context in which a footshock is received such as a chamber with certain dimensions and a certain odor can elicit the same fear response when the mouse is placed back in that chamber in the absence of the footshock.

In this paradigm, extinction occurs when the animal is re-exposed to the conditioned cue or conditioned context in the absence of the unconditioned stimulus. As the animal learns that the cue or context no longer predicts the coming of the unconditioned stimulus, conditioned responding gradually decreases, or extinguishes.

Operant conditioning

In the operant conditioning paradigm, extinction refers to the process of no longer providing the reinforcement that has been maintaining a behavior. Operant extinction differs from forgetting in that the latter refers to a decrease in the strength of a behavior over time when it has not been emitted.^[6] For example, a child who climbs under his desk, a response which has been reinforced by attention, is subsequently ignored until the attention-seeking behavior no longer occurs. In his autobiography, B. F. Skinner noted how he accidentally discovered the extinction of an operant response due to the malfunction of his laboratory equipment:

My first extinction curve showed up by accident. A rat was pressing the lever in an experiment on satiation when the pellet dispenser jammed. I was not there at the time, and when I returned I found a beautiful curve. The rat had gone on pressing although no pellets were received. ... The change was more orderly than the extinction of a salivary reflex in Pavlov's setting, and I was terribly excited. It was a Friday afternoon and there was no one in the laboratory whom I could tell. All that weekend I crossed streets with particular care and avoided all unnecessary risks to protect my discovery from loss through my accidental death.^[7]

When the extinction of a response has occurred, the discriminative stimulus is then known as an extinction stimulus (SΔ or S-delta). When an S-delta is present, the reinforcing consequence which characteristically follows a behavior does not occur. This is the opposite of a discriminative stimulus, which is a signal that reinforcement will occur. For instance, in an operant conditioning chamber, if food pellets are only delivered when a response is emitted in the presence of a green light, the green light is a discriminative stimulus. If when a red light is present. food will not be delivered, then the red light is an extinction stimulus. (Food is used here as an example of a reinforcer.) However, some make the distinction between extinction stimuli and "S-Delta" due to the behavior not having a reinforcement history, i.e. in an array of three items (phone, pen, paper) "Which one is the phone" the "pen" and "paper" will not produce a response in the teacher, but is not technically extinction on the first trial due to selecting "pen" or "paper", missing a reinforcement history. This still would be considered as S-Delta.

Successful extinction procedures

In order for extinction to work effectively, it must be done consistently. Extinction is considered successful when responding in the presence of an extinction stimulus (a red light or a teacher not giving a bad student attention, for instance) is zero. When a behavior reappears again after it has gone through extinction, it is called spontaneous recovery. It (extinction) is the result of challenging behavior(s) no longer occurring without the need for reinforcement. If there is a relapse and reinforcements are given, the problem behavior will return. Extinction can be a long process; therefore, it requires that the facilitator of the procedure be completely invested from beginning to end in order for the outcome to be successful.^[8] The fewer challenging behaviors observed after extinction will most likely produce a less significant spontaneous recovery.^[9] While working towards extinction there are different distributions or schedules of when to administer reinforcements. Some people may use an intermittent reinforcement schedule that include: fixed ratio, variable ratio, fixed interval and variable interval. Another option is to use a continuous reinforcement. Schedules can be both fixed and variable and also the number of reinforcements given during each interval can vary.^[10]

Extinction procedures in the classroom

A positive classroom environment wields better results in learning growth. Therefore, in order for children to be successful in the classroom, their environment should be free of problem behaviors that can cause distractions.^[11] The classroom should be a place that offers consistency, structure, and stability, where the student feels empowered, supported and safe. When problem behaviors occur, learning opportunities decrease.^[12] Problem behaviors in the classroom that would benefit from extinction may include off-task behaviors, blurting, yelling, interrupting and use of inappropriate language.^[13] The use of extinction has been used primarily when the problem behaviors interfered with successful classroom outcomes.^[14] While other methods have been used in conjunction with extinction, positive outcomes are not likely when extinction is not used in behavior interventions.^[13]

Burst

While extinction, when implemented consistently over time, results in the eventual decrease of the undesired behavior, in the short term the subject might exhibit what is called an extinction burst. An extinction burst will often occur when the extinction procedure has just begun. This usually consists of a sudden and temporary increase in the response's frequency, followed by the eventual decline and extinction of the behavior targeted for elimination. Novel behavior, or emotional responses or aggressive behavior, may also occur.^[2]

For example, a pigeon has been reinforced to peck an electronic button. During its training history, every time the pigeon pecked the button, it will have received a small amount of bird seed as a reinforcer. Thus, whenever the bird is hungry, it will peck the button to receive food. However, if the button were to be turned off, the hungry pigeon will first try pecking the button just as it has in the past. When no food is forthcoming, the bird will likely try repeatedly. After a period of frantic activity, in which their pecking behavior yields no result, the pigeon's pecking will decrease in frequency.

Although not explained by reinforcement theory, the extinction burst can be understood using control theory. In perceptual control theory, the degree of output involved in any action is proportional to the discrepancy between the reference value (desired rate of reward in the operant paradigm) and the current input. Thus, when reward is removed, the discrepancy increases, and the output is increased. In the long term, 'reorganisation', the learning algorithm of control theory, would adapt the control system such that output is reduced.

The evolutionary advantage of this extinction burst is clear. In a natural environment, an animal that persists in a learned behavior, despite not resulting in immediate reinforcement, might still have a chance of producing reinforcing consequences if the animal tries again. This animal would be at an advantage over another animal that gives up too easily.

Despite the name, however, not every explosive reaction to adverse stimuli subsides to extinction. Indeed, a small minority of individuals persist in their reaction indefinitely.

Extinction-induced variability

Extinction-induced variability serves an adaptive role similar to the extinction burst. When extinction begins, subjects can exhibit variations in response topography (the movements involved in the response). Response topography is always somewhat variable due to differences in environment or idiosyncratic causes but normally a subject's history of reinforcement keeps slight variations stable by maintaining successful variations over less successful variations. Extinction can increase these variations significantly as the subject attempts to acquire the reinforcement that previous behaviors produced. If a person attempts to open a door by turning the knob, but is unsuccessful, they may next try jiggling the knob, pushing on the frame, knocking on the door or other behaviors to get the door to open. Extinction-induced variability can be used in shaping to reduce problematic behaviors by reinforcing desirable behaviors produced by extinction-induced variability.

Autism

See also: Autism rights movement § Ethical challenges to autism treatment

Children with Autism Spectrum Disorder (ASD) are known to have restricted or repetitive behaviors that can cause problems when trying to function in day-to-day activities.^[15] Extinction is used as an intervention to help with problem behaviors.^[16] Some problem behaviors may include but are not limited to, self-injurious behaviors, aggression, tantrums, problems with sleep, and making choices.^[17] Ignoring certain self-injurious behaviors can lead to the extinction of said behaviors in children with ASD.^[18] Escape Extinction (EE) is commonly used in instances when having to make choices causes problem behavior.^[19] An example could be having to choose between mint or strawberry flavored toothpaste when brushing your teeth. Those would be the only two options available. When implementing EE, the interventionist will use physical and verbal prompting to help the subject make a choice.^[19]

Anxiety

Fear extinction is the fundamental principle behind exposure therapy, a common treatment for anxiety disorders. In this process, the conditioned fear responses diminish progressively over time, when the previously conditioned stimulus is presented without being paired with the unconditioned stimulus.^[20] To understand the brain changes during this, a task-functional Magnetic Resonance Imaging (fMRI) can be performed. Moreover, Positron Emission Tomography (PET) can be used to quantify endogenous dopamine release. Dopamine antagonists like [¹¹C] raclopride and [¹⁸F] fallypride can be used to study D2/D3 dopamine receptor binding potential in the brain. [¹¹C] Raclopride is popular in studies focusing on striatal dopamine activity^[21] and ease of use considering a shorter half-life (about 20 minutes). On the other hand, [¹⁸F] fallypride is best for studying extrastriatal^[22] dopamine binding potential^[23] but has a half-life of approximately 110 minutes. Additionally, simultaneous PET and fMRI allow researchers to capture both dopamine binding potential and blood oxygen level-dependent (BOLD) signals during the task. Recent studies highlight the critical role of dorsolateral and ventromedial prefrontal cortex regions (vmPFC), together with other areas like the anterior insula, amygdala, and hippocampus in facilitating fear extinction processes.^[24]

Neurobiology

Glutamate

Glutamate is a neurotransmitter that has been extensively implicated in the neural basis of learning.^[25] D-Cycloserine (DCS) is a partial agonist for the glutamate receptor NMDA at the glycine site, and has been trialed as an adjunct to conventional exposure-based treatments based on the principle of cue extinction.

A role for glutamate has also been identified in the extinction of a cocaine-associated environmental stimulus through testing in rats. Specifically, the metabotropic glutamate 5 receptor (mGlu5) is important for the extinction of a cocaine-associated context^[26] and a cocaine-associated cue.^[27]

Dopamine

Dopamine is another neurotransmitter implicated in learning extinction across both appetitive and aversive domains.^[28] Dopamine signaling has been implicated in the extinction of conditioned fear^{[29][30][31][32][33]} and the extinction of drug-related learning^[34][35]

Circuitry

The brain region most extensively implicated in learning extinction is the infralimbic cortex (IL) of the medial prefrontal cortex (mPFC)^[36] The IL is important for the extinction of reward- and fear-associated behaviors, while the amygdala has been strongly implicated in the extinction of conditioned fear.^[4] The posterior cingulate cortex (PCC) and temporoparietal junction (TPJ) have also been identified as regions that may be associated with impaired extinction in adolescents.^[37]

Across development

There is a strong body of evidence to suggest that extinction alters across development.^[38][39] That is, learning extinction may differ during infancy, childhood, adolescence and adulthood. During infancy and childhood, learning extinction is especially persistent, which some have interpreted as erasure of the original CS-US association,^[40][41][42] but this remains contentious. In contrast, during adolescence and adulthood extinction is less persistent, which is interpreted as new learning of a CS-no US association that exists in tandem and opposition to the original CS-US memory.^[43][44]

See also

• Operant conditioning
• Post-traumatic stress disorder

References

1. Moreira, Márcio Borges. Princípios Básicos de Análise do Comportamento. artmed. ISBN 9788582715161.
2. Miltenberger, R. (2012). Behavior modification, principles and procedures. (5th ed., pp. 87-99). Wadsworth Publishing Company.
3. VanElzakker, M. B.; Dahlgren, M. K.; Davis, F. C.; Dubois, S.; Shin, L. M. (2014). "From Pavlov to PTSD: The extinction of conditioned fear in rodents, humans, and anxiety disorders". Neurobiology of Learning and Memory. 113: 3–18. doi:10.1016/j.nlm.2013.11.014. PMC 4156287. PMID 24321650.
4. Myers; Davis (2007). "Mechanisms of Fear Extinction". Molecular Psychiatry. 12 (2): 120–150. doi:10.1038/sj.mp.4001939. PMID 17160066.
5. Amano, T; Unal, CT; Paré, D (2010). "Synaptic correlates of fear extinction in the amygdala". Nature Neuroscience. 13 (4): 489–494. doi:10.1038/nn.2499. PMC 2847017. PMID 20208529.
6. Vargas, Julie S. (2013). Behavior Analysis for effective Teaching. New York: Routledge. p. 52.
7. B. F. Skinner (1979). The Shaping of a Behaviorist: Part Two of an Autobiography, p. 95.
8. Wheeler, John J. (2019). Behavior management : principles and practices of positive behavioral interventions and supports. David Dean Richey (4th ed.). New York, NY. ISBN 978-0-13-479218-7. OCLC 1008776079.
9. Thrailkill, Eric A.; Kimball, Ryan T.; Kelley, Michael E.; Craig, Andrew R.; Podlesnik, Christopher A. (2018). "Greater reinforcement rate during training increases spontaneous recovery: Spontaneous Recovery". Journal of the Experimental Analysis of Behavior. 109 (1): 238–252. doi:10.1002/jeab.307. PMID 29314021.
10. Applied behavior analysis for everyone : principles and practices explained by applied researchers who use them. Robert C. Pennington. Shawnee, KS: AAPC. 2019. p. 120. ISBN 978-1-942197-45-4. OCLC 1103852953.
11. Crawley, Daisy; Zhang, Lei; Jones, Emily J. H.; Ahmad, Jumana; Oakley, Bethany; San José Cáceres, Antonia; Charman, Tony; Buitelaar, Jan K.; Murphy, Declan G. M.; Chatham, Christopher; den Ouden, Hanneke (2020-10-27). "Modeling flexible behavior in childhood to adulthood shows age-dependent learning mechanisms and less optimal learning in autism in each age group". PLOS Biology. 18 (10): e3000908. doi:10.1371/journal.pbio.3000908. ISSN 1545-7885. PMC 7591042. PMID 33108370.
12. Rivers, Susan E.; Brackett, Marc A.; Reyes, Maria R.; Elbertson, Nicole A.; Salovey, Peter (2012-11-28). "Improving the Social and Emotional Climate of Classrooms: A Clustered Randomized Controlled Trial Testing the RULER Approach". Prevention Science. 14 (1): 77–87. doi:10.1007/s11121-012-0305-2. ISSN 1389-4986. PMID 23188089. S2CID 5616258.
13. Janney, Donna M.; Umbreit, John; Ferro, Jolenea B.; Liaupsin, Carl J.; Lane, Kathleen L. (2013). "The Effect of the Extinction Procedure in Function-Based Intervention". Journal of Positive Behavior Interventions. 15 (2): 113–123. doi:10.1177/1098300712441973. ISSN 1098-3007. S2CID 144675039.
14. Rajaraman, Adithyan; Hanley, Gregory P.; Gover, Holly C.; Staubitz, Johanna L.; Staubitz, John E.; Simcoe, Kathleen M.; Metras, Rachel (2022). "Minimizing Escalation by Treating Dangerous Problem Behavior Within an Enhanced Choice Model". Behavior Analysis in Practice. 15 (1): 219–242. doi:10.1007/s40617-020-00548-2. ISSN 1998-1929. PMC 8854458. PMID 35340377.
15. Rispoli, Mandy; Camargo, Siglia; Machalicek, Wendy; Lang, Russell; Sigafoos, Jeff (2014). "Functional communication training in the treatment of problem behavior maintained by access to rituals". Journal of Applied Behavior Analysis. 27 (47): 3. doi:10.1002/jaba.1994.27.issue-1. ISSN 0021-8855.
16. Falcomata, Terry S.; Hoffman, Katherine J.; Gainey, Summer; Muething, Colin S.; Fienup, Daniel M. (2013-07-10). "A Preliminary Evaluation of Reinstatement of Destructive Behavior Displayed by Individuals With Autism". The Psychological Record. 63 (3): 453–466. doi:10.11133/j.tpr.2013.63.3.004 (inactive 1 November 2024). S2CID 147662158.
17. Hanley, Gregory P.; Jin, C. Sandy; Vanselow, Nicholas R.; Hanratty, Laura A. (2014). "Producing meaningful improvements in problem behavior of children with autism via synthesized analyses and treatments: Severe Problem Behavior". Journal of Applied Behavior Analysis. 47 (1): 16–36. doi:10.1002/jaba.106. PMID 24615474.
18. Banda, Devender R.; McAfee, James K.; Hart, Stephanie L. (2009-06-03). "Decreasing Self-Injurious Behavior in a Student with Autism and Tourette Syndrome through Positive Attention and Extinction". Child & Family Behavior Therapy. 31 (2): 144–156. doi:10.1080/07317100902910604. ISSN 0731-7107. S2CID 144329726.
19. Allison, Janelle; Wilder, David A; Chong, Ivy; Lugo, Ashley; Pike, Jessica; Rudy, Nikki (2012). "A Comparison of Differential Reinforcement and Noncontingent Reinforcement to Treat Food Selectivity in a Child With Autism". Journal of Applied Behavior Analysis. 45 (3): 613–617. doi:10.1901/jaba.2012.45-613. PMC 3469290. PMID 23060675.
20. Myers, K. M.; Davis, M. (February 2007). "Mechanisms of fear extinction". Molecular Psychiatry. 12 (2): 120–150. doi:10.1038/sj.mp.4001939. ISSN 1476-5578. PMID 17160066.
21. Zürcher, Nicole R.; Walsh, Erin C.; Phillips, Rachel D.; Cernasov, Paul M.; Tseng, Chieh-En J.; Dharanikota, Ayarah; Smith, Eric; Li, Zibo; Kinard, Jessica L.; Bizzell, Joshua C.; Greene, Rachel K.; Dillon, Daniel; Pizzagalli, Diego A.; Izquierdo-Garcia, David; Truong, Kinh (2021-01-11). "A simultaneous [11C]raclopride positron emission tomography and functional magnetic resonance imaging investigation of striatal dopamine binding in autism". Translational Psychiatry. 11 (1): 33. doi:10.1038/s41398-020-01170-0. ISSN 2158-3188. PMC 7801430. PMID 33431841.
22. Pfeifer, Philippe; Sebastian, Alexandra; Buchholz, Hans Georg; Kaller, Christoph P.; Gründer, Gerhard; Fehr, Christoph; Schreckenberger, Mathias; Tüscher, Oliver (February 2022). "Prefrontal and striatal dopamine D2/D3 receptors correlate with fMRI BOLD activation during stopping". Brain Imaging and Behavior. 16 (1): 186–198. doi:10.1007/s11682-021-00491-y. ISSN 1931-7557. PMC 8825403. PMID 34403039.
23. Stark, Adam J.; Smith, Christopher T.; Petersen, Kalen J.; Trujillo, Paula; van Wouwe, Nelleke C.; Donahue, Manus J.; Kessler, Robert M.; Deutch, Ariel Y.; Zald, David H.; Claassen, Daniel O. (2018-01-01). "[18F]fallypride characterization of striatal and extrastriatal D2/3 receptors in Parkinson's disease". NeuroImage: Clinical. 18: 433–442. doi:10.1016/j.nicl.2018.02.010. ISSN 2213-1582. PMC 5849871. PMID 29541577.
24. Fullana, Miquel A.; Albajes-Eizagirre, Anton; Soriano-Mas, Carles; Vervliet, Bram; Cardoner, Narcís; Benet, Olívia; Radua, Joaquim; Harrison, Ben J. (2018-05-01). "Fear extinction in the human brain: A meta-analysis of fMRI studies in healthy participants". Neuroscience & Biobehavioral Reviews. 88: 16–25. doi:10.1016/j.neubiorev.2018.03.002. ISSN 0149-7634. PMID 29530516.
25. Riedel, Gernot; Platt, Bettina; Micheau, Jacques (2003-03-18). "Glutamate receptor function in learning and memory". Behavioural Brain Research. 140 (1–2): 1–47. doi:10.1016/s0166-4328(02)00272-3. ISSN 0166-4328. PMID 12644276. S2CID 41221872.
26. Kim, Jee Hyun; Perry, Christina; Luikinga, Sophia; Zbukvic, Isabel; Brown, Robyn M.; Lawrence, Andrew J. (2015-05-01). "Extinction of a cocaine-taking context that protects against drug-primed reinstatement is dependent on the metabotropic glutamate 5 receptor". Addiction Biology. 20 (3): 482–489. doi:10.1111/adb.12142. ISSN 1369-1600. PMID 24712397. S2CID 11626810.
27. Perry, Christina J; Reed, Felicia; Zbukvic, Isabel C; Kim, Jee Hyun; Lawrence, Andrew J (2016-01-01). "The metabotropic glutamate 5 receptor is necessary for extinction of cocaine associated cues". British Journal of Pharmacology. 173 (6): 1085–1094. doi:10.1111/bph.13437. ISSN 1476-5381. PMC 5341241. PMID 26784278.
28. Abraham, Antony D.; Neve, Kim A.; Lattal, K. Matthew (2014-02-01). "Dopamine and extinction: A convergence of theory with fear and reward circuitry". Neurobiology of Learning and Memory. 108: 65–77. doi:10.1016/j.nlm.2013.11.007. ISSN 1074-7427. PMC 3927738. PMID 24269353.
29. Haaker, Jan; Lonsdorf, Tina B.; Kalisch, Raffael (2015-10-01). "Effects of post-extinction l-DOPA administration on the spontaneous recovery and reinstatement of fear in a human fMRI study". European Neuropsychopharmacology. 25 (10): 1544–1555. doi:10.1016/j.euroneuro.2015.07.016. ISSN 1873-7862. PMID 26238968. S2CID 6242752.
30. Haaker, Jan; Gaburro, Stefano; Sah, Anupam; Gartmann, Nina; Lonsdorf, Tina B.; Meier, Kolja; Singewald, Nicolas; Pape, Hans-Christian; Morellini, Fabio (2013-06-25). "Single dose of L-dopa makes extinction memories context-independent and prevents the return of fear". Proceedings of the National Academy of Sciences of the United States of America. 110 (26): E2428–2436. Bibcode:2013PNAS..110E2428H. doi:10.1073/pnas.1303061110. ISSN 1091-6490. PMC 3696794. PMID 23754384.
31. Ponnusamy, Ravikumar; Nissim, Helen A.; Barad, Mark (2005-07-01). "Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice". Learning & Memory. 12 (4): 399–406. doi:10.1101/lm.96605. ISSN 1072-0502. PMC 1183258. PMID 16077018.
32. Zbukvic, Isabel C.; Ganella, Despina E.; Perry, Christina J.; Madsen, Heather B.; Bye, Christopher R.; Lawrence, Andrew J.; Kim, Jee Hyun (2016-03-05). "Role of Dopamine 2 Receptor in Impaired Drug-Cue Extinction in Adolescent Rats". Cerebral Cortex. 26 (6): 2895–904. doi:10.1093/cercor/bhw051. ISSN 1047-3211. PMC 4869820. PMID 26946126.
33. Madsen, Heather B.; Guerin, Alexandre A.; Kim, Jee Hyun (2017). "Investigating the role of dopamine receptor- and parvalbumin-expressing cells in extinction of conditioned fear". Neurobiology of Learning and Memory. 145: 7–17. doi:10.1016/j.nlm.2017.08.009. PMID 28842281. S2CID 26875742.
34. Abraham, Antony D.; Neve, Kim A.; Lattal, K. Matthew (2016-07-01). "Activation of D1/5 Dopamine Receptors: A Common Mechanism for Enhancing Extinction of Fear and Reward-Seeking Behaviors". Neuropsychopharmacology. 41 (8): 2072–2081. doi:10.1038/npp.2016.5. PMC 4908654. PMID 26763483.
35. Zbukvic, Isabel C.; Ganella, Despina E.; Perry, Christina J.; Madsen, Heather B.; Bye, Christopher R.; Lawrence, Andrew J.; Kim, Jee Hyun (2016-03-05). "Role of Dopamine 2 Receptor in Impaired Drug-Cue Extinction in Adolescent Rats". Cerebral Cortex. 26 (6): 2895–2904. doi:10.1093/cercor/bhw051. ISSN 1047-3211. PMC 4869820. PMID 26946126.
36. Do-Monte, Fabricio H.; Manzano-Nieves, Gabriela; Quiñones-Laracuente, Kelvin; Ramos-Medina, Liorimar; Quirk, Gregory J. (2015-02-25). "Revisiting the Role of Infralimbic Cortex in Fear Extinction with Optogenetics". The Journal of Neuroscience. 35 (8): 3607–3615. doi:10.1523/JNEUROSCI.3137-14.2015. ISSN 0270-6474. PMC 4339362. PMID 25716859.
37. Ganella, Despina E.; Drummond, Katherine D.; Ganella, Eleni P.; Whittle, Sarah; Kim, Jee Hyun (2018). "Extinction of Conditioned Fear in Adolescents and Adults: A Human fMRI Study". Frontiers in Human Neuroscience. 11: 647. doi:10.3389/fnhum.2017.00647. ISSN 1662-5161. PMC 5766664. PMID 29358913.
38. Yap, C.S., Richardson, R. (2007). "Extinction in the developing rat: an examination of renewal effects". Developmental Psychobiology. 49 (6): 565–575. CiteSeerX 10.1.1.583.1720. doi:10.1002/dev.20244. PMID 17680605.
39. Ganella, Despina E; Kim, Jee Hyun (2014-10-01). "Developmental rodent models of fear and anxiety: from neurobiology to pharmacology". British Journal of Pharmacology. 171 (20): 4556–4574. doi:10.1111/bph.12643. ISSN 1476-5381. PMC 4209932. PMID 24527726.
40. Kim, Jee Hyun; Richardson, Rick (2008-02-06). "The Effect of Temporary Amygdala Inactivation on Extinction and Reextinction of Fear in the Developing Rat: Unlearning as a Potential Mechanism for Extinction Early in Development". The Journal of Neuroscience. 28 (6): 1282–1290. doi:10.1523/JNEUROSCI.4736-07.2008. ISSN 0270-6474. PMC 6671587. PMID 18256248.
41. Kim, Jee Hyun; Richardson, Rick (2007). "A developmental dissociation in reinstatement of an extinguished fear response in rats". Neurobiology of Learning and Memory. 88 (1): 48–57. doi:10.1016/j.nlm.2007.03.004. PMID 17459734. S2CID 19611691.
42. Kim, Jee Hyun; Hamlin, Adam S.; Richardson, Rick (2009-09-02). "Fear Extinction across Development: The Involvement of the Medial Prefrontal Cortex as Assessed by Temporary Inactivation and Immunohistochemistry" (PDF). The Journal of Neuroscience. 29 (35): 10802–10808. doi:10.1523/JNEUROSCI.0596-09.2009. ISSN 0270-6474. PMC 6665532. PMID 19726637.
43. Kim, Jee Hyun; Li, Stella; Richardson, Rick (2010-06-24). "Immunohistochemical Analyses of Long-Term Extinction of Conditioned Fear in Adolescent Rats". Cerebral Cortex. 21 (3): 530–8. doi:10.1093/cercor/bhq116. hdl:10536/DRO/DU:30144599. ISSN 1047-3211. PMID 20576926.
44. Kim, Jee Hyun; Ganella, Despina E. (2015). "A Review of Preclinical Studies to Understand Fear During Adolescence". Australian Psychologist. 50 (1): 25–31. doi:10.1111/ap.12066. S2CID 142760996.