Single-unit Activity in the Medial Prefrontal Cortex During Immediate and Delayed Extinction of Fear in Rats

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2010 Aug 12

PMID 20700483

Citations 66

Authors

Chun-Hui Chang

Joshua D Berke

Stephen Maren

Affiliations

Soon will be listed here.

Abstract

Delivering extinction trials minutes after fear conditioning yields only a short-term fear suppression that fully recovers the following day. Because extinction has been reported to increase CS-evoked spike firing and spontaneous bursting in the infralimbic (IL) division of the medial prefrontal cortex (mPFC), we explored the possibility that this immediate extinction deficit is related to altered mPFC function. Single-units were simultaneously recorded in rats from neurons in IL and the prelimbic (PrL) division of the mPFC during an extinction session conducted 10 minutes (immediate) or 24 hours (delayed) after auditory fear conditioning. In contrast to previous reports, IL neurons exhibited CS-evoked responses early in extinction training in both immediate and delayed conditions and these responses decreased in magnitude over the course of extinction training. During the retention test, CS-evoked firing in IL was significantly greater in animals that failed to acquire extinction. Spontaneous bursting during the extinction and test sessions was also different in the immediate and delayed groups. There were no group differences in PrL activity during extinction or retention testing. Alterations in both spontaneous and CS-evoked neuronal activity in the IL may contribute to the immediate extinction deficit.

Citing Articles

Distinct neural responses of ventromedial prefrontal cortex-projecting nucleus reuniens neurons during aversive memory extinction.

Mochizuki Y, Joji-Nishino A, Emoto K, Uematsu A Mol Brain. 2025; 18(1):18.

PMID: 40045388 PMC: 11881366. DOI: 10.1186/s13041-025-01185-y.

Circadian Rhythms in Conditioned Threat Extinction Reflect Time-of-Day Differences in Ventromedial Prefrontal Cortex Neural Processing.

Hartsock M, Levy C, Navarro M, Saddoris M, Spencer R J Neurosci. 2024; 44(39).

PMID: 39251355 PMC: 11426375. DOI: 10.1523/JNEUROSCI.0878-24.2024.

Quantification of prefrontal cortical neuronal ensembles following conditioned fear learning in a Fos-LacZ transgenic rat with photoacoustic imaging .

Matchynski J, Cilley T, Sadik N, Makki K, Wu M, Manwar R Photoacoustics. 2023; 33:100551.

PMID: 38021296 PMC: 10658601. DOI: 10.1016/j.pacs.2023.100551.

The Role of Expectancy Violation in Extinction Learning: A Two-Day Online Fear Conditioning Study.

Gromer D, Hildebrandt L, Stegmann Y Clin Psychol Eur. 2023; 5(2):e9627.

PMID: 37732150 PMC: 10508258. DOI: 10.32872/cpe.9627.

Parvalbumin-Positive Interneurons in the Medial Prefrontal Cortex Regulate Stress-Induced Fear Extinction Impairments in Male and Female Rats.

Binette A, Liu J, Bayer H, Crayton K, Melissari L, Sweck S J Neurosci. 2023; 43(22):4162-4173.

PMID: 37127359 PMC: 10255009. DOI: 10.1523/JNEUROSCI.1442-22.2023.

References

Maroun M . Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala. Eur J Neurosci. 2006; 24(10):2917-22. DOI: 10.1111/j.1460-9568.2006.05169.x. View

McDonald A, Mascagni F, Guo L . Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience. 1996; 71(1):55-75. DOI: 10.1016/0306-4522(95)00417-3. View

Bisson J, Jenkins P, Alexander J, Bannister C . Randomised controlled trial of psychological debriefing for victims of acute burn trauma. Br J Psychiatry. 1997; 171:78-81. DOI: 10.1192/bjp.171.1.78. View

LeDoux J . Emotion circuits in the brain. Annu Rev Neurosci. 2000; 23:155-84. DOI: 10.1146/annurev.neuro.23.1.155. View

Maren S . Auditory fear conditioning increases CS-elicited spike firing in lateral amygdala neurons even after extensive overtraining. Eur J Neurosci. 2000; 12(11):4047-54. DOI: 10.1046/j.1460-9568.2000.00281.x. View

Chang C, Maren S . Early extinction after fear conditioning yields a context-independent and short-term suppression of conditional freezing in rats. Learn Mem. 2009; 16(1):62-8. PMC: 2632848. DOI: 10.1101/lm.1085009. View

Likhtik E, Popa D, Apergis-Schoute J, Fidacaro G, Pare D . Amygdala intercalated neurons are required for expression of fear extinction. Nature. 2008; 454(7204):642-5. PMC: 2528060. DOI: 10.1038/nature07167. View

Buzsaki G, Csicsvari J, Dragoi G, Harris K, Henze D, Hirase H . Homeostatic maintenance of neuronal excitability by burst discharges in vivo. Cereb Cortex. 2002; 12(9):893-9. DOI: 10.1093/cercor/12.9.893. View

Norrholm S, Vervliet B, Jovanovic T, Boshoven W, Myers K, Davis M . Timing of extinction relative to acquisition: a parametric analysis of fear extinction in humans. Behav Neurosci. 2008; 122(5):1016-30. PMC: 3731450. DOI: 10.1037/a0012604. View

10.

Pare D, Quirk G, LeDoux J . New vistas on amygdala networks in conditioned fear. J Neurophysiol. 2004; 92(1):1-9. DOI: 10.1152/jn.00153.2004. View

11.

Rasmusson A, Charney D . Animal models of relevance to PTSD. Ann N Y Acad Sci. 1997; 821:332-51. DOI: 10.1111/j.1749-6632.1997.tb48290.x. View

12.

Maren S . Building and burying fear memories in the brain. Neuroscientist. 2005; 11(1):89-99. DOI: 10.1177/1073858404269232. View

13.

Maren S, Chang C . Recent fear is resistant to extinction. Proc Natl Acad Sci U S A. 2006; 103(47):18020-5. PMC: 1693865. DOI: 10.1073/pnas.0608398103. View

14.

Maren S, Quirk G . Neuronal signalling of fear memory. Nat Rev Neurosci. 2004; 5(11):844-52. DOI: 10.1038/nrn1535. View

15.

Herry C, Garcia R . Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci. 2002; 22(2):577-83. PMC: 6758664. View

16.

Sotres-Bayon F, Diaz-Mataix L, Bush D, LeDoux J . Dissociable roles for the ventromedial prefrontal cortex and amygdala in fear extinction: NR2B contribution. Cereb Cortex. 2008; 19(2):474-82. PMC: 2626130. DOI: 10.1093/cercor/bhn099. View

17.

Rothbaum B, Davis M . Applying learning principles to the treatment of post-trauma reactions. Ann N Y Acad Sci. 2004; 1008:112-21. DOI: 10.1196/annals.1301.012. View

18.

Garcia R, Chang C, Maren S . Electrolytic lesions of the medial prefrontal cortex do not interfere with long-term memory of extinction of conditioned fear. Learn Mem. 2006; 13(1):14-7. PMC: 1360128. DOI: 10.1101/lm.60406. View

19.

Wiltschko A, Pettibone J, Berke J . Opposite effects of stimulant and antipsychotic drugs on striatal fast-spiking interneurons. Neuropsychopharmacology. 2010; 35(6):1261-70. PMC: 3055348. DOI: 10.1038/npp.2009.226. View

20.

Quirk G, Mueller D . Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology. 2007; 33(1):56-72. PMC: 2668714. DOI: 10.1038/sj.npp.1301555. View