Periaqueductal Grey Differential Modulation of Nucleus Accumbens and Basolateral Amygdala Plasticity Under Controllable and Uncontrollable Stress

Overview

Journal Sci Rep

Specialty Science

Date 2017 Mar 30

PMID 28352073

Citations 3

Authors

Omer Horovitz

Alon Richter-Levin

Lin Xu

Liang Jing

Gal Richter-Levin

Affiliations

Soon will be listed here.

Abstract

Resilience has been conceptualized in part as a dynamic process that includes the ability to adapt to stressful conditions. As such it encompasses the extent to which neural plasticity may be promoted. The current study examined metaplasticity by referring to the "plasticity of synaptic plasticity" in a neural circuit composed of the basolateral amygdala (BLA) and the nucleus accumbens (NAcc), using behavioural stress controllability with or without preceding stimulation of the dorsal periaqueductal gray (i.e. dPAG priming). A tendency for increased plasticity in the controllable versus the uncontrollable group was found in both the BLA and NAcc. dPAG priming suppressed NAcc LTP in all groups, but it suppressed BLA LTP only in the uncontrollable group, demonstrating dissociation between either controllable and uncontrollable groups or the NAcc and BLA. Thus, metaplasticity in the dPAG-BLA-NAcc circuit regulated differentially by controllable or uncontrollable stress may underlie stress coping, and thus contribute to stress-related psychopathologies.

Citing Articles

Distinct Neural Representations and Cognitive Behaviors Attributable to Naturally Developed Active Avoidance or Reactive Escape Strategies in the Male Rat.

Jing L, Ma C, Xu L, Richter-Levin G Int J Neuropsychopharmacol. 2023; 26(11):761-772.

PMID: 37725443 PMC: 10674082. DOI: 10.1093/ijnp/pyad054.

Anterior cingulate cortex, but not amygdala, modulates the anxiogenesis induced by living with conspecifics subjected to chronic restraint stress in male mice.

Silveira L, Rodrigues Tavares L, Baptista-de-Souza D, Carmona I, Carneiro de Oliveira P, Nunes-de-Souza R Front Behav Neurosci. 2023; 16:1077368.

PMID: 36688134 PMC: 9853544. DOI: 10.3389/fnbeh.2022.1077368.

The Periaqueductal Gray and Its Extended Participation in Drug Addiction Phenomena.

Vazquez-Leon P, Miranda-Paez A, Chavez-Reyes J, Allende G, Barragan-Iglesias P, Marichal-Cancino B Neurosci Bull. 2021; 37(10):1493-1509.

PMID: 34302618 PMC: 8490541. DOI: 10.1007/s12264-021-00756-y.

References

Ilin Y, Richter-Levin G . ERK2 and CREB activation in the amygdala when an event is remembered as "Fearful" and not when it is remembered as "Instructive". J Neurosci Res. 2009; 87(8):1823-31. DOI: 10.1002/jnr.21994. View

Vollmayr B, Bachteler D, Vengeliene V, Gass P, Spanagel R, Henn F . Rats with congenital learned helplessness respond less to sucrose but show no deficits in activity or learning. Behav Brain Res. 2004; 150(1-2):217-21. DOI: 10.1016/S0166-4328(03)00259-6. View

Maier S, Anderson C, Lieberman D . Influence of control of shock on subsequent shock-elicited aggression. J Comp Physiol Psychol. 1972; 81(1):94-100. DOI: 10.1037/h0033329. View

Kim E, Pellman B, Kim J . Stress effects on the hippocampus: a critical review. Learn Mem. 2015; 22(9):411-6. PMC: 4561403. DOI: 10.1101/lm.037291.114. View

Dolen G, Darvishzadeh A, Huang K, Malenka R . Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature. 2013; 501(7466):179-84. PMC: 4091761. DOI: 10.1038/nature12518. View

Anisman H, Matheson K . Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev. 2005; 29(4-5):525-46. DOI: 10.1016/j.neubiorev.2005.03.007. View

Panksepp J . Cross-species affective neuroscience decoding of the primal affective experiences of humans and related animals. PLoS One. 2011; 6(9):e21236. PMC: 3168430. DOI: 10.1371/journal.pone.0021236. View

Misslin R . The defense system of fear: behavior and neurocircuitry. Neurophysiol Clin. 2003; 33(2):55-66. DOI: 10.1016/s0987-7053(03)00009-1. View

Amat J, Matus-Amat P, Watkins L, Maier S . Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Res. 1998; 797(1):12-22. DOI: 10.1016/s0006-8993(98)00368-0. View

10.

Cabib S, Puglisi-Allegra S . Opposite responses of mesolimbic dopamine system to controllable and uncontrollable aversive experiences. J Neurosci. 1994; 14(5 Pt 2):3333-40. PMC: 6577451. View

11.

Maier S . Behavioral control blunts reactions to contemporaneous and future adverse events: medial prefrontal cortex plasticity and a corticostriatal network. Neurobiol Stress. 2014; 1:12-22. PMC: 4260419. DOI: 10.1016/j.ynstr.2014.09.003. View

12.

Day J, Carelli R . The nucleus accumbens and Pavlovian reward learning. Neuroscientist. 2007; 13(2):148-59. PMC: 3130622. DOI: 10.1177/1073858406295854. View

13.

Horovitz O, Richter-Levin G . Dorsal periaqueductal gray simultaneously modulates ventral subiculum induced-plasticity in the basolateral amygdala and the nucleus accumbens. Front Behav Neurosci. 2015; 9:53. PMC: 4349162. DOI: 10.3389/fnbeh.2015.00053. View

14.

Berton O, Covington 3rd H, Ebner K, Tsankova N, Carle T, Ulery P . Induction of deltaFosB in the periaqueductal gray by stress promotes active coping responses. Neuron. 2007; 55(2):289-300. DOI: 10.1016/j.neuron.2007.06.033. View

15.

Sapolsky R . Stress hormones: good and bad. Neurobiol Dis. 2000; 7(5):540-2. DOI: 10.1006/nbdi.2000.0350. View

16.

Amat J, Aleksejev R, Paul E, Watkins L, Maier S . Behavioral control over shock blocks behavioral and neurochemical effects of later social defeat. Neuroscience. 2009; 165(4):1031-8. PMC: 2847505. DOI: 10.1016/j.neuroscience.2009.11.005. View

17.

Lei Z, Liu B, Wang J . Reward memory relieves anxiety-related behavior through synaptic strengthening and protein kinase C in dentate gyrus. Hippocampus. 2015; 26(4):502-16. DOI: 10.1002/hipo.22540. View

18.

Likhtik E, Paz R . Amygdala-prefrontal interactions in (mal)adaptive learning. Trends Neurosci. 2015; 38(3):158-66. PMC: 4352381. DOI: 10.1016/j.tins.2014.12.007. View

19.

Maier S, Watkins L . Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev. 2005; 29(4-5):829-41. DOI: 10.1016/j.neubiorev.2005.03.021. View

20.

Overmier J, Seligman M . Effects of inescapable shock upon subsequent escape and avoidance responding. J Comp Physiol Psychol. 1967; 63(1):28-33. DOI: 10.1037/h0024166. View