2018/04/12

2018/04/12 榎本

Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions

Justin M. Moscarello and Joseph E. LeDoux
J Neurosci. 2013 Feb 27;33(9):3815-23.

Abstract
Signaled active avoidance (AA) paradigms train subjects to prevent an aversive outcome by performing a learned behavior during the presentation of a conditioned cue. This complex form of conditioning involves pavlovian and instrumental components, which produce competing behavioral responses that must be reconciled for the subject to successfully avoid an aversive stimulus. In signaled AA paradigm for rat, we tested the hypothesis that the instrumental component of AA training recruits infralimbic prefrontal cortex (ilPFC) to inhibit central amygdala (CeA)-mediated Pavlovian reactions. Pretraining lesions of ilPFC increased conditioned freezing while causing a corresponding decrease in avoidance; lesions of CeA produced opposite effects, reducing freezing and facilitating avoidance behavior. Pharmacological inactivation experiments demonstrated that ilPFC is relevant to both acquisition and expression phases of AA learning. Inactivation experiments also revealed that AA produces an ilPFC-mediated diminution of pavlovian reactions that extends beyond the training context, even when the conditioned stimulus is presented in an environment that does not allow the avoidance response. Finally, injection of a protein synthesis inhibitor into either ilPFC or CeA impaired or facilitated AA, respectively, showing that avoidance training produces two opposing memory traces in these regions. These data support a model in which AA learning recruits ilPFC to inhibit CeA-mediated defense behaviors, leading to a robust suppression of freezing that generalizes across environments. Thus, ilPFC functions as an inhibitory interface, allowing instrumental control over an aversive outcome to attenuate the expression of freezing and other reactions to conditioned threat.
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レビューがいくつか出ています。

Surviving threats: neural circuit and computational implications of a new taxonomy of defensive behaviour.
Joseph LeDoux & Nathaniel D. Daw
Nat Rev Neurosci. 2018 Mar 29. doi: 10.1038/nrn.2018.22.
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New perspectives on central amygdala function.
Jonathan P Fadok, Milica Markovic, Philip Tovote, Andreas Luthi
Curr Opin Neurobiol. 2018 Apr;49:141-147. doi: 10.1016/j.conb.2018.02.009.
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Basolateral amygdala circuitry in positive and negative valence.
Pia-Kelsey O’Neill, Felicity Gore, C Daniel Salzman
Curr Opin Neurobiol. 2018 Apr;49:175-183. doi: 10.1016/j.conb.2018.02.012.
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2018/03/23

2018/03/23 春野

Gating of Fear in Prelimbic Cortex by Hippocampal and Amygdala Inputs

Francisco Sotres-Bayon, Demetrio Sierra-Mercado, Enmanuelle Pardilla-Delgado, Gregory J. Quirk
Neuron. 2012 Nov 21;76(4):804-12. doi: 10.1016/j.neuron.2012.09.028.

Highlights
  • In behaving rats, BLA excites projection cells and vHPC excites interneurons in PL
  • BLA promotes fear-signaling in PL, whereas vHPC inhibits it
  • vHPC inhibits fear expression after, but not before, extinction
  • vHPC gates fear expression via the PL after, but not before, extinction
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2018/03/09

2018/03/09 榎本

Amygdala and Ventral Striatum Make Distinct Contributions to Reinforcement Learning

Vincent D. Costa, Olga Dal Monte, Daniel R. Lucas, Elisabeth A. Murray, Bruno B. Averbeck
Neuron. 2016 Oct 19;92(2):505-517. doi: 10.1016/j.neuron.2016.09.025.

Highlights
  • The amygdala is necessary for deterministic and stochastic reinforcement learning
  • The ventral striatum is only necessary for learning stochastic reward associations
  • Amygdala and ventral striatum lesions decrease choice consistency
  • Ventral striatum lesions hasten choice reaction times leading to more errors

これまでいろいろと見てきましたが、扁桃体を含んだ神経回路にどのような計算モデルが実装されているか、というのはまだ判然としませんし、そこに挑んでいる仕事もまだ多くありません。今回の論文は扁桃体と腹側線条体を損傷させたサルに確率的な行動選択課題を行わせ、強化学習モデルなどの計算モデルを当てはめることで、その問題にアプローチしています。

両側で扁桃体(イボテン酸使用)もしくは側坐核(キノリン酸使用)を損傷させ、一般的なTwo-arms bandit taskをやらせます。動物の行動は正と負のフィードバックそれぞれに別の学習率をおく強化学習モデルで(ベイズモデルやPearce-Hallモデルよりも)よりよく推定できました。扁桃体損傷動物ではタスク全体的に学習率が落ちますが、線条体損傷動物では確率的な課題条件でのみ学習率が下がっていました。また選択行動はどちらも雑になります(行動の一貫性……逆温度が低くなる)が、線条体損傷動物でのみ反応時間が短く(衝動的に)なりました。

今回の結果からでは神経回路についてはもちろん、BLAやCeA、NAc shellとNAc coreの違いなどについては何も分かりませんが、このような計算論的アプローチと最新の手法とを組み合わせることで、重要な問題解決につながるのでは、という示唆を得られました。

最近の報告


Reversal Learning and Dopamine: A Bayesian Perspective
Vincent D. Costa, Valery L. Tran, Janita Turchi and Bruno B. Averbeck
J Neurosci. 2015 Feb 11;35(6):2407-16. doi: 10.1523/JNEUROSCI.1989-14.2015.
同じタスクでドパミンをコントロールしてベイズ/強化学習で行動モデルに当てはめています。ベイズは今回ぜんぜんダメでしたけど……。


おまけです。
Long time-scales in primate amygdala neurons support aversive learning
Aryeh H. Taub, Tamar Stolero, Uri Livneh, Yosef Shohat, Rony Paz

2018/02/23

2018/02/23 春野

Shared neural coding for social hierarchy and reward value in primate amygdala

Jérôme Munuera, Mattia Rigotti & C. Daniel Salzman
Nat Neurosci. 2018 Mar;21(3):415-423. doi: 10.1038/s41593-018-0082-8.

Abstract
The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli.

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2018/02/14

2018/2/14 木村

Multiple systems for emotion-based action selection in the amygdala




Htr2a-Expressing Cells in the Central Amygdala Control the Hierarchy between Innate and Learned Fear

Tomoko Isosaka, Tomohiko Matsuo, Takashi Yamaguchi, Kazuo Funabiki, Shigetada Nakanishi, Reiko Kobayakawa, Ko Kobayakawa
Cell. 2015 Nov 19;163(5):1153-1164. doi: 10.1016/j.cell.2015.10.047.

Highlights
  • A hierarchical relationship exists between innate- and learned-fear responses 
  • Innate but not learned-fear stimuli suppress the activity of CeA Htr2a+ cells 
  • CeA Htr2a+ cell inhibition up/downregulates innate/learned freezing, respectively 
  • CeA Htr2a+ cells act as a hierarchy generator prioritizing innate over learned fear


A competitive inhibitory circuit for selection of active and passive fear responses

Jonathan P. Fadok, Sabine Krabbe, Milica Markovic, Julien Courtin, Chun Xu, Lema Massi, Paolo Botta, Kristine Bylund, Christian Müller, Aleksandar Kovacevic, Philip Tovote & Andreas Lüthi
Nature. 2017 Feb 2;542(7639):96-100. doi: 10.1038/nature21047.

Abstract
When faced with threat, the survival of an organism is contingent upon the selection of appropriate active or passive behavioural responses. Freezing is an evolutionarily conserved passive fear response that has been used extensively to study the neuronal mechanisms of fear and fear conditioning in rodents. However, rodents also exhibit active responses such as flight under natural conditions. The central amygdala (CEA) is a forebrain structure vital for the acquisition and expression of conditioned fear responses, and the role of specific neuronal sub-populations of the CEA in freezing behaviour is well-established. Whether the CEA is also involved in flight behaviour, and how neuronal circuits for active and passive fear behaviour interact within the CEA, are not yet understood. Here, using in vivo optogenetics and extracellular recordings of identified cell types in a behavioural model in which mice switch between conditioned freezing and flight, we show that active and passive fear responses are mediated by distinct and mutually inhibitory CEA neurons. Cells expressing corticotropin-releasing factor (CRF+) mediate conditioned flight, and activation of somatostatin-positive (SOM+) neurons initiates passive freezing behaviour. Moreover, we find that the balance between conditioned flight and freezing behaviour is regulated by means of local inhibitory connections between CRF+ and SOM+ neurons, indicating that the selection of appropriate behavioural responses to threat is based on competitive interactions between two defined populations of inhibitory neurons, a circuit motif allowing for rapid and flexible action selection.
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2018/2/14 榎本

Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment

Burgos-Robles A, Kimchi EY, IzadmehrEM, PorzenheimMJ, Ramos-GuaspWA, NiehEH, Felix-Ortiz AC, NamburiP, LepplaCA, PresbreyKN, AnandalingamKK, Pagan-Rivera PA, AnahtarM, BeyelerA, TyeKM.
Nat Neurosci. 2017 Jun;20(6):824-835. doi: 10.1038/nn.4553.

報酬+嫌悪条件下において扁桃体BLAと内側前頭前野PL(前辺縁皮質)領域との相互神経連絡がもつ行動情報。砂糖水も貰えるけれどもフットショックもくるアンビバレントな課題。ラットで電気生理実験と相互相関解析、オプトジェネティクスやDREADDなんかも用いて、BLA→PL投射がショックを予告する刺激に対してフリージングを引き起こすに必要十分であることを示しています。機械学習で(いちおう)行動予測もできる。

PLはIL(下辺縁皮質)とも相互連絡があり、どちらも腹側海馬から入力を受けて扁桃体や側坐核に投射しています。かねてより恐怖学習・消去、薬物依存などのパラダイムで役割の違いなどについて調べられており、ここ数年でその神経回路メカニズムが明らかになりつつあります。PL・ILはヒトやサルにおける帯状皮質の一部ですので、そのへんの対応関係にも注意してまとめてみたいと思います。つづく。



参考文献

Prefrontal control of fear: more than just extinction.
Sotres-Bayon F, Quirk GJ.
Curr Opin Neurobiol. 2010 Apr;20(2):231-5. doi: 10.1016/j.conb.2010.02.005.

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Long-range connectivity defines behavioral specificity of amygdala neurons.
Senn V, Wolff SB, Herry C, Grenier F, Ehrlich I, Gründemann J, Fadok JP, Müller C, Letzkus JJ, Lüthi A.
Neuron. 2014 Jan 22;81(2):428-37. doi: 10.1016/j.neuron.2013.11.006.

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Functional Connectivity between Amygdala and Cingulate Cortex for Adaptive Aversive Learning
Oded Klavir, Rotem Genud-Gabai, Rony Paz
Neuron. 2013 Dec 4;80(5):1290-300. doi: 10.1016/j.neuron.2013.09.035.

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Selective inhibitory control of pyramidal neuron ensembles and cortical subnetworks by chandelier cells.
Lu J, Tucciarone J, Padilla-Coreano N, He M, Gordon JA, Huang ZJ.
Nat Neurosci. 2017 Oct;20(10):1377-1383. doi: 10.1038/nn.4624.

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Combined Social and Spatial Coding in a Descending Projection from the Prefrontal Cortex.
Murugan M, Jang HJ, Park M, Miller EM, Cox J, Taliaferro JP, Parker NF, Bhave V, Hur H, Liang Y, Nectow AR, Pillow JW, Witten IB.
Cell. 2017 Dec 14;171(7):1663-1677.e16. doi: 10.1016/j.cell.2017.11.002.

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2018/01/31

2018/1/31 木村

扁桃体の行動学習と記憶:神経回路と情報(1)

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Amygdala microcircuits controlling learned fear.

Sevil Duvarci, Denis Pare
Neuron. 2014 Jun 4;82(5):966-80. doi: 10.1016/j.neuron.2014.04.042.


Molecular Mechanisms of Fear Learning and Memory

Joshua P. Johansen, Christopher K. Cain, Linnaea E. Ostroff, Joseph E. LeDoux
Neuron. 2004 Sep 30;44(1):75-91.


Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation

Joshua P. Johansen, Lorenzo Diaz-Mataix, Hiroki Hamanaka, Takaaki Ozawa, Edgar Ycu, Jenny Koivumaa, Ashwani Kumar, Mian Hou, Karl Deisseroth, Edward S. Boyden and Joseph E. LeDoux
Proc Natl Acad Sci U S A. 2014 Dec 23;111(51):E5584-92. doi: 10.1073/pnas.1421304111.


Modular organization of the brainstem noradrenaline system coordinates opposing learning states

Akira Uematsu, Bao Zhen Tan, Edgar A Ycu, Jessica Sulkes Cuevas, Jenny Koivumaa, Felix Junyent, Eric J Kremer, Ilana B Witten, Karl Deisseroth & Joshua P Johansen
Nat Neurosci. 2017 Nov;20(11):1602-1611. doi: 10.1038/nn.4642.


Cholinergic Signaling Controls Conditioned Fear Behaviors and Enhances Plasticity of Cortical-Amygdala Circuits

Li Jiang, Srikanya Kundu, James D. Lederman, Gretchen Y. López-Hernández, Elizabeth C. Ballinger, Shaohua Wang, David A. Talmage, Lorna W. Role
Neuron. 2016 Jun 1;90(5):1057-70. doi: 10.1016/j.neuron.2016.04.028.

2018/01/24

2016/1/24 榎本

Paraventricular Thalamus Balances Danger and Reward

Eun A. Choi and Gavan P. McNally
J Neurosci. 2017 Mar 15;37(11):3018-3029.

視床室傍核(PVT / Pa: Paraventricular nucleus of thalamus)と視床下部室傍核(PVN / PVH: Paraventricular hypothalamic nucleus)は別の神経核であることにご注意ください。略称統一してほしい……今回はPVTの話です。

PVTは脳幹や視床下部から入力をうけ、辺縁皮質(PL, IL)や島皮質と相互連絡、側坐核や扁桃体中心核(CeA)、分界条床核(BST)や前交連後肢間質核(IPAC)なんかに出力します。睡眠/覚醒や摂食制御、不安やムード、ストレスなどに関わる機能について調べられてきましたが、近年の計測制御技術興隆の恩恵をうけ、より精密な神経回路メカニズムが明らかになりつつあります。今回は報酬とフットショックがくる相克的な条件の課題を学習させたラットを用い、DREADDでPVTを可逆的に不活性化させてフリージング/報酬接近行動を観察することにより、一見矛盾するような結果を示しています。



参考文献

High field FMRI reveals thalamocortical integration of segregated cognitive and emotional processing in mediodorsal and intralaminar thalamic nuclei.
Metzger CD1, Eckert U, Steiner J, Sartorius A, Buchmann JE, Stadler J, Tempelmann C, Speck O, Bogerts B, Abler B, Walter M.
Front Neuroanat. 2010 Nov 1;4:138.

ヒトfMRIでPVTの活動を報告しているのは今のところこれだけ。セクシー画像で興奮するみたい。


Placing the paraventricular nucleus of the thalamus within the brain circuits that control behavior.
Kirouac GJ.
Neurosci Biobehav Rev. 2015 Sep;56:315-29.


A thalamic input to the nucleus accumbens mediates opiate dependence
Yingjie Zhu, Carl F. R. Wienecke, Gregory Nachtrab& Xiaoke Chen
Nature. 2016 Feb 11;530(7589):219-22.


A food-predictive cue attributed with incentive salience engages subcortical afferents and efferents of the paraventricular nucleus of the thalamus.
Haight JL, Fuller ZL, Fraser KM, Flagel SB.
Neuroscience. 2017 Jan 6;340:135-152.


Contributions of the paraventricular thalamic nucleus in the regulation of stress, motivation, and mood.
Hsu DT, Kirouac GJ, Zubieta JK, Bhatnagar S.
Front Behav Neurosci. 2014 Mar 11;8:73.

サルです。PaというのがPVT。

2018/01/17

2018/01/17 春野

Aversive Prediction Errorはどこにありどう学習に使われるのか?

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Dysregulation of aversive signaling pathways: a novel circuit endophenotype for pain and anxiety disorders.

Li-Feng Yeh, Mayumi Watanabe, Jessica Sulkes-Cuevas, Joshua P Johansen
Curr Opin Neurobiol. 2017 Sep 28;48:37-44.

abstract
Aversive experiences activate dedicated neural instructive pathways which trigger memory formation and change behavior. The strength of these aversive memories and the degree to which they alter behavior is proportional to the intensity of the aversive experience. Dysregulation of aversive learning circuits can lead to psychiatric pathology. Here we review recent findings elucidating aversive instructive signaling circuits for fear conditioning. We then examine how chronic pain as well as stress and anxiety disrupt these circuits and the implications this has for understanding and treating psychiatric disease. Together this review synthesizes current work on aversive instructive signaling circuits in health and disease and suggests a novel circuit based framework for understanding pain and anxiety syndromes.
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A temporal shift in the circuits mediating retrieval of fear memory.


Fabricio H. Do-Monte, Kelvin Quiñones-Laracuente & Gregory J. Quirk
Nature. 2015 Mar 26;519(7544):460-3.

abstract
Fear memories allow animals to avoid danger, thereby increasing their chances of survival. Fear memories can be retrieved long after learning, but little is known about how retrieval circuits change with time. Here we show that the dorsal midline thalamus of rats is required for the retrieval of auditory conditioned fear at late (24 hours, 7 days, 28 days), but not early (0.5 hours, 6 hours) time points after learning. Consistent with this, the paraventricular nucleus of the thalamus (PVT), a subregion of the dorsal midline thalamus, showed increased c-Fos expression only at late time points, indicating that the PVT is gradually recruited for fear retrieval. Accordingly, the conditioned tone responses of PVT neurons increased with time after training. The prelimbic (PL) prefrontal cortex, which is necessary for fear retrieval, sends dense projections to the PVT. Retrieval at late time points activated PL neurons projecting to the PVT, and optogenetic silencing of these projections impaired retrieval at late, but not early, time points. In contrast, silencing of PL inputs to the basolateral amygdala impaired retrieval at early, but not late, time points, indicating a time-dependent shift in retrieval circuits. Retrieval at late time points also activated PVT neurons projecting to the central nucleus of the amygdala, and silencing these projections at late, but not early, time points induced a persistent attenuation of fear. Thus, the PVT may act as a crucial thalamic node recruited into cortico-amygdalar networks for retrieval and maintenance of long-term fear memories.
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Placing prediction into the fear circuit.

Gavan P. McNally, Gavan P. McNally, Joshua P. Johansen, Hugh T. Blair
Trends Neurosci. 2011 Jun;34(6):283-92.

Abstract
Pavlovian fear conditioning depends on synaptic plasticity at amygdala neurons. Here, we review recent electrophysiological, molecular and behavioral evidence suggesting the existence of a distributed neural circuitry regulating amygdala synaptic plasticity during fear learning. This circuitry, which involves projections from the midbrain periaqueductal gray region, can be linked to prediction error and expectation modulation of fear learning, as described by associative and computational learning models. It controls whether, and how much, fear learning occurs by signaling aversive events when they are unexpected. Functional neuroimaging and clinical studies indicate that this prediction circuit is recruited in humans during fear learning and contributes to exposure-based treatments for clinical anxiety. This aversive prediction error circuit might represent a conserved mechanism for regulating fear learning in mammals.
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Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray.

Joshua P Johansen, Jason W Tarpley, Joseph E LeDoux & Hugh T Blair
Nat Neurosci. 2010 Aug;13(8):979-86. doi: 10.1038/nn.2594.

Abstract
A form of aversively motivated learning called fear conditioning occurs when a neutral conditioned stimulus is paired with an aversive unconditioned stimulus (UCS). UCS-evoked depolarization of amygdala neurons may instruct Hebbian plasticity that stores memories of the conditioned stimulus-unconditioned stimulus association, but the origin of UCS inputs to the amygdala is unknown. Theory and evidence suggest that instructive UCS inputs to the amygdala will be inhibited when the UCS is expected, but this has not been found during fear conditioning. We investigated neural pathways that relay information about the UCS to the amygdala by recording neurons in the amygdala and periaqueductal gray (PAG) of rats during fear conditioning. UCS-evoked responses in both amygdala and PAG were inhibited by expectation. Pharmacological inactivation of the PAG attenuated UCS-evoked responses in the amygdala and impaired acquisition of fear conditioning, indicating that PAG may be an important part of the pathway that relays instructive signals to the amygdala.
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A feedback neural circuit for calibrating aversive memory strength.

Takaaki Ozawa, Edgar A Ycu, Ashwani Kumar, Li-Feng Yeh, Touqeer Ahmed, Jenny Koivumaa & Joshua P Johansen
Nat Neurosci. 2017 Jan;20(1):90-97. doi: 10.1038/nn.4439.

Abstract
Aversive experiences powerfully regulate memory formation, and memory strength is proportional to the intensity of these experiences. Inhibition of the neural circuits that convey aversive signals when they are predicted by other sensory stimuli is hypothesized to set associative memory strength. However, the neural circuit mechanisms that produce this predictive inhibition to regulate memory formation are unknown. Here we show that predictive sensory cues recruit a descending feedback circuit from the central amygdala that activates a specific population of midbrain periaqueductal gray pain-modulatory neurons to control aversive memory strength. Optogenetic inhibition of this pathway disinhibited predicted aversive responses in lateral amygdala neurons, which store fear memories, resulting in the resetting of fear learning levels. These results reveal a control mechanism for calibrating learning signals to adaptively regulate the strength of behavioral learning. Dysregulation of this circuit could contribute to psychiatric disorders associated with heightened fear responsiveness.
恐怖記憶の強さを制御するフィードバック機構 : ライフサイエンス 新着論文レビュー
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Hypothalamic corticotropin-releasing factor is centrally involved in learning under moderate stress.

Morgan Lucas, Alon Chen & Gal Richter-Levin
Neuropsychopharmacology. 2013 Aug;38(9):1825-32. doi: 10.1038/npp.2013.82.

Abstract
The corticotropin-releasing factor (CRF) neuropeptide is found to have a pivotal role in the regulation of the behavioral and neuroendocrine responses to stressful challenges. Here, we studied the involvement of the hypothalamic CRF in learning under stressful conditions. We have used a site-specific viral approach to knockdown (KD) CRF expression in the paraventricular nucleus of the hypothalamus (PVN). The two-way shuttle avoidance (TWSA) task was chosen to assess learning and memory under stressful conditions. Control animals learned to shuttle from one side to the other to avoid electrical foot shock by responding to a tone. Novel object and social recognition tasks were used to assess memory under less stressful conditions. KD of PVN-CRF expression decreased the number of avoidance responses in a TWSA session under moderate (0.8 mA), but not strong (1.5 mA), stimulus intensity compared to control rats. On the other hand, KD of PVN-CRF had no effect on memory performance in the less stressful novel object or social recognition tasks. Interestingly, basal or stress-induced corticosterone levels in CRF KD rats were not significantly different from controls. Taken together, the data suggest that the observed impairment was not a result of alteration in HPA axis activity, but rather due to reduced PVN-CRF activity on other brain areas. We propose that hypothalamic CRF is centrally involved in learning under moderate stressful challenge. Under 'basal' (less stressful) conditions or when the intensity of the stress is more demanding, central CRF ceases to be the determinant factor, as was indicated by performances in the TWSA with higher stimulus intensity or in the less stressful tasks of object and social recognition.
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