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研究生: 莊逸琪
Jhuang, Yi-Ci
論文名稱: 大鼠連結核及嗅緣皮質於痕跡恐懼制約所扮演之不同角色
Differential Roles of Nucleus Reuniens and Perirhinal Cortex in Pavlovian Trace Fear Conditioning in Rats
指導教授: 張鈞惠
Chang, Chun-Hui
口試委員: 陳景宗
Chen, Jin-Chung
呂國棟
Lu, Kwok-Tung
賴文崧
Lai, Wen-Sung
黃佳瑜
Huang, Chia-Yu
學位類別: 碩士
Master
系所名稱: 生命科學暨醫學院 - 系統神經科學研究所
Institute of Systems Neuroscience
論文出版年: 2022
畢業學年度: 110
語文別: 英文
論文頁數: 35
中文關鍵詞: 連結核嗅緣皮質痕跡恐懼制約
外文關鍵詞: reuniens, perirhinal
相關次數: 點閱:3下載:0
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  • 連結核(nucleus reuniens, RE)與嗅緣皮質(perirhinal cortex, PRC)兩腦區和海馬迴(hippocampus, HPC)與內側前額葉皮質(medial prefrontal cortex, mPFC)之間有著直接且雙向的神經投射關係,是海馬迴與內側前額葉皮質之間重要的訊息傳遞中繼站。先前研究指出痕跡恐懼制約(trace fear conditioning)的學習需要海馬迴與內側前額葉皮質的參與,而連結核與嗅緣皮質也皆參與其中,然而我們對於此二腦區各自所扮演的角色還不甚瞭解,因此在本研究中,我們利用藥理學方法來比較在痕跡恐懼制約學習中,大鼠的連結核與嗅緣皮質之間的功能差異。
    研究結果顯示,在痕跡恐懼制約的習得階段單獨抑制連結核或嗅緣皮質會部分影響記憶習得,而同時抑制兩腦區時,動物則完全無法習得恐懼記憶。接著我們測試在抑制連結核的狀態下增強嗅緣皮質的膽鹼性神經活性(cholinergic activity),是否能夠挽救抑制連結核所造成的恐懼記憶習得瑕疵;反之,在抑制嗅緣皮質的狀態下,增強連結核的膽鹼性神經活性,是否能夠挽救抑制嗅緣皮質所造成的恐懼記憶習得瑕疵。實驗結果與我們的假設有所不同,無論連結核在恐懼記憶的習得階段是否被抑制,增強嗅緣皮質的膽鹼性神經活性皆會造成動物在習得階段的恐懼行為表現異常,並且完全無法習得恐懼記憶;而當增強連結核的膽鹼性神經活性時,動物在記憶提取階段的恐懼反應出現整體下降的趨勢。我們的研究結果說明了連結核與嗅緣皮質在痕跡恐懼制約的習得階段皆扮演了不同的角色;而當改變嗅緣皮質中的膽鹼性神經活性時,動物的恐懼記憶習得瑕疵與改變連結核的膽鹼性神經活性相比較為嚴重,顯示出膽鹼性神經調控在此二腦區中重要性之差異。


    The nucleus reuniens (RE) and the perirhinal cortex (PRC) are two major relay stations that interconnect the hippocampus (HPC) and the medial prefrontal cortex (mPFC). Previous studies have shown that both the RE and the PRC are involved in the acquisition of trace fear conditioning. However, the respective contribution of the two regions is unclear. In this study, we used pharmacological approach to compare their roles. Our data suggested that inactivation of the RE or the PRC during conditioning partially impaired, while inactivation of both areas totally abolished, the encoding of trace fear. We next examined whether the impaired encoding of trace fear under RE inactivation can be rescued with enhanced cholinergic tone in the PRC, and vice versa. Against our hypothesis, regardless of whether the RE was on-line or not, animals failed to encode trace fear when further engaging cholinergic activities in the PRC. Conversely, depending on PRC activation level during conditioning, further recruiting cholinergic activities in the RE led to a down-shift of fear response during retrieval. Our results revealed that the RE and the PRC were necessary for the encoding of trace fear. Moreover, there was differential importance of cholinergic modulation during the process.

    中文摘要 (p.i) Abstract (p.ii) 致謝 (p.iii) Chapter 1 Introduction (p.1) 1.1 Pavlovian trace fear conditioning (p.1) 1.2 The HPC-mPFC circuitry (p.2) 1.3 The nucleus reuniens (p.2) 1.4 The perirhinal cortex (p.3) 1.5 The cholinergic modulation system (p.4) 1.6 Specific aims (p.5) Chapter 2 Materials and Methods (p.6) 2.1 Subjects (p.6) 2.2 Surgery (p.6) 2.3 Drug infusion (p.7) 2.4 Behavioral apparatus (p.7) 2.5 Experimental design (p.8) 2.6 Histology (p.9) 2.7 Statistical analysis (p.9) Chapter 3 Results (p.11) 3.1 Experiment 1: Inactivation of the RE and/or the PRC in acquisition/consolidation of trace fear conditioning (p.11) 3.2 Experiment 2: Enhanced PRC cholinergic modulation under RE inactivation in acquisition/consolidation of trace fear conditioning (p.12) 3.3 Experiment 3: Enhanced RE cholinergic modulation under PRC inactivation in acquisition/consolidation of trace fear conditioning (p.15) Chapter 4 Discussion (p.18) Chapter 5 Figures (p.24) References (p.29)

    Aggleton JP, Nelson AJD (2020) Distributed interactive brain circuits for object-in-place memory: A place for time? Brain Neurosci Adv 4:2398212820933471.
    Allen LM, Lesyshyn RA, O'Dell SJ, Allen TA, Fortin NJ (2020) The hippocampus, prefrontal cortex, and perirhinal cortex are critical to incidental order memory. Behav Brain Res 379:112215.
    Apergis-Schoute J, Pinto A, Paré D (2007) Muscarinic control of long-range GABAergic inhibition within the rhinal cortices. J Neurosci 27:4061-4071.
    Bang SJ, Brown TH (2009a) Perirhinal cortex supports acquired fear of auditory objects. Neurobiol Learn Mem 92:53-62.
    Bang SJ, Brown TH (2009b) Muscarinic receptors in perirhinal cortex control trace conditioning. J Neurosci 29:4346-4350.
    Bangasser DA, Waxler DE, Santollo J, Shors TJ (2006) Trace conditioning and the hippocampus: the importance of contiguity. J Neurosci 26:8702-8706.
    Barker GR, Bird F, Alexander V, Warburton EC (2007) Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci 27:2948-2957.
    Barker GRI, Warburton EC (2015) Object-in-place associative recognition memory depends on glutamate receptor neurotransmission within two defined hippocampal-cortical circuits: a critical role for AMPA and NMDA receptors in the hippocampus, perirhinal, and prefrontal cortices. Cereb Cortex 25:472-481.
    Barker GRI, Warburton EC (2018) A Critical Role for the Nucleus Reuniens in Long-Term, But Not Short-Term Associative Recognition Memory Formation. J Neurosci 38:3208-3217.
    Baydin S, Gungor A, Baran O, Tanriover N, Rhoton AL (2016) The double massa intermedia. Surg Neurol Int 7:30.
    Baysinger AN, Kent BA, Brown TH (2012) Muscarinic receptors in amygdala control trace fear conditioning. PLoS One 7:e45720.
    Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66:921-936.
    Cassel JC, Pereira de Vasconcelos A, Loureiro M, Cholvin T, Dalrymple-Alford JC, Vertes RP (2013) The reuniens and rhomboid nuclei: neuroanatomy, electrophysiological characteristics and behavioral implications. Prog Neurobiol 111:34-52.
    Chao OY, de Souza Silva MA, Yang YM, Huston JP (2020) The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties. Neurosci Biobehav Rev 113:373-407.
    Colgin LL (2011) Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol 21:467-474.
    Connor DA, Gould TJ (2016) The role of working memory and declarative memory in trace conditioning. Neurobiol Learn Mem 134 Pt B:193-209.
    D'Souza D, Sadananda M (2017) Estrous Cycle Phase-Dependent Changes in Anxiety- and Depression-Like Profiles in the Late Adolescent Wistar-Kyoto Rat. Ann Neurosci 24:136-145.
    Deacon TW, Eichenbaum H, Rosenberg P, Eckmann KW (1983) Afferent connections of the perirhinal cortex in the rat. J Comp Neurol 220:168-190.
    Delatour B, Witter MP (2002) Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur J Neurosci 15:1400-1407.
    Diana RA, Yonelinas AP, Ranganath C (2010) Medial temporal lobe activity during source retrieval reflects information type, not memory strength. J Cogn Neurosci 22:1808-1818.
    Dolleman-van der Weel MJ, Lopes da Silva FH, Witter MP (2017) Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat. Brain Struct Funct 222:2421-2438.
    Dolleman-van der Weel MJ, Griffin AL, Ito HT, Shapiro ML, Witter MP, Vertes RP, Allen TA (2019) The nucleus reuniens of the thalamus sits at the nexus of a hippocampus and medial prefrontal cortex circuit enabling memory and behavior. Learn Mem 26:191-205.
    Egorov AV, Unsicker K, von Bohlen und Halbach O (2006) Muscarinic control of graded persistent activity in lateral amygdala neurons. Eur J Neurosci 24:3183-3194.
    Eilam D, Izhar R, Mort J (2011) Threat detection: Behavioral practices in animals and humans. Neuroscience and biobehavioral reviews 35:999-1006.
    Eleore L, López-Ramos JC, Guerra-Narbona R, Delgado-García JM (2011) Role of reuniens nucleus projections to the medial prefrontal cortex and to the hippocampal pyramidal CA1 area in associative learning. PLoS One 6:e23538.
    Esclassan F, Coutureau E, Di Scala G, Marchand AR (2009) A cholinergic-dependent role for the entorhinal cortex in trace fear conditioning. J Neurosci 29:8087-8093.
    Faravelli C, Alessandra Scarpato M, Castellini G, Lo Sauro C (2013) Gender differences in depression and anxiety: the role of age. Psychiatry Res 210:1301-1303.
    Ferraris M, Cassel JC, Pereira de Vasconcelos A, Stephan A, Quilichini PP (2021) The nucleus reuniens, a thalamic relay for cortico-hippocampal interaction in recent and remote memory consolidation. Neurosci Biobehav Rev 125:339-354.
    Fritz CO, Morris PE, Richler JJ (2012) Effect size estimates: current use, calculations, and interpretation. J Exp Psychol Gen 141:2-18.
    Froemke RC, Merzenich MM, Schreiner CE (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450:425-429.
    Furtak SC, Wei SM, Agster KL, Burwell RD (2007) Functional neuroanatomy of the parahippocampal region in the rat: the perirhinal and postrhinal cortices. Hippocampus 17:709-722.
    Gao W, Ping S, Liu X (2020) Gender differences in depression, anxiety, and stress among college students: A longitudinal study from China. J Affect Disord 263:292-300.
    Gilmartin MR, Helmstetter FJ (2010) Trace and contextual fear conditioning require neural activity and NMDA receptor-dependent transmission in the medial prefrontal cortex. Learn Mem 17:289-296.
    Gilmartin MR, Miyawaki H, Helmstetter FJ, Diba K (2013) Prefrontal activity links nonoverlapping events in memory. J Neurosci 33:10910-10914.
    Godsil BP, Kiss JP, Spedding M, Jay TM (2013) The hippocampal–prefrontal pathway: The weak link in psychiatric disorders? Eur Neuropsychopharmacol 23:1165-1181.
    Griffin AL (2021) The nucleus reuniens orchestrates prefrontal-hippocampal synchrony during spatial working memory. Neurosci Biobehav Rev 128:415-420.
    Guillén-Ruiz G, Cueto-Escobedo J, Hernández-López F, Rivera-Aburto LE, Herrera-Huerta EV, Rodríguez-Landa JF (2021) Estrous cycle modulates the anxiogenic effects of caffeine in the elevated plus maze and light/dark box in female rats. Behav Brain Res 413:113469.
    Haritha AT, Wood KH, Ver Hoef LW, Knight DC (2013) Human trace fear conditioning: right-lateralized cortical activity supports trace-interval processes. Cogn Affect Behav Neurosci 13:225-237.
    Hoover WB, Vertes RP (2012) Collateral projections from nucleus reuniens of thalamus to hippocampus and medial prefrontal cortex in the rat: a single and double retrograde fluorescent labeling study. Brain Struct Funct 217:191-209.
    Howe WM, Gritton HJ, Lusk NA, Roberts EA, Hetrick VL, Berke JD, Sarter M (2017) Acetylcholine Release in Prefrontal Cortex Promotes Gamma Oscillations and Theta-Gamma Coupling during Cue Detection. J Neurosci 37:3215-3230.
    Hyman JM, Zilli EA, Paley AM, Hasselmo ME (2010) Working Memory Performance Correlates with Prefrontal-Hippocampal Theta Interactions but not with Prefrontal Neuron Firing Rates. Front Integr Neurosci 4:2.
    Ito HT, Zhang S-J, Witter MP, Moser EI, Moser M-B (2015) A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation. Nature 522:50-55.
    Jayachandran M, Linley SB, Schlecht M, Mahler SV, Vertes RP, Allen TA (2019) Prefrontal Pathways Provide Top-Down Control of Memory for Sequences of Events. Cell Reports 28:640-654.e646.
    Jin J, Maren S (2015) Prefrontal-Hippocampal Interactions in Memory and Emotion. Frontiers in systems neuroscience 9:170.
    Kafetzopoulos V, Kokras N, Sotiropoulos I, Oliveira JF, Leite-Almeida H, Vasalou A, Sardinha VM, Papadopoulou-Daifoti Z, Almeida OFX, Antoniou K, Sousa N, Dalla C (2018) The nucleus reuniens: a key node in the neurocircuitry of stress and depression. Mol Psychiatry 23:579-586.
    Kawai H, Lazar R, Metherate R (2007) Nicotinic control of axon excitability regulates thalamocortical transmission. Nat Neurosci 10:1168-1175.
    Kennedy PJ, Shapiro ML (2004) Retrieving memories via internal context requires the hippocampus. J Neurosci 24:6979-6985.
    Kent BA, Brown TH (2012) Dual functions of perirhinal cortex in fear conditioning. Hippocampus 22:2068-2079.
    Kholodar-Smith DB, Boguszewski P, Brown TH (2008) Auditory trace fear conditioning requires perirhinal cortex. Neurobiol Learn Mem 90:537-543.
    Knauer B, Jochems A, Valero-Aracama MJ, Yoshida M (2013) Long-lasting intrinsic persistent firing in rat CA1 pyramidal cells: a possible mechanism for active maintenance of memory. Hippocampus 23:820-831.
    Knight DC, Cheng DT, Smith CN, Stein EA, Helmstetter FJ (2004) Neural substrates mediating human delay and trace fear conditioning. J Neurosci 24:218-228.
    Lakens D (2013) Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol 4:863.
    Laroche S, Davis S, Jay TM (2000) Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus 10:438-446.
    LeDoux JE (1996) The emotional brain: The mysterious underpinnings of emotional life. New York, NY, US: Simon & Schuster.
    LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
    Levin ED (2013) Complex relationships of nicotinic receptor actions and cognitive functions. Biochem Pharmacol 86:1145-1152.
    Likhtik E, Johansen JP (2019) Neuromodulation in circuits of aversive emotional learning. Nat Neurosci 22:1586-1597.
    Lin YJ, Chiou RJ, Chang CH (2020) The Reuniens and Rhomboid Nuclei Are Required for Acquisition of Pavlovian Trace Fear Conditioning in Rats. eNeuro 7:ENEURO.0106-0120.2020.
    Liu W, Ge T, Leng Y, Pan Z, Fan J, Yang W, Cui R (2017) The Role of Neural Plasticity in Depression: From Hippocampus to Prefrontal Cortex. Neural Plast 2017:6871089.
    Marder E (2011) Variability, compensation, and modulation in neurons and circuits. Proc Natl Acad Sci U S A 108:15542-15548.
    Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417-428.
    Martina M, Royer S, Paré D (2001) Propagation of neocortical inputs in the perirhinal cortex. J Neurosci 21:2878-2888.
    Massey PV, Bhabra G, Cho K, Brown MW, Bashir ZI (2001) Activation of muscarinic receptors induces protein synthesis-dependent long-lasting depression in the perirhinal cortex. Eur J Neurosci 14:145-152.
    McEchron MD, Bouwmeester H, Tseng W, Weiss C, Disterhoft JF (1998) Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8:638-646.
    McGaughy J, Koene RA, Eichenbaum H, Hasselmo ME (2005) Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. J Neurosci 25:10273-10281.
    McHenry J, Carrier N, Hull E, Kabbaj M (2014) Sex differences in anxiety and depression: role of testosterone. Front Neuroendocrinol 35:42-57.
    McKenna JT, Vertes RP (2004) Afferent projections to nucleus reuniens of the thalamus. J Comp Neurol 480:115-142.
    Melichercik AM, Elliott KS, Bianchi C, Ernst SM, Winters BD (2012) Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats. Neuropharmacology 62:2096-2105.
    Miller CK, Halbing AA, Patisaul HB, Meitzen J (2021) Interactions of the estrous cycle, novelty, and light on female and male rat open field locomotor and anxiety-related behaviors. Physiol Behav 228:113203.
    Miyashita Y (2019) Perirhinal circuits for memory processing. Nat Rev Neurosci 20:577-592.
    Mizusaki BEP, O'Donnell C (2021) Neural circuit function redundancy in brain disorders. Curr Opin Neurobiol 70:74-80.
    Navaroli VL, Zhao Y, Boguszewski P, Brown TH (2012) Muscarinic receptor activation enables persistent firing in pyramidal neurons from superficial layers of dorsal perirhinal cortex. Hippocampus 22:1392-1404.
    Ochoa EL, Chattopadhyay A, McNamee MG (1989) Desensitization of the nicotinic acetylcholine receptor: molecular mechanisms and effect of modulators. Cell Mol Neurobiol 9:141-178.
    Ottersen OP, Storm-Mathisen J (1984) GABA-containing neurons in the thalamus and pretectum of the rodent. An immunocytochemical study. Anat Embryol (Berl) 170:197-207.
    Palanza P, Parmigiani S (2017) How does sex matter? Behavior, stress and animal models of neurobehavioral disorders. Neurosci Biobehav Rev 76:134-143.
    Parikh V, Bangasser DA (2020) Cholinergic Signaling Dynamics and Cognitive Control of Attention. Curr Top Behav Neurosci 45:71-87.
    Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex: Oxford Univ. Press.
    Picciotto MR, Higley MJ, Mineur YS (2012) Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 76:116-129.
    Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369-391.
    Prado VF, Janickova H, Al-Onaizi MA, Prado MA (2017) Cholinergic circuits in cognitive flexibility. Neuroscience 345:130-141.
    Preston AR, Eichenbaum H (2013) Interplay of hippocampus and prefrontal cortex in memory. Curr Biol 23:R764-R773.
    Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56-72.
    Rahman F, Nanu R, Schneider NA, Katz D, Lisman J, Pi HJ (2021) Optogenetic perturbation of projections from thalamic nucleus reuniens to hippocampus disrupts spatial working memory retrieval more than encoding. Neurobiol Learn Mem 179:107396.
    Raybuck JD, Lattal KM (2014) Bridging the interval: theory and neurobiology of trace conditioning. Behav Processes 101:103-111.
    Reitstetter R, Lukas RJ, Gruener R (1999) Dependence of nicotinic acetylcholine receptor recovery from desensitization on the duration of agonist exposure. J Pharmacol Exp Ther 289:656-660.
    Richardson JTE (2011) Eta squared and partial eta squared as measures of effect size in educational research. Educ Res Rev 6:135-147.
    Rigoli F, Pezzulo G, Dolan RJ (2016) Prospective and Pavlovian mechanisms in aversive behaviour. Cognition 146:415-425.
    Shumake J, Monfils MH (2015) Assessing Fear Following Retrieval + Extinction Through Suppression of Baseline Reward Seeking vs. Freezing. Front Behav Neurosci 9:355.
    Simons JS, Spiers HJ (2003) Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci 4:637-648.
    Stiver ML, Jacklin DL, Mitchnick KA, Vicic N, Carlin J, O'Hara M, Winters BD (2015) Cholinergic manipulations bidirectionally regulate object memory destabilization. Learn Mem 22:203-214.
    Tuscher JJ, Taxier LR, Fortress AM, Frick KM (2018) Chemogenetic inactivation of the dorsal hippocampus and medial prefrontal cortex, individually and concurrently, impairs object recognition and spatial memory consolidation in female mice. Neurobiol Learn Mem 156:103-116.
    van den Bos R, Jolles J, van der Knaap L, Baars A, de Visser L (2012) Male and female Wistar rats differ in decision-making performance in a rodent version of the Iowa Gambling Task. Behav Brain Res 234:375-379.
    Varela C, Kumar S, Yang JY, Wilson MA (2014) Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens. Brain Struct Funct 219:911-929.
    Vertes RP (2002) Analysis of projections from the medial prefrontal cortex to the thalamus in the rat, with emphasis on nucleus reuniens. J Comp Neurol 442:163-187.
    Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
    Vertes RP, Hoover WB, Szigeti-Buck K, Leranth C (2007) Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res Bull 71:601-609.
    Vertes RP, Hoover WB, Do Valle AC, Sherman A, Rodriguez JJ (2006) Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J Comp Neurol 499:768-796.
    Viena TD, Linley SB, Vertes RP (2018) Inactivation of nucleus reuniens impairs spatial working memory and behavioral flexibility in the rat. Hippocampus 28:297-311.
    Wamsley JK, Zarbin MA, Kuhar MJ (1984) Distribution of muscarinic cholinergic high and low affinity agonist binding sites: a light microscopic autoradiographic study. Brain Res Bull 12:233-243.
    Warburton EC, Brown MW (2010) Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 48:2262-2272.
    Wu YT, Chang CH (2022) Functional Reuniens and Rhomboid Nuclei are Required for Proper Acquisition and Expression of Cued and Contextual Fear in Trace Fear Conditioning. Int J Neuropsychopharmacol 25:319-327.
    Yoon T, Okada J, Jung MW, Kim JJ (2008) Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learning & memory (Cold Spring Harbor, NY) 15:97-105.
    Yoshida M, Hasselmo ME (2009) Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29:4945-4952.

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