Putting Together Pieces of the Lateral Septum: Multifaceted Functions and Its Neural Pathways

Abstract

The lateral septum (LS) is implicated as a hub that regulates a variety of affects, such as reward, feeding, anxiety, fear, sociability, and memory. However, it remains unclear how the LS, previously treated as a structure of homogeneity, exhibits such multifaceted functions. Emerging evidence suggests that different functions of the LS are mediated largely by its diverse input and output connections. It has also become clear that the LS is a heterogeneous region, where its dorsal and ventral poles play dissociable and often opposing roles. This functional heterogeneity can often be explained by distinct dorsal and ventral hippocampal inputs along the LS dorsoventral axis, as well as antagonizing connections between LS subregions. Similarly, outputs from LS subregions to respective downstream targets, such as hypothalamic, preoptic, and tegmental areas, also account for this functional heterogeneity. In this review, we provide an updated perspective on LS subregion classification, connectivity, and functions. We also identify key questions that have yet to be addressed in the field.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 91

1. 1.

   Anthony TE, Dee N, Bernard A, Lerchner W, Heintz N, Anderson DJ (2014 ) Control of stress-induced persistent anxiety by an extra-amygdala septohypothalamic circuit. Cell 156:522–536.

   Not in our library10.1016/j.cell.2013.12.040

2. 2.

   Azevedo EP, Pomeranz L, Cheng J, Schneeberger M, Vaughan R, Stern SA, Tan B, Doerig K, Greengard P, Friedman JM (2019 ) A role of Drd2 hippocampal neurons in context-dependent food intake. Neuron 102:873–886.e5.

   Not in our library10.1016/j.neuron.2019.03.011

3. 3.

   Azevedo EP, Tan B, Pomeranz LE, Ivan V, Fetcho R, Schneeberger M, Doerig KR, Liston C, Friedman JM, Stern SA (2020 ) A limbic circuit selectively links active escape to food suppression. Elife 9:e58894.

   Not in our library10.7554/elife.58894

4. 4.
   Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway · 2015

   No notice
5. 5.

   Besnard A, Gao Y, TaeWoo Kim M, Twarkowski H, Reed AK, Langberg T, Feng W, Xu X, Saur D, Zweifel LS, Davison I, Sahay A (2019 ) Dorsolateral septum somatostatin interneurons gate mobility to calibrate context-specific behavioral fear responses. Nat Neurosci 22:436–446.

   Not in our library10.1038/s41593-018-0330-y

6. 6.

   Besnard A, Miller SM, Sahay A (2020 ) Distinct dorsal and ventral hippocampal CA3 outputs govern contextual fear discrimination. Cell Rep 30:2360–2373.5.

   Not in our library10.1016/j.celrep.2020.01.055

7. 7.

   Brady JV, Nauta WJ (1953 ) Subcortical mechanisms in emotional behavior: affective changes following septal forebrain lesions in the albino rat. J Comp Physiol Psychol 46:339–346.

   Not in our library10.1037/h0059531

8. 8.
   Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context · 2014

   No notice
9. 9.

   Buzsáki G (2015 ) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–1188.

   Not in our library10.1002/hipo.22488

10. 10.

    Calandreau L, Jaffard R, Desmedt A (2007 ) Dissociated roles for the lateral and medial septum in elemental and contextual fear conditioning. Learn Mem 14:422–429.

    Not in our library10.1101/lm.531407

11. 11.

    Calandreau L, Desgranges B, Jaffard R, Desmedt A (2010 ) Switching from contextual to tone fear conditioning and vice versa: the key role of the glutamatergic hippocampal-lateral septal neurotransmission. Learn Mem 17:440–443.

    Not in our library10.1101/lm.1859810

12. 12.

    Calderwood MT, Tseng A, Glenn Stanley B (2020 ) Lateral septum mu opioid receptors in stimulation of feeding. Brain Res 1734:146648.

    Not in our library10.1016/j.brainres.2020.146648

13. 13.

    Carus-Cadavieco M, Gorbati M, Ye L, Bender F, van der Veldt S, Kosse C, Börgers C, Lee SY, Ramakrishnan C, Hu Y, Denisova N, Ramm F, Volitaki E, Burdakov D, Deisseroth K, Ponomarenko A, Korotkova T (2017 ) Gamma oscillations organize top-down signalling to hypothalamus and enable food seeking. Nature 542:232–236.

    Not in our library10.1038/nature21066

14. 14.

    Chen YH, Wu JL, Hu NY, Zhuang JP, Li WP, Zhang SR, Li XW, Yang JM, Gao TM (2021 ) Distinct projections from the infralimbic cortex exert opposing effects in modulating anxiety and fear. J Clin Invest 131:e145692.

    Not in our library10.1172/jci145692

15. 15.

    Clemens AM, Wang H, Brecht M (2020 ) The lateral septum mediates kinship behavior in the rat. Nat Commun 11:3161.

    Not in our library10.1038/s41467-020-16489-x

16. 16.

    Dantzer R, Koob GF, Bluthe RM, Le Moal M (1988 ) Septal vasopressin modulates social memory in male rats. Brain Res 457:143–147.

    Not in our library10.1016/0006-8993(88)90066-2

17. 17.

    Davis M (1992 ) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375.

    Not in our library10.1146/annurev.ne.15.030192.002033

18. 18.

    De Vries GJ, Buijs RM (1983 ) The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res 273:307–317.

    Not in our library10.1016/0006-8993(83)90855-7

19. 19.

    Desmedt A, Garcia R, Jaffard R (1999 ) Vasopressin in the lateral septum promotes elemental conditioning to the detriment of contextual fear conditioning in mice. Eur J Neurosci 11:3913–3921.

    Not in our library10.1046/j.1460-9568.1999.00815.x

20. 20.

    Donaldson ZR, Young LJ (2008 ) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900–904.

    Not in our library10.1126/science.1158668

21. 21.

    Everts HG, Koolhaas JM (1997 ) Lateral septal vasopressin in rats: role in social and object recognition? Brain Res 760:1–7.

    Not in our library10.1016/s0006-8993(97)00269-2

22. 22.

    Fanselow MS, Dong HW (2010 ) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19.

    Not in our library10.1016/j.neuron.2009.11.031

23. 23.

    Franklin TR, Druhan JP (2000 ) Expression of Fos-related antigens in the nucleus accumbens and associated regions following exposure to a cocaine-paired environment. Eur J Neurosci 12:2097–2106.

    Not in our library10.1046/j.1460-9568.2000.00071.x

24. 24.

    Fu O, Iwai Y, Narukawa M, Ishikawa AW, Ishii KK, Murata K, Yoshimura Y, Touhara K, Misaka T, Minokoshi Y, Nakajima KI (2019 ) Hypothalamic neuronal circuits regulating hunger-induced taste modification. Nat Commun 10:4560.

    Not in our library10.1038/s41467-019-12478-x

25. 25.

    Harasta AE, Power JM, von Jonquieres G, Karl T, Drucker DJ, Housley GD, Schneider M, Klugmann M (2015 ) Septal glucagon-like peptide 1 receptor expression determines suppression of cocaine-induced behavior. Neuropsychopharmacology 40:1969–1978.

    Not in our library10.1038/npp.2015.47

26. 26.

    Hitti FL, Siegelbaum SA (2014 ) The hippocampal CA2 region is essential for social memory. Nature 508:88–92.

    Not in our library10.1038/nature13028

27. 27.

    Hunsaker MR, Tran GT, Kesner RP (2009 ) A behavioral analysis of the role of CA3 and CA1 subcortical efferents during classical fear conditioning. Behav Neurosci 123:624–630.

    Not in our library10.1037/a0015455

28. 28.

    Janzsó G, Valcz G, Thuma A, Szoke B, Lendvai Z, Abrahám H, Kozicz T, Halasy K (2010 ) Cocaine- and amphetamine-regulated transcript (CART) peptide-immunopositive neuronal elements in the lateral septum: rostrocaudal distribution in the male rat. Brain Res 1362:40–47.

    Not in our library10.1016/j.brainres.2010.09.079

29. 29.

    Jiang JX, Liu H, Huang ZZ, Cui Y, Zhang XQ, Zhang XL, Cui Y, Xin WJ (2018 ) The role of CA3-LS-VTA loop in the formation of conditioned place preference induced by context-associated reward memory for morphine. Addict Biol 23:41–54.

    Not in our library10.1111/adb.12468

30. 30.

    Jonsson S, Morud J, Stomberg R, Ericson M, Söderpalm B (2017 ) Involvement of lateral septum in alcohol’s dopamine-elevating effect in the rat. Addict Biol 22:93–102.

    Not in our library10.1111/adb.12297

31. 31.

    Kask A, Nguyen HP, Pabst R, Von Hörsten S (2001 ) Neuropeptide Y Y1 receptor-mediated anxiolysis in the dorsocaudal lateral septum: functional antagonism of corticotropin-releasing hormone-induced anxiety. Neuroscience 104:799–806.

    Not in our library10.1016/s0306-4522(01)00116-6

32. 32.

    Kelly AM, Ong JY, Witmer RA, Ophir AG (2020 ) Paternal deprivation impairs social behavior putatively via epigenetic modification to lateral septum vasopressin receptor. Sci Adv 6:eabb9116.

    Not in our library10.1126/sciadv.abb9116

33. 33.

    Kosugi K, Yoshida K, Suzuki T, Kobayashi K, Yoshida K, Mimura M, Tanaka KF (2021 ) Activation of ventral CA1 hippocampal neurons projecting to the lateral septum during feeding. Hippocampus 31:294–304.

    Not in our library10.1002/hipo.23289

34. 34.

    Lee EH (1995 ) Corticotropin-releasing factor injected into the lateral septum improves memory function in rats. Chin J Physiol 38:125–129.

    Not in our library

35. 35.

    Leroy F, Park J, Asok A, Brann DH, Meira T, Boyle LM, Buss EW, Kandel ER, Siegelbaum SA (2018 ) A circuit from hippocampal CA2 to lateral septum disinhibits social aggression. Nature 564:213–218.

    Not in our library10.1038/s41586-018-0772-0

36. 36.

    Leutgeb S, Mizumori SJ (2002 ) Context-specific spatial representations by lateral septal cells. Neuroscience 112:655–663.

    Not in our library10.1016/s0306-4522(02)00101-x

37. 37.

    Li YL, Wei S, Liu Q, Gong Q, Zhang QJ, Zheng TG, Yong Z, Chen F, Lawrence AJ, Liang JH (2021 ) Mu-opioid receptors in septum mediate the development of behavioural sensitization to a single morphine exposure in male rats. Addict Biol e13066.

    Not in our library10.1111/adb.13066

38. 38.

    Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ (2011 ) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221–226.

    Not in our library10.1038/nature09736

39. 39.

    Liu Y, Curtis JT, Wang Z (2001 ) Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav Neurosci 115:910–919.

    Not in our library10.1037/0735-7044.115.4.910

40. 40.

    Lukas M, Toth I, Veenema AH, Neumann ID (2013 ) Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 38:916–926.

    Not in our library10.1016/j.psyneuen.2012.09.018

41. 41.

    Luo AH, Tahsili-Fahadan P, Wise RA, Lupica CR, Aston-Jones G (2011 ) Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333:353–357.

    Not in our library10.1126/science.1204622

42. 42.

    McGlinchey EM, Aston-Jones G (2018 ) Dorsal hippocampus drives context-induced cocaine seeking via inputs to lateral septum. Neuropsychopharmacology 43:987–1000.

    Not in our library10.1038/npp.2017.144

43. 43.

    Mu MD, Geng HY, Rong KL, Peng RC, Wang ST, Geng LT, Qian ZM, Yung WH, Ke Y (2020 ) A limbic circuitry involved in emotional stress-induced grooming. Nat Commun 11:2261.

    Not in our library10.1038/s41467-020-16203-x

44. 44.

    O’Keefe J, Nadel L (1978 ) The hippocampus as a cognitive map. Oxford; New York: Clarendon Press; Oxford University Press.

    Not in our library

45. 45.

    Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, et al. (2014 ) A mesoscale connectome of the mouse brain. Nature 508:207–214.

    Not in our library10.1038/nature13186

46. 46.

    Okuyama T, Kitamura T, Roy DS, Itohara S, Tonegawa S (2016 ) Ventral CA1 neurons store social memory. Science 353:1536–1541.

    Not in our library10.1126/science.aaf7003

47. 47.

    Olds J, Milner P (1954 ) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 47:419–427.

    Not in our library10.1037/h0058775

48. 48.

    Oliveira VEM, Lukas M, Wolf HN, Durante E, Lorenz A, Mayer AL, Bludau A, Bosch OJ, Grinevich V, Egger V, de Jong TR, Neumann ID (2021 ) Oxytocin and vasopressin within the ventral and dorsal lateral septum modulate aggression in female rats. Nat Commun 12:2900.

    Not in our library10.1038/s41467-021-23064-5

49. 49.

    Opalka AN, Wang DV (2020 ) Hippocampal efferents to retrosplenial cortex and lateral septum are required for memory acquisition. Learn Mem 27:310–318.

    Not in our library10.1101/lm.051797.120

50. 50.

    Pantazis CB, Aston-Jones G (2020 ) Lateral septum inhibition reduces motivation for cocaine: reversal by diazepam. Addict Biol 25:e12742.

    Not in our library10.1111/adb.12742

51. 51.

    Parfitt GM, Nguyen R, Bang JY, Aqrabawi AJ, Tran MM, Seo DK, Richards BA, Kim JC (2017 ) Bidirectional control of anxiety-related behaviors in mice: role of inputs arising from the ventral hippocampus to the lateral septum and medial prefrontal cortex. Neuropsychopharmacol 42:1715–1728.

    Not in our library10.1038/npp.2017.56

52. 52.

    Popik P, Vos PE, Van Ree JM (1992 ) Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat. Behav Pharmacol 3:351–358.

    Not in our library

53. 53.

    Prado-Alcala R, Streather A, Wise RA (1984 ) Brain stimulation reward and dopamine terminal fields. II. Septal and cortical projections. Brain Res 301:209–219.

    Not in our library10.1016/0006-8993(84)91089-8

54. 54.

    Risold PY, Swanson LW (1997a ) Chemoarchitecture of the rat lateral septal nucleus. Brain Res Brain Res Rev 24:91–113.

    Not in our library10.1016/s0165-0173(97)00008-8

55. 55.

    Risold PY, Swanson LW (1997b ) Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:115–195.

    Not in our library10.1016/s0165-0173(97)00009-x

56. 56.

    Rosen JB, Schulkin J (1998 ) From normal fear to pathological anxiety. Psychol Rev 105:325–350.

    Not in our library10.1037/0033-295x.105.2.325

57. 57.

    Roth BL (2016 ) DREADDs for neuroscientists. Neuron 89:683–694.

    Not in our library10.1016/j.neuron.2016.01.040

58. 58.

    Roy DS, Kitamura T, Okuyama T, Ogawa SK, Sun C, Obata Y, Yoshiki A, Tonegawa S (2017 ) Distinct neural circuits for the formation and retrieval of episodic memories. Cell 170:1000–1012.e19.

    Not in our library10.1016/j.cell.2017.07.013

59. 59.

    Sartor GC, Aston-Jones GS (2012 ) A septal-hypothalamic pathway drives orexin neurons, which is necessary for conditioned cocaine preference. J Neurosci 32:4623–4631.

    Not in our library10.1523/jneurosci.4561-11.2012

60. 60.

    Sheehan TP, Chambers RA, Russell DS (2004 ) Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Brain Res Rev 46:71–117.

    Not in our library10.1016/j.brainresrev.2004.04.009

61. 61.

    Shohamy D, Turk-Browne NB (2013 ) Mechanisms for widespread hippocampal involvement in cognition. J Exp Psychol Gen 142:1159–1170.

    Not in our library10.1037/a0034461

62. 62.

    Singewald GM, Rjabokon A, Singewald N, Ebner K (2011 ) The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacology 36:793–804.

    Not in our library10.1038/npp.2010.213

63. 63.

    Sinha R (2001 ) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343–359.

    Not in our library10.1007/s002130100917

64. 64.

    Steinert RE, Feinle-Bisset C, Asarian L, Horowitz M, Beglinger C, Geary N (2017 ) Ghrelin, CCK, GLP-1, and PYY(3-36): secretory controls and physiological roles in eating and glycemia in health, obesity, and after RYGB. Physiol Rev 97:411–463.

    Not in our library10.1152/physrev.00031.2014

65. 65.
    An excitatory ventral hippocampus to lateral septum circuit that suppresses feeding · 2015

    No notice
66. 66.

    Sweeney P, Yang Y (2016 ) An inhibitory septum to lateral hypothalamus circuit that suppresses feeding. J Neurosci 36:11185–11195.

    Not in our library10.1523/jneurosci.2042-16.2016

67. 67.

    Takamura Y, Tamura R, Zhou TL, Kobayashi T, Tran AH, Eifuku S, Ono T (2006 ) Spatial firing properties of lateral septal neurons. Hippocampus 16:635–644.

    Not in our library10.1002/hipo.20196

68. 68.

    Terrill SJ, Jackson CM, Greene HE, Lilly N, Maske CB, Vallejo S, Williams DL (2016 ) Role of lateral septum glucagon-like peptide 1 receptors in food intake. Am J Physiol Regul Integr Comp Physiol 311:R124–R132.

    Not in our library10.1152/ajpregu.00460.2015

69. 69.

    Terrill SJ, Wall KD, Medina ND, Maske CB, Williams DL (2018 ) Lateral septum growth hormone secretagogue receptor affects food intake and motivation for sucrose reinforcement. Am J Physiol Regul Integr Comp Physiol 315:R76–R83.

    Not in our library10.1152/ajpregu.00339.2017

70. 70.

    Terrill SJ, Holt MK, Maske CB, Abrams N, Reimann F, Trapp S, Williams DL (2019 ) Endogenous GLP-1 in lateral septum promotes satiety and suppresses motivation for food in mice. Physiol Behav 206:191–199.

    Not in our library10.1016/j.physbeh.2019.04.008

71. 71.

    Thomas E, Yadin E, Strickland CE (1991 ) Septal unit activity during classical conditioning: a regional comparison. Brain Res 547:303–308.

    Not in our library10.1016/0006-8993(91)90975-2

72. 72.

    Thomas E, Burock D, Knudsen K, Deterding E, Yadin E (2013 ) Single unit activity in the lateral septum and central nucleus of the amygdala in the elevated plus-maze: a model of exposure therapy? Neurosci Lett 548:269–274.

    Not in our library10.1016/j.neulet.2013.05.078

73. 73.

    Tingley D, Buzsáki G (2018 ) Transformation of a spatial map across the hippocampal-lateral septal circuit. Neuron 98:1229–1242.e5.

    Not in our library10.1016/j.neuron.2018.04.028

74. 74.

    Tingley D, Buzsáki G (2020 ) Routing of hippocampal ripples to subcortical structures via the lateral septum. Neuron 105:138–149.e5.

    Not in our library10.1016/j.neuron.2019.10.012

75. 75.

    Tingley D, McClain K, Kaya E, Carpenter J, Buzsáki G (2021 ) A metabolic function of the hippocampal sharp wave-ripple. Nature 597:82–86.

    Not in our library10.1038/s41586-021-03811-w

76. 76.

    Trent NL, Menard JL (2011 ) Infusions of neuropeptide Y into the lateral septum reduce anxiety-related behaviors in the rat. Pharmacol Biochem Behav 99:580–590.

    Not in our library10.1016/j.pbb.2011.06.009

77. 77.

    Tsanov M (2018 ) Differential and complementary roles of medial and lateral septum in the orchestration of limbic oscillations and signal integration. Eur J Neurosci 48:2783–2794.

    Not in our library10.1111/ejn.13746

78. 78.

    van der Veldt S, Etter G, Mosser CA, Manseau F, Williams S (2021 ) Conjunctive spatial and self-motion codes are topographically organized in the GABAergic cells of the lateral septum. PLoS Biol 19:e3001383.

    Not in our library10.1371/journal.pbio.3001383

79. 79.

    Vega-Quiroga I, Yarur HE, Gysling K (2018 ) Lateral septum stimulation disinhibits dopaminergic neurons in the antero-ventral region of the ventral tegmental area: role of GABA-A alpha 1 receptors. Neuropharmacology 128:76–85.

    Not in our library10.1016/j.neuropharm.2017.09.034

80. 80.
    Neurons in the amygdala with response-selectivity for anxiety in two ethologically based tests. · 2011

    Not checked
81. 81.

    Werner CT, Mitra S, Auerbach BD, Wang ZJ, Martin JA, Stewart AF, Gobira PH, Iida M, An C, Cobb MM (2020 ) Neuroadaptations in the dorsal hippocampus underlie cocaine seeking during prolonged abstinence. Proc Natl Acad Sci USA 117:26460–26469.

    Not in our library10.1073/pnas.2006133117

82. 82.

    Wirtshafter HS, Wilson MA (2019 ) Locomotor and hippocampal processing converge in the lateral septum. Curr Biol 29:3177–3192.e3.

    Not in our library10.1016/j.cub.2019.07.089

83. 83.

    Wirtshafter HS, Wilson MA (2020 ) Differences in reward biased spatial representations in the lateral septum and hippocampus. Elife 9:e55252.

    Not in our library10.7554/elife.55252

84. 84.

    Wong LC, Wang L, D’Amour JA, Yumita T, Chen G, Yamaguchi T, Chang BC, Bernstein H, You X, Feng JE, Froemke RC, Lin D (2016 ) Effective modulation of male aggression through lateral septum to medial hypothalamus projection. Curr Biol 26:593–604.

    Not in our library10.1016/j.cub.2015.12.065

85. 85.

    Xu Y, Lu Y, Cassidy RM, Mangieri LR, Zhu C, Huang X, Jiang Z, Justice NJ, Xu Y, Arenkiel BR, Tong Q (2019 ) Identification of a neurocircuit underlying regulation of feeding by stress-related emotional responses. Nat Commun 10:3446.

    Not in our library10.1038/s41467-019-11399-z

86. 86.

    Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K (2011 ) Optogenetics in neural systems. Neuron 71:9–34.

    Not in our library10.1016/j.neuron.2011.06.004

87. 87.

    Zahm DS, Becker ML, Freiman AJ, Strauch S, Degarmo B, Geisler S, Meredith GE, Marinelli M (2010 ) Fos after single and repeated self-administration of cocaine and saline in the rat: emphasis on the Basal forebrain and recalibration of expression. Neuropsychopharmacology 35:445–463.

    Not in our library10.1038/npp.2009.149

88. 88.

    Zahm DS, Parsley KP, Schwartz ZM, Cheng AY (2013 ) On lateral septum-like characteristics of outputs from the accumbal hedonic “hotspot” of Peciña and Berridge with commentary on the transitional nature of basal forebrain “boundaries.” J Comp Neurol 521:50–68.

    Not in our library10.1002/cne.23157

89. 89.
    Characterization of GABAergic neurons in the mouse lateral septum: a double fluorescence in situ hybridization and immunohistochemical study using tyramide signal amplification. · 2013

    Not checked
90. 90.

    Zhou TL, Tamura R, Kuriwaki J, Ono T (1999 ) Comparison of medial and lateral septal neuron activity during performance of spatial tasks in rats. Hippocampus 9:220–234.

    Not in our library10.1002/(sici)1098-1063(1999)9:3<220::aid-hipo3>3.0.co;2-e

91. 91.

    Zoicas I, Slattery DA, Neumann ID (2014 ) Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum. Neuropsychopharmacol 39:3027–3035.

    Not in our library10.1038/npp.2014.156

Cited by papers we hold 1

• Lateral septum-lateral hypothalamus circuit dysfunction in comorbid pain and anxiety · 2023
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.