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Annual Review of Psychology

Volume 66, 2015

Adult Neurogenesis: Beyond Learning and Memory*

Abstract

New neurons continue to be generated in the dentate gyrus throughout life, providing this region of the hippocampus with exceptional structural plasticity, but the function of this ongoing neurogenesis is unknown. Inhibition of adult neurogenesis produces some behavioral impairments that suggest a role for new neurons in learning and memory; however, other behavioral changes appear inconsistent with this function. A review of studies investigating the function of the hippocampus going back several decades reveals many ideas that seem to converge on a critical role for the hippocampus in stress response and emotion. These potential hippocampal functions provide new avenues for investigating the behavioral functions of adult neurogenesis. And, conversely, studies in animals lacking adult neurogenesis, which are likely to have more limited and more specific impairments than are seen with lesions, may provide valuable new insights into the function of the hippocampus. A complete understanding of the function of the hippocampus must explain its role in emotion and the relationship between its emotional and memory functions.

Keyword(s): behavior, emotion, granule cells, hippocampus, stress
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2015-01-03
2024-04-16
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Literature Cited

  1. Abela AR, Chudasama Y. 2013. Dissociable contributions of the ventral hippocampus and orbitofrontal cortex to decision-making with a delayed or uncertain outcome. Eur. J. Neurosci. 37:4640–47 [Google Scholar]
  2. Acsády L, Kamondi A, Sík A, Freund T, Buzsáki G. 1998. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18:93386–403 [Google Scholar]
  3. Addis DR, Schacter DL. 2011. The hippocampus and imagining the future: Where do we stand?. Front. Hum. Neurosci. 5:173 [Google Scholar]
  4. Agis-Balboa RC, Fischer A. 2014. Generating new neurons to circumvent your fears: the role of IGF signaling. Cell. Mol. Life Sci. 71:121–42 [Google Scholar]
  5. Aimone JB, Deng W, Gage FH. 2010. Adult neurogenesis: integrating theories and separating functions. Trends Cogn. Sci. 14:7325–37 [Google Scholar]
  6. Aimone JB, Gage FH. 2011. Modeling new neuron function: a history of using computational neuroscience to study adult neurogenesis. Eur. J. Neurosci. 33:61160–69 [Google Scholar]
  7. Aimone JB, Wiles J, Gage FH. 2009. Computational influence of adult neurogenesis on memory encoding. Neuron 61:2187–202 [Google Scholar]
  8. Airan RD, Meltzer LA, Roy M, Gong Y, Chen H, Deisseroth K. 2007. High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 317:5839819–23 [Google Scholar]
  9. Altman J, Brunner RL, Bayer SA. 1973. The hippocampus and behavioral maturation. Behav. Biol. 8:5557–96 [Google Scholar]
  10. Amsel A. 1958. The role of frustrative nonreward in noncontinuous reward situations. Psychol. Bull. 55:2102–19 [Google Scholar]
  11. Amsel A. 1990. Arousal, suppression, and persistence: frustration theory, attention, and its disorders. Cogn. Emot. 4:3239–68 [Google Scholar]
  12. Amsel A. 1992. Frustration Theory: An Analysis of Dispositional Learning and Memory London: Cambridge Univ. Press
  13. Amsel A. 1993. Hippocampal function in the rat: cognitive mapping or vicarious trial and error?. Hippocampus 3:3251–56 [Google Scholar]
  14. Arruda-Carvalho M, Sakaguchi M, Akers KG, Josselyn SA, Frankland PW. 2011. Posttraining ablation of adult-generated neurons degrades previously acquired memories. J. Neurosci. 31:4215113–27 [Google Scholar]
  15. Bakker A, Kirwan CB, Miller M, Stark CEL. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:58701640–42 [Google Scholar]
  16. Bannerman DM, Deacon RMJ, Offen S, Friswell J, Grubb M, Rawlins JNP. 2002. Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav. Neurosci. 116:5884–901 [Google Scholar]
  17. Bannerman DM, Good MA, Butcher SP, Ramsay M, Morris RG. 1995. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378:6553182–86 [Google Scholar]
  18. Bannerman DM, Grubb M, Deacon RMJ, Yee BK, Feldon J, Rawlins JNP. 2003. Ventral hippocampal lesions affect anxiety but not spatial learning. Behav. Brain Res. 139:1–2197–213 [Google Scholar]
  19. Bannerman DM, Rawlins JNP, McHugh SB, Deacon RMJ, Yee BK. et al. 2004. Regional dissociations within the hippocampus—memory and anxiety. Neurosci. Biobehav. Rev. 28:3273–83 [Google Scholar]
  20. Bannerman DM, Sprengel R, Sanderson DJ, McHugh SB, Rawlins JNP. et al. 2014. Hippocampal synaptic plasticity, spatial memory and anxiety. Nat. Rev. Neurosci. 15:1–13 [Google Scholar]
  21. Barkus C, McHugh SB, Sprengel R, Seeburg PH, Rawlins JNP, Bannerman DM. 2010. Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion. Eur. J. Pharmacol. 626:149–56 [Google Scholar]
  22. Becker S, Macqueen G, Wojtowicz JM. 2009. Computational modeling and empirical studies of hippocampal neurogenesis-dependent memory: effects of interference, stress and depression. Brain Res. 1299:45–54 [Google Scholar]
  23. Ben Abdallah NM-B, Filipkowski RK, Pruschy M, Jaholkowski P, Winkler J. et al. 2013. Impaired long-term memory retention: common denominator for acutely or genetically reduced hippocampal neurogenesis in adult mice. Behav. Brain Res. 252:275–86 [Google Scholar]
  24. Bett D, Allison E, Murdoch LH, Kaefer K, Wood ER, Dudchenko PA. 2012. The neural substrates of deliberative decision making: contrasting effects of hippocampus lesions on performance and vicarious trial-and-error behavior in a spatial memory task and a visual discrimination task. Front. Behav. Neurosci. 6:70 [Google Scholar]
  25. Beylin AV, Gandhi CC, Wood GE, Talk AC, Matzel LD, Shors TJ. 2001. The role of the hippocampus in trace conditioning: temporal discontinuity or task difficulty?. Neurobiol. Learn. Mem. 76:3447–61 [Google Scholar]
  26. Blanchard DC, Griebel G, Pobbe R, Blanchard RJ. 2011. Risk assessment as an evolved threat detection and analysis process. Neurosci. Biobehav. Rev. 35:4991–98 [Google Scholar]
  27. Blanchard DC, Hori K, Rodgers RJ, Hendrie CA, Blanchard RJ. 1989. Attenuation of defensive threat and attack in wild rats (Rattus rattus) by benzodiazepines. Psychopharmacology (Berl.) 97:3392–401 [Google Scholar]
  28. Blanchard RJ, Blanchard DC. 1972. Effects of hippocampal lesions on the rat's reaction to a cat. J. Comp. Physiol. Psychol. 78:177–82 [Google Scholar]
  29. Bremner JD, Elzinga B, Schmahl C, Vermetten E. 2008. Structural and functional plasticity of the human brain in posttraumatic stress disorder. Prog. Brain Res. 167:171–86 [Google Scholar]
  30. Britton JC, Lissek S, Grillon C, Norcross MA, Pine DS. 2011. Development of anxiety: the role of threat appraisal and fear learning. Depress. Anxiety 28:15–17 [Google Scholar]
  31. Buckner RL. 2010. The role of the hippocampus in prediction and imagination. Annu. Rev. Psychol. 61:27–48 [Google Scholar]
  32. Burghardt NS, Park EH, Hen R, Fenton AA. 2012. Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 22:91795–808 [Google Scholar]
  33. Carr MF, Jadhav SP, Frank LM. 2011. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14:2147–53 [Google Scholar]
  34. Chudasama Y, Doobay VM, Liu Y. 2012. Hippocampal-prefrontal cortical circuit mediates inhibitory response control in the rat. J. Neurosci. 32:3210915–24 [Google Scholar]
  35. Chudasama Y, Izquierdo A, Murray EA. 2009. Distinct contributions of the amygdala and hippocampus to fear expression. Eur. J. Neurosci. 30:122327–37 [Google Scholar]
  36. Chudasama Y, Wright KS, Murray EA. 2008. Hippocampal lesions in rhesus monkeys disrupt emotional responses but not reinforcer devaluation effects. Biol. Psychiatry 63:111084–91 [Google Scholar]
  37. Clark DA, Beck AT. 2010. Cognitive theory and therapy of anxiety and depression: convergence with neurobiological findings. Trends Cogn. Sci. 14:9418–24 [Google Scholar]
  38. Clelland CD, Choi M, Romberg C, Clemenson GD, Fragniere A. et al. 2009. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:5937210–13 [Google Scholar]
  39. Conrad CD. 2006. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus?. Behav. Cogn. Neurosci. Rev. 5:141–60 [Google Scholar]
  40. Coover GD, Goldman L, Levine S. 1971. Plasma corticosterone levels during extinction of a lever-press response in hippocampectomized rats. Physiol. Behav. 7:5727–32 [Google Scholar]
  41. Dalgleish T. 2004. The emotional brain. Nat. Rev. Neurosci. 5:7583–89 [Google Scholar]
  42. David DJ, Samuels BA, Rainer Q, Wang J-W, Marsteller D. et al. 2009. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62:4479–93 [Google Scholar]
  43. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA. 2005. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol. 168:3415–27 [Google Scholar]
  44. de Kloet ER, Karst H, Joëls M. 2008. Corticosteroid hormones in the central stress response: quick-and-slow. Front. Neuroendocrinol. 29:2268–72 [Google Scholar]
  45. Deacon RMJ, Bannerman DM, Rawlins JNP. 2002. Anxiolytic effects of cytotoxic hippocampal lesions in rats. Behav. Neurosci. 116:3494–97 [Google Scholar]
  46. Deng W, Aimone JB, Gage FH. 2010. New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci. 11:5339–50 [Google Scholar]
  47. Denny CA, Burghardt NS, Schachter DM, Hen R, Drew MR. 2012. 4- to 6-week-old adult-born hippocampal neurons influence novelty-evoked exploration and contextual fear conditioning. Hippocampus 22:51188–201 [Google Scholar]
  48. Douglas RJ. 1967. The hippocampus and behavior. Psychol. Bull. 67:6416–22 [Google Scholar]
  49. Douglas RJ, Pribram KH. 1969. Distraction and habituation in monkeys with limbic lesions. J. Comp. Physiol. Psychol. 69:3473–80 [Google Scholar]
  50. Dragoi G, Tonegawa S. 2011. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469:7330397–401 [Google Scholar]
  51. Dragoi G, Tonegawa S. 2013. Distinct preplay of multiple novel spatial experiences in the rat. Proc. Natl. Acad. Sci. USA 110:229100–5 [Google Scholar]
  52. Drew MR, Denny CA, Hen R. 2010. Arrest of adult hippocampal neurogenesis in mice impairs single- but not multiple-trial contextual fear conditioning. Behav. Neurosci. 124:4446–54 [Google Scholar]
  53. Dzirasa K, Covington HE. 2012. Increasing the validity of experimental models for depression. Ann. N. Y. Acad. Sci. 1265:36–45 [Google Scholar]
  54. Eichenbaum H, Cohen NJ. 2014. Can we reconcile the declarative memory and spatial navigation views on hippocampal function?. Neuron 83:4764–70 [Google Scholar]
  55. Enkel T, Gholizadeh D, von Bohlen Und Halbach O, Sanchis-Segura C, Hurlemann R. et al. 2010. Ambiguous-cue interpretation is biased under stress- and depression-like states in rats. Neuropsychopharmacology 35:41008–15 [Google Scholar]
  56. Ernst A, Alkass K, Bernard S, Salehpour M, Perl S. et al. 2014. Neurogenesis in the striatum of the adult human brain. Cell 156:51072–83 [Google Scholar]
  57. Fanselow MS, Dong H-W. 2010. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 65:17–19 [Google Scholar]
  58. Feierstein CE. 2012. Linking adult olfactory neurogenesis to social behavior. Front. Neurosci. 6:173 [Google Scholar]
  59. Feierstein CE, Lazarini F, Wagner S, Gabellec M-M, de Chaumont F. et al. 2010. Disruption of adult neurogenesis in the olfactory bulb affects social interaction but not maternal behavior. Front. Behav. Neurosci. 4:176 [Google Scholar]
  60. Felix-Ortiz AC, Tye KM. 2013. BLA to vHPC inputs modulate anxiety-related behaviors. Neuron 79:4658–64 [Google Scholar]
  61. Fendler K, Karmos G, Telegdy G. 1961. The effect of hippocampal lesion on pituitary-adrenal function. Acta Physiol. Acad. Sci. Hung. 20:293–97 [Google Scholar]
  62. Ferbinteanu J, Ray C, McDonald RJ. 2003. Both dorsal and ventral hippocampus contribute to spatial learning in Long-Evans rats. Neurosci. Lett. 345:2131–35 [Google Scholar]
  63. Gaesser B, Spreng RN, McLelland VC, Addis DR, Schacter DL. 2013. Imagining the future: evidence for a hippocampal contribution to constructive processing. Hippocampus 23:121150–61 [Google Scholar]
  64. Garthe A, Behr J, Kempermann G. 2009. Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLOS ONE 4:5e5464 [Google Scholar]
  65. Garthe A, Kempermann G. 2013. An old test for new neurons: refining the Morris water maze to study the functional relevance of adult hippocampal neurogenesis. Front. Neurosci. 7:63 [Google Scholar]
  66. Gerlach JL, McEwen BS. 1972. Rat brain binds adrenal steroid hormone: radioautography of hippocampus with corticosterone. Science 175:261133–36 [Google Scholar]
  67. Gianaros PJ, Jennings JR, Sheu LK, Greer PJ, Kuller LH, Matthews KA. 2007. Prospective reports of chronic life stress predict decreased grey matter volume in the hippocampus. NeuroImage 35:2795–803 [Google Scholar]
  68. Gould E, Cameron HA. 1997. Early NMDA receptor blockade impairs defensive behavior and increases cell proliferation in the dentate gyrus of developing rats. Behav. Neurosci. 111:149–56 [Google Scholar]
  69. Gould E, Woolley CS, Cameron HA, Daniels DC, McEwen BS. 1991. Adrenal steroids regulate postnatal development of the rat dentate gyrus: II. Effects of glucocorticoids and mineralocorticoids on cell birth. J. Comp. Neurol. 313:3486–93 [Google Scholar]
  70. Gray JA, McNaughton N. 2000. The Neuropsychology of Anxiety: An Enquiry into the Function of the Septo-Hippocampal System Oxford, UK: Oxford Univ. Press, 2nd ed..
  71. Groves JO, Leslie I, Huang G-J, McHugh SB, Taylor A. et al. 2013. Ablating adult neurogenesis in the rat has no effect on spatial processing: evidence from a novel pharmacogenetic model. PLOS Genet. 9:9e1003718 [Google Scholar]
  72. Hendrickson CW, Kimble RJ, Kimble DP. 1969. Hippocampal lesions and the orienting response. J. Comp. Physiol. Psychol. 67:2220–27 [Google Scholar]
  73. Herman JP, Dolgas CM, Carlson SL. 1998. Ventral subiculum regulates hypothalamo-pituitary-adrenocortical and behavioural responses to cognitive stressors. Neuroscience 86:2449–59 [Google Scholar]
  74. Holick KA, Lee DC, Hen R, Dulawa SC. 2008. Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33:2406–17 [Google Scholar]
  75. Honey RC, Good M. 2000. Associative modulation of the orienting response: distinct effects revealed by hippocampal lesions. J. Exp. Psychol. Anim. Behav. Process. 26:13–14 [Google Scholar]
  76. Hu D, Amsel A. 1995. A simple test of the vicarious trial-and-error hypothesis of hippocampal function. Proc. Natl. Acad. Sci. USA 92:125506–9 [Google Scholar]
  77. Isaacson RL, Kimble DP. 1972. Lesions of the limbic system: their effects upon hypotheses and frustration. Behav. Biol. 7:6767–93 [Google Scholar]
  78. Jacobson L, Sapolsky R. 1991. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12:2118–34 [Google Scholar]
  79. Jankord R, Herman JP. 2008. Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. N. Y. Acad. Sci. 1148:64–73 [Google Scholar]
  80. Jarrard LE. 1968. Behavior of hippocampal lesioned rats in home cage and novel situations. Physiol. Behav. 3:65–70 [Google Scholar]
  81. Johnson A, Redish AD. 2007. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27:4512176–89 [Google Scholar]
  82. Kesner RP. 2013. An analysis of the dentate gyrus function. Behav. Brain Res. 254:1–7 [Google Scholar]
  83. Kheirbek MA, Drew LJ, Burghardt NS, Costantini DO, Tannenholz L. et al. 2013. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 77:5955–68 [Google Scholar]
  84. Kheirbek MA, Klemenhagen KC, Sahay A, Hen R. 2012a. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat. Neurosci. 15:121613–20 [Google Scholar]
  85. Kheirbek MA, Tannenholz L, Hen R. 2012b. NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J. Neurosci. 32:258696–702 [Google Scholar]
  86. Kjelstrup KG, Tuvnes FA, Steffenach H-A, Murison R, Moser EI, Moser M-B. 2002. Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. USA 99:1610825–30 [Google Scholar]
  87. Knigge KM. 1961. Adrenocortical response to stress in rats with lesions in hippocampus and amygdala. Proc. Soc. Exp. Biol. Med. 108:18–21 [Google Scholar]
  88. Koolhaas JM, Bartolomucci A, Buwalda B. Boer SF, Flügge G. , De et al. 2011. Stress revisited: a critical evaluation of the stress concept. Neurosci. Biobehav. Rev. 35:51291–301 [Google Scholar]
  89. Lagace DC, Donovan MH, DeCarolis NA, Farnbauch LA, Malhotra S. et al. 2010. Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc. Natl. Acad. Sci. USA 107:94436–41 [Google Scholar]
  90. Landgraf R, Wigger A, Holsboer F, Neumann ID. 1999. Hyper-reactive hypothalamo-pituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J. Neuroendocrinol. 11:6405–7 [Google Scholar]
  91. Lazic SE. 2010. Relating hippocampal neurogenesis to behavior: the dangers of ignoring confounding variables. Neurobiol. Aging 31:122169–71 discussion 2172–75 [Google Scholar]
  92. Lazic SE. 2012. Using causal models to distinguish between neurogenesis-dependent and -independent effects on behaviour. J. R. Soc. Interface 9:70907–17 [Google Scholar]
  93. Lever C, Burton S, O'Keefe J. 2006. Rearing on hind legs, environmental novelty, and the hippocampal formation. Rev. Neurosci. 17:1–2111–33 [Google Scholar]
  94. Levine S, Goldman L, Coover GD. 1972. Expectancy and the pituitary-adrenal system. Ciba Found. Symp. 8:281–91 [Google Scholar]
  95. Liebsch G, Linthorst AC, Neumann ID, Reul JM, Holsboer F, Landgraf R. 1998. Behavioral, physiological, and neuroendocrine stress responses and differential sensitivity to diazepam in two Wistar rat lines selectively bred for high- and low-anxiety-related behavior. Neuropsychopharmacology 19:5381–96 [Google Scholar]
  96. Long JM, Kesner RP. 1996. The effects of dorsal versus ventral hippocampal, total hippocampal, and parietal cortex lesions on memory for allocentric distance in rats. Behav. Neurosci. 110:5922–32 [Google Scholar]
  97. Luu P, Sill OC, Gao L, Becker S, Wojtowicz JM, Smith DM. 2012. The role of adult hippocampal neurogenesis in reducing interference. Behav. Neurosci. 126:3381–91 [Google Scholar]
  98. Machado CJ, Bachevalier J. 2008. Behavioral and hormonal reactivity to threat: effects of selective amygdala, hippocampal or orbital frontal lesions in monkeys. Psychoneuroendocrinology 33:7926–41 [Google Scholar]
  99. Machado CJ, Kazama AM, Bachevalier J. 2009. Impact of amygdala, orbital frontal, or hippocampal lesions on threat avoidance and emotional reactivity in nonhuman primates. Emotion 9:2147–63 [Google Scholar]
  100. Mak GK, Weiss S. 2010. Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat. Neurosci. 13:6753–58 [Google Scholar]
  101. Mandell AJ, Chapman LF, Rand RW, Walter RD. 1963. Plasma corticosteroids: changes in concentration after stimulation of hippocampus and amygdala. Science 139:35601212 [Google Scholar]
  102. Martin VC, Schacter DL, Corballis MC, Addis DR. 2011. A role for the hippocampus in encoding simulations of future events. Proc. Natl. Acad. Sci. USA 108:3313858–63 [Google Scholar]
  103. McEwen BS. 1998. Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840:33–44 [Google Scholar]
  104. McEwen BS, Weiss JM, Schwartz LS. 1968. Selective retention of corticosterone by limbic structures in rat brain. Nature 220:5170911–12 [Google Scholar]
  105. McHugh SB, Deacon RMJ, Rawlins JNP, Bannerman DM. 2004. Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav. Neurosci. 118:163–78 [Google Scholar]
  106. McNaughton N, Corr PJ. 2004. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci. Biobehav. Rev. 28:3285–305 [Google Scholar]
  107. Miller JS, Nonneman AJ, Kelly KS, Neisewander JL, Isaac WL. 1986. Disruption of neophobia, conditioned odor aversion, and conditioned taste aversion in rats with hippocampal lesions. Behav. Neural Biol. 45:2240–53 [Google Scholar]
  108. Molitor RJ, Ko PC, Hussey EP, Ally BA. 2014. Memory-related eye movements challenge behavioral measures of pattern completion and pattern separation. Hippocampus 24:6666–72 [Google Scholar]
  109. Mueller NK, Dolgas CM, Herman JP. 2004. Stressor-selective role of the ventral subiculum in regulation of neuroendocrine stress responses. Endocrinology 145:83763–68 [Google Scholar]
  110. Mullally SL, Maguire EA. 2013. Memory, imagination, and predicting the future: a common brain mechanism?. Neuroscientist 20:3220–34 [Google Scholar]
  111. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL. et al. 2012. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:1188–201 [Google Scholar]
  112. Niibori Y, Yu T-S, Epp JR, Akers KG, Josselyn SA, Frankland PW. 2012. Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region. Nat. Commun. 3:1253 [Google Scholar]
  113. Noguès X, Corsini MM, Marighetto A, Abrous DN. 2012. Functions for adult neurogenesis in memory: an introduction to the neurocomputational approach and to its contribution. Behav. Brain Res. 227:2418–25 [Google Scholar]
  114. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map New York: Oxford Univ. Press
  115. Papez JW. 1937. A proposed mechanism of emotion. Arch. Neurol. Psychiatry 38:725–43 [Google Scholar]
  116. Pentkowski NS, Blanchard DC, Lever C, Litvin Y, Blanchard RJ. 2006. Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur. J. Neurosci. 23:82185–96 [Google Scholar]
  117. Pfeiffer BE, Foster DJ. 2013. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497:744774–79 [Google Scholar]
  118. Piatti VC, An Y, Appalaraju M, Gillet S, Cameron HA. et al. 2014. Behavioral discrimination and network pattern separation can occur in the absence of neurogenesis. Program No. 465.01. 2014 Neurosci. Meet. Plan. Washington, DC: Soc. Neurosci.
  119. Pigareva ML, Preobrazhenskaya LA. 1991. Comparative psychological approach to the analysis of the functions of the hippocampus. Neurosci. Behav. Physiol. 21:3238–46 [Google Scholar]
  120. Poucet B, Herrmann T, Buhot MC. 1991. Effects of short-lasting inactivations of the ventral hippocampus and medial septum on long-term and short-term acquisition of spatial information in rats. Behav. Brain Res. 44:153–65 [Google Scholar]
  121. Pribram KH, McGuinness D. 1975. Arousal, activation, and effort in the control of attention. Psychol. Rev. 82:2116–49 [Google Scholar]
  122. Raber J, Rola R, LeFevour A, Morhardt D, Curley J. et al. 2004. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 162:139–47 [Google Scholar]
  123. Ramón y Cajal S. 1906. Nobel Lecture: The Structure and Connexions of Neurons http://www.nobelprize.org/nobel_prizes/medicine/laureates/1906/cajal-lecture.pdf
  124. Raphelson AC, Isaacson RL, Douglas RJ. 1965. The effect of distracting stimuli on the runway performance of limbic damaged rats. Psychon. Sci. 3:483–84 [Google Scholar]
  125. Rawlins JN, Feldon J, Gray JA. 1980. The effects of hippocampectomy and of fimbria section upon the partial reinforcement extinction effect in rats. Exp. Brain Res. 38:3273–83 [Google Scholar]
  126. Richmond MA, Yee BK, Pouzet B, Veenman L, Rawlins JN. et al. 1999. Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav. Neurosci. 113:61189–203 [Google Scholar]
  127. Robertson DAF, Beattie JE, Reid IC, Balfour DJK. 2005. Regulation of corticosteroid receptors in the rat brain: the role of serotonin and stress. Eur. J. Neurosci. 21:61511–20 [Google Scholar]
  128. Robins SC, Stewart I, McNay DE, Taylor V, Giachino C. et al. 2013. α-Tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat. Commun. 4:2049 [Google Scholar]
  129. Rubin RT, Mandell AJ, Crandall PH. 1966. Corticosteroid responses to limbic stimulation in man: localization of stimulus sites. Science 153:3737767–68 [Google Scholar]
  130. Rudy JW, Matus-Amat P. 2005. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus. Behav. Neurosci. 119:1154–63 [Google Scholar]
  131. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA. et al. 2011a. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:7344466–70 [Google Scholar]
  132. Sahay A, Wilson DA, Hen R. 2011b. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70:4582–88 [Google Scholar]
  133. Sanchez-Andrade G, Kendrick KM. 2009. The main olfactory system and social learning in mammals. Behav. Brain Res. 200:2323–35 [Google Scholar]
  134. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F. et al. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:5634805–9 [Google Scholar]
  135. Sapolsky RM. 2000. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch. Gen. Psychiatry 57:10925–35 [Google Scholar]
  136. Sapolsky RM, Krey LC, McEwen BS. 1984. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl. Acad. Sci. USA 81:196174–77 [Google Scholar]
  137. Saucier D, Cain DP. 1995. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature 378:6553186–89 [Google Scholar]
  138. Saxe MD, Battaglia F, Wang J-W, Malleret G, David DJ. et al. 2006. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. USA 103:4617501–6 [Google Scholar]
  139. Schmidt B, Papale A, Redish AD, Markus EJ. 2013. Conflict between place and response navigation strategies: effects on vicarious trial and error (VTE) behaviors. Learn. Mem. 20:3130–38 [Google Scholar]
  140. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:6826372–76 [Google Scholar]
  141. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E. 2002. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:5578–84 [Google Scholar]
  142. Silveira JM, Kimble DP. 1968. Brightness discrimination and reversal in hippocampally-lesioned rats. Physiol. Behav. 3:625–30 [Google Scholar]
  143. Simonov PV. 1974. On the role of the hippocampus in the integrative activity of the brain. Acta Neurobiol. Exp. 34:133–41 [Google Scholar]
  144. Simonov PV. 1991. Thwarted action and need—informational theories of emotions. Int. J. Comp. Psychol. 5:2103–7 [Google Scholar]
  145. Singer AC, Carr MF, Karlsson MP, Frank LM. 2013. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 77:61163–73 [Google Scholar]
  146. Slusher MA, Hyde JE. 1961. Effect of limbic stimulation on release of corticosteroids into the adrenal venous effluent of the cat. Endocrinology 69:1080–84 [Google Scholar]
  147. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P. et al. 2009a. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J. Neurosci. 29:4614484–95 [Google Scholar]
  148. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM. 2005. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:4843–52 [Google Scholar]
  149. Snyder JS, Radik R, Wojtowicz JM, Cameron HA. 2009b. Anatomical gradients of adult neurogenesis and activity: Young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19:4360–70 [Google Scholar]
  150. Snyder JS, Ramchand P, Rabbett S, Radik R, Wojtowicz JM, Cameron HA. 2011a. Septo-temporal gradients of neurogenesis and activity in 13-month-old rats. Neurobiol. Aging 32:61149–56 [Google Scholar]
  151. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. 2011b. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476:7361458–61 [Google Scholar]
  152. Sun M-Y, Yetman MJ, Lee T-C, Chen Y, Jankowsky JL. 2014. Specificity and efficiency of reporter expression in adult neural progenitors vary substantially among nestin-CreER(T2) lines. J. Comp. Neurol. 522:51191–208 [Google Scholar]
  153. Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q. et al. 2011. Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 16:121177–88 [Google Scholar]
  154. Takahashi LK. 1992. Developmental expression of defensive responses during exposure to conspecific adults in preweanling rats (Rattus norvegicus). J. Comp. Psychol. 106:169–77 [Google Scholar]
  155. Takahashi LK. 1995. Glucocorticoids, the hippocampus, and behavioral inhibition in the preweanling rat. J. Neurosci. 15:96023–34 [Google Scholar]
  156. Takahashi LK. 1996. Glucocorticoids and the hippocampus. Developmental interactions facilitating the expression of behavioral inhibition. Mol. Neurobiol. 13:3213–26 [Google Scholar]
  157. Tan Y-F, Rosenzweig S, Jaffray D, Wojtowicz JM. 2011. Depletion of new neurons by image guided irradiation. Front. Neurosci. 5:59 [Google Scholar]
  158. Tolman EC. 1938. The determiners of behavior at a choice point. Psychol. Rev. 45:1–41 [Google Scholar]
  159. Tsetsenis T, Ma X-H, Lo Iacono L, Beck SG, Gross C. 2007. Suppression of conditioning to ambiguous cues by pharmacogenetic inhibition of the dentate gyrus. Nat. Neurosci. 10:7896–902 [Google Scholar]
  160. Ulrich-Lai YM, Herman JP. 2009. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10:6397–409 [Google Scholar]
  161. Wang J-W, David DJ, Monckton JE, Battaglia F, Hen R. 2008. Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 28:61374–84 [Google Scholar]
  162. Weeden CSS. 2012. The role of ventral dentate gyrus in olfactory learning and memory and anxiety-like behaviors PhD Thesis, Univ. Utah. http://content.lib.utah.edu/cdm/ref/collection/etd3/id/1779
  163. Wickelgren WO, Isaacson RL. 1963. Effect of the introduction of an irrelevant stimulus on runway performance of the hippocampectomized rat. Nature 200:48–50 [Google Scholar]
  164. Winocur G, Becker S, Luu P, Rosenzweig S, Wojtowicz JM. 2012. Adult hippocampal neurogenesis and memory interference. Behav. Brain Res. 227:2464–69 [Google Scholar]
  165. Winocur G, Wojtowicz JM, Sekeres M, Snyder JS, Wang S. 2006. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16:3296–304 [Google Scholar]
  166. Wojtowicz JM. 2006. Irradiation as an experimental tool in studies of adult neurogenesis. Hippocampus 16:3261–66 [Google Scholar]
  167. Wojtowicz JM, Askew ML, Winocur G. 2008. The effects of running and of inhibiting adult neurogenesis on learning and memory in rats. Eur. J. Neurosci. 27:61494–502 [Google Scholar]
  168. Wong-Goodrich SJE, Pfau ML, Flores CT, Fraser JA, Williams CL, Jones LW. 2010. Voluntary running prevents progressive memory decline and increases adult hippocampal neurogenesis and growth factor expression after whole-brain irradiation. Cancer Res. 70:229329–38 [Google Scholar]
  169. Woodruff ML, Hatton DC, Meyer ME. 1975. Hippocampal ablation prolongs immobility response in rabbits (Oryctolagus cuniculus). J. Comp. Physiol. Psychol. 88:1329–34 [Google Scholar]
  170. Wu MV, Hen R. 2014. Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus. Hippocampus 24:7751–61 [Google Scholar]
  171. Yee LT, Warren DE, Voss JL, Duff MC, Tranel D, Cohen NJ. 2014. The hippocampus uses information just encountered to guide efficient ongoing behavior. Hippocampus 24:2154–64 [Google Scholar]
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