Advertisement

Neuronal Bases of Systemic Organization of Behavior

  • Yuri I. Alexandrov
  • Alexey A. Sozinov
  • Olga E. Svarnik
  • Alexander G. Gorkin
  • Evgeniya A. Kuzina
  • Vladimir V. Gavrilov
Chapter
Part of the Advances in Neurobiology book series (NEUROBIOL, volume 21)

Abstract

Despite the years of studies in the field of systems neuroscience, functions of neural circuits and behavior-related systems are still not entirely clear. The systems description of brain activity has recently been associated with cognitive concepts, e.g. a cognitive map, reconstructed via place-cell activity analysis and the like, and a cognitive schema, modeled in consolidation research. The issue we find of importance is that a cognitive unit reconstructed in neuroscience research is mainly formulated in terms of environment. In other words, the individual experience is considered as a model or reflection of the outside world and usually lacks a biological meaning, such as describing a given part of the world for the individual. In this chapter, we present the idea of a cognitive component that serves as a model of behavioral interaction with environment, rather than a model of the environment itself. This intangible difference entails the need in substantial revision of several well-known phenomena, including the long-term potentiation.

The principal questions developed here are how the cognitive units appear and change upon learning and performance, and how the links between them create the whole structure of individual experience. We argue that a clear distinction between processes that provide the emergence of new components and those underlying the retrieval and/or changes in the existing ones is necessary in learning and memory research. We then describe a view on learning and corresponding neuronal activity analysis that may help set this distinction.

Keywords

Memory Learning Memory consolidation Memory reconsolidation Apoptosis Neurogenesis Specialization of neurons Systemogenesis Gene expression Long-term potentiation 

Abbreviations

IEG

Immediate early gene

RSC

Retrosplenial cortex

TFS

Theory of Functional Systems

LTP

Long-term potentiation

Notes

Acknowledgements

This work was supported by Russian Science Foundation grant #14-28-00229 for Institute of Psychology, Russian Academy of Sciences.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Abdou K, Shehata M, Choko K, Nishizono H, Matsuo M, Muramatsu SI, Inokuchi K. Synapse-specific representation of the identity of overlapping memory engrams. Science. 2018;360(6394):1227–31CrossRefGoogle Scholar
  2. Adams NE, Sherfey JS, Kopell NJ, Whittington MA, Lebeau FE. Hetereogeneity in neuronal intrinsic properties: a possible mechanism for hub-like properties of the rat anterior cingulate cortex during network activity. eNeuro. 2017;4(1):ENEURO-0313.Google Scholar
  3. Aggleton JP, Brown MW, Albasser MM. Contrasting brain activity patterns for item recognition memory and associative recognition memory: insights from immediate-early gene functional imaging. Neuropsychologia. 2012;50(13):3141–55.  https://doi.org/10.1016/j.neuropsychologia.2012.05.018.CrossRefPubMedGoogle Scholar
  4. Aleksandrov YI. Learning and memory: traditional and systems approaches. Neurosci Behav Physiol. 2006;36(9):969–85.CrossRefGoogle Scholar
  5. Alexandrov YI. How we fragment the world: the view from inside versus the view from outside. Soc Sci Inf. 2008;47:419–57.CrossRefGoogle Scholar
  6. Alexandrov YI. Cognition as systemogenesis. In: Nadin M, editor. Anticipation: learning from the past. Cognitive systems monographs, vol. 25. Cham: Springer; 2015. p. 193–220.CrossRefGoogle Scholar
  7. Alexandrov YI, Alexandrov IO. Specificity of visual and motor cortex neurons activity in behavior. Acta Neurobiol Exp. 1982;42:457–68.Google Scholar
  8. Alexandrov YI, Sams M. Emotion and consciousness: ends of a continuity. Cogn Brain Res. 2005;25(2):387–405.CrossRefGoogle Scholar
  9. Alexandrov YI, Grinchenko YV, Laukka S, Jarvilehto T, Maz VN, Svetlaev IA. Acute effect of ethanol on the pattern of behavioral specialization of neurons in the limbic cortex of the freely moving rabbit. Acta Physiol Scand. 1990;140:257–68.CrossRefGoogle Scholar
  10. Alexandrov YI, Grinchenko YV, Laukka S, Jarvilehto T, Matz VN. Acute effects of alcohol on unit activity in the motor cortex of freely moving rabbits: comparison with the limbic cortex. Acta Physiol Scand. 1991;142:429–35.CrossRefGoogle Scholar
  11. Alexandrov YI, Grinchenko YV, Laukka S, Jarvilehto T, Maz VN, Korpusova AV. Effect of ethanol on hippocampal neurons depends on their behavioral specialization. Acta Physiol Scand. 1993;149:429–35.CrossRefGoogle Scholar
  12. Alexandrov YI, Grechenko TN, Gavrilov VV, et al. Formation and realization of individual experience: a psychophysiological approach. In: Miller R, Ivanitsky AM, Balaban PM, editors. Conceptual advances in brain research. Vol. 2. Conceptual advances in Russian neuroscience: complex brain functions. Amsterdam: Harwood Academic Publishers; 2000. p. 181–200.Google Scholar
  13. Alexandrov YI, Grinchenko YV, Shevchenko DG, Averkin RG, Matz VN, Laukka S, Korpusova AV. A subset of cingulate cortical neurons is specifically activated during alcohol-acquisition behavior. Acta Physiol Scand. 2001;171:87–97.PubMedGoogle Scholar
  14. Alexandrov YI, Grinchenko YV, Shevchenko DG, Averkin RG, Matz VN, Laukka S, Sams M. The effect of ethanol on the neuronal subserving of behavior in the hippocampus. J Behav Brain Sci. 2013;3:107–30.CrossRefGoogle Scholar
  15. Allsopp TE, Fazakerley JK. Altruistic cell suicide and the specialized case of the virus-infected nervous system. Trends Neurosci. 2000;23:284–90.CrossRefGoogle Scholar
  16. Ambrogini P, Orsini L, Mancini C, Ferri P, Ciaroni S, Cuppini R. Learning may reduce neurogenesis in adult rat dentate gyrus. Neurosci Lett. 2004;359:13–6.CrossRefGoogle Scholar
  17. Anacker C, Hen R. Adult hippocampal neurogenesis and cognitive flexibility—linking memory and mood. Nat Rev Neurosci. 2017;18(6):335–46.CrossRefGoogle Scholar
  18. Anokhin KV, Rose SP. Learning-induced increase of immediate early gene messenger RNA in the chick forebrain. Eur J Neurosci. 1991;3(2):162–7.CrossRefGoogle Scholar
  19. Anokhin KV, Sudakov KV. Genome of brain neurons in organization of systemic mechanisms of behavior. Bull Exp Biol Med. 2003;135(2):107–13.CrossRefGoogle Scholar
  20. Anokhin KV, Tiunova AA, Rose SPR. Reminder effects -reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci. 2002;15:1759–65.CrossRefGoogle Scholar
  21. Anokhin PK. Biology and neurophysiology of the conditioned reflex and its role in adaptive behavior. New York: Pergamon Press; 1974.Google Scholar
  22. Barry DN, Commins S. Imaging spatial learning in the brain using immediate early genes: insights, opportunities and limitations. Rev Neurosci. 2011;22:131–42.  https://doi.org/10.1515/RNS.2011.019.CrossRefPubMedGoogle Scholar
  23. Bartlett FC. Remembering: a study in experimental and social psychology. New York: Cambridge University Press; 1995.CrossRefGoogle Scholar
  24. Bonner JT. The evolution of complexity by means of natural selection. Princeton, NJ: Princeton University Press; 1988.Google Scholar
  25. Brecht M, Scneider M, Manns ID. Silent neurons in sensorimotor cortices: implication for cortical plasticity. In: Ebner FF, editor. Neural plasticity in adult somatic sensory-motor systems. Boca Raton: Taylor & Francis Group, LLC; 2005. p. 1–19.Google Scholar
  26. Buitrago MM, Ringer T, Schulz JB, Dichgans J, Luft AR. Characterization of motor skill and instrumental learning time scales in a skilled reaching task in rat. Behav Brain Res. 2004;155:249–56.CrossRefGoogle Scholar
  27. Bunge MA. Causality: the place of the causal principle in modern science. Cambridge: Harvard University Press; 1963.Google Scholar
  28. Burgess N, O’Keefe J. Models of place and grid cell firing and theta rhythmicity. Curr Opin Neurobiol. 2011;21(5):734–44.  https://doi.org/10.1016/j.conb.2011.07.002.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Cacioppo JT, Gardner WL. Emotion. Annu Rev Psychol. 1999;50:191–214.CrossRefGoogle Scholar
  30. Carleton A, Petreanu LT, Lansford L, Lledo P-M. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci. 2003;6:507–18.CrossRefGoogle Scholar
  31. Changeux JP, Connes A. Conversations on mind, matter, and mathematics. Princeton, NJ: Princeton University Press; 1999.Google Scholar
  32. Chestek CA, Batista AP, Santhanam G, Yu BM, Afshar A, Cunningham JP, Gilja V, Ryu SI, Churchland MM, Shenoy KV. Single-neuron stability during repeated reaching in macaque premotor cortex. J Neurosci. 2007;27:10742–50.CrossRefGoogle Scholar
  33. Cisek PI, Kalaska JF. Neural mechanisms for interacting with a world full of action choices. Annu Rev Neurosci. 2010;33:269–98.  https://doi.org/10.1146/annurev.neuro.051508.135409.CrossRefPubMedGoogle Scholar
  34. Clayton DF. The genomic action potential. Neurobiol Learn Mem. 2000;74:185–216.CrossRefGoogle Scholar
  35. Davis S, Renaudineau S, Poirier R, Poucet B, Save E, Laroche S. The formation and stability of recognition memory: what happens upon recall? Front Behav Neurosci. 2010;4:177.  https://doi.org/10.3389/fnbeh.2010.00177.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Defelipe J. The evolution of the brain, the human nature of cortical circuits, and intellectual creativity. Front Neuroanat. 2011;5:29.  https://doi.org/10.3389/fnana.2011.00029.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Dudai Y. Memory from a to Z. Keywords, concepts and beyond. Oxford: Oxford University Press; 2002.Google Scholar
  38. Dudai Y. The restless engram consolidations never end. Annu Rev Neurosci. 2012;35:227–47.  https://doi.org/10.1146/annurev-neuro-062111-150500.CrossRefPubMedGoogle Scholar
  39. Dudai Y, Eisenberg M. Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron. 2004;44:93–100.CrossRefGoogle Scholar
  40. Dudai Y, Karni A, Born J. The consolidation and transformation of memory. Neuron. 2015;88(1):20–32.  https://doi.org/10.1016/j.neuron.2015.09.004.CrossRefPubMedGoogle Scholar
  41. Edelman GM. Neural Darwinism: the theory of neural group selection. New York: Basic Books; 1987.Google Scholar
  42. Einarsson EO, Nader K. Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory. Learn Mem. 2012;19:449–52.  https://doi.org/10.1101/lm.027227.112.CrossRefPubMedGoogle Scholar
  43. Engel AK, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top–down processing. Nat Rev Neurosci. 2001;2(10):704–16.  https://doi.org/10.1038/35094565.CrossRefPubMedGoogle Scholar
  44. Erickson CA, Desimone R. Responses of macaque perirhinal neurons during and after visual stimulus association learning. J Neurosci. 1999;19:10404–16.CrossRefGoogle Scholar
  45. Feld GB, Born J. Sculpting memory during sleep: concurrent consolidation and forgetting. Curr Opin Neurobiol. 2017;44:20–7.  https://doi.org/10.1016/j.conb.2017.02.012.CrossRefPubMedGoogle Scholar
  46. Fodor J. Against darwinism. In: Vosniadou S, Kayser D, Protopapas A, editors. Proceedings of EuroCogSci07. Hillsdale, NJ: Lawrence Erlbaum Associates; 2007. p. 23–8.Google Scholar
  47. Frankland PW, Kohler S, Josselyn SA. Hippocampal neurogenesis and forgetting. Trends Neurosci. 2013;36:497–503.  https://doi.org/10.1016/j.tins.2013.05.002.CrossRefPubMedGoogle Scholar
  48. Fraser GW, Schwartz AB. Recording from the same neurons chronically in motor cortex. J Neurophysiol. 2012;107:1970–8.  https://doi.org/10.1152/jn.01012.2010.CrossRefPubMedGoogle Scholar
  49. Freeman JH Jr, Gabriel M. Changes of cingulothalamic topographic excitation patterns and avoidance response incubation over time following initial discriminative conditioning in rabbits. Neurobiol Learn Mem. 1999;72:259–72.CrossRefGoogle Scholar
  50. Gabriel M, Vogt BA, Kubota Y, Poremba A, Kang E. Training-stage related neuronal plasticity in limbic thalamus and cingulate cortex during learning: a possible key to mnemonic retrieval. Behav Brain Res. 1991;46:175–85.CrossRefGoogle Scholar
  51. Gavrilov V, Grinchenko YV, Alexandrov YI. Do neurons in homologous cortical areas of rabbits and rats have similar behavioral specialization? FENS Abstr. 2002;1:A040.8.Google Scholar
  52. Gorkin AG, Shevchenko DG. Distinctions in the neuronal activity of the rabbit limbic cortex under different training strategies. Neurosci Behav Physiol. 1996;26(2):103–12.CrossRefGoogle Scholar
  53. Greenberg PA, Wilson FAW. Functional stability of dorsolateral prefrontal neurons. J Neurophysiol. 2004;92:1042–55.CrossRefGoogle Scholar
  54. Gregory TR. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol Rev. 2001;76:65–101.CrossRefGoogle Scholar
  55. Grosmark AD, Buzsáki G. Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences. Science. 2016;351(6280):1440–3.  https://doi.org/10.1126/science.aad1935.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Hartley T, Lever C, Burgess N, O’Keefe J. Space in the brain: how the hippocampal formation supports spatial cognition. Philos Trans R Soc Lond Ser B Biol Sci. 2013;369(1635):20120510.  https://doi.org/10.1098/rstb.2012.0510.CrossRefGoogle Scholar
  57. Hayden BY, Smith DV, Platt ML. Cognitive control signals in posterior cingulate cortex. Front Hum Neurosci. 2010;4:1–8.  https://doi.org/10.3389/fnhum.2010.00223.CrossRefGoogle Scholar
  58. Hennies N, Ralph MA, Kempkes M, Cousins JN, Lewis PA. Sleep spindle density predicts the effect of prior knowledge on memory consolidation. J Neurosci. 2016;36(13):3799–810.  https://doi.org/10.1523/JNEUROSCI.3162-15.2016.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Herrera DG, Robertson HA. Activation of c-fos in the brain. Prog Neurobiol. 1996;50(2–3):83–107.CrossRefGoogle Scholar
  60. Horn G. Pathways of the past: the imprint of memory. Nat Rev Neurosci. 2004;5:108–21.CrossRefGoogle Scholar
  61. Hoshiba Y, Wada T, Hayashi-Takagi A. Synaptic ensemble underlying the selection and consolidation of neuronal circuits during learning. Front Neural Circuits. 2017;11:12.  https://doi.org/10.3389/fncir.2017.00012.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Hupbach A, Gomez R, Hardt O, Nadel L. The dynamics of memory: context-dependent updating. Learn Mem. 2008;15:574579.  https://doi.org/10.1101/lm.1022308.CrossRefGoogle Scholar
  63. Jackson A, Mavoori J, Fetz EE. Correlations between the same motor cortex cells and arm muscles during a trained task, free behavior, and natural sleep in the macaque monkey. J Neurophysiol. 2007;97:360–74.CrossRefGoogle Scholar
  64. Kandel ER. In search of memory: the emergence of a new science of mind. New York: WW Norton & Company; 2006.Google Scholar
  65. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG. Functional MRI evidences for adult motor cortex plasticity during motor skill learning. Nature. 1995;377:155–8.CrossRefGoogle Scholar
  66. Katche C, Dorman G, Slipczuk L, Cammarota M, Medina JH. Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory. Learn Mem. 2013;20:170–3.  https://doi.org/10.1101/lm.030080.112.CrossRefPubMedGoogle Scholar
  67. Kelly AMC, Garavan H. Human functional neuroimaging of brain changes associated with practice. Cereb Cortex. 2005;15:1089–102.CrossRefGoogle Scholar
  68. Kempermann G, Kuhn GH, Gage FH. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci. 1998;18:3206–12.CrossRefGoogle Scholar
  69. Kitamura T, Ogawa SK, Roy DS, Okuyama T, Morrissey MD, Smith LM, Redondo RL, Tonegawa S. Engrams and circuits crucial for systems consolidation of a memory. Science. 2017;356(6333):73–8.  https://doi.org/10.1126/science.aam6808.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Korhonen O, Saarimäki H, Glerean E, Sams M, Saramäki J. Consistency of regions of interest as nodes of fMRI functional brain networks. Netw Neurosci. 2017;1(3):254–74.  https://doi.org/10.1162/NETN_a_00013.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Kubik S, Miyashita T, Guzowski JF. Using immediate-early genes to map hippocampal subregional functions. Learn Mem. 2007;14:758–70.CrossRefGoogle Scholar
  72. Kuzina EA, Gorkin AG, AlexandrovYu.I. Neuron activity in the retrosplenial cortex of the rat at the early and late stages of memory consolidation. Neuroscience and Behavioral Physiology. 2016;46(7):789–793. https://doi.org/10.1007/s11055-016-0312-z.CrossRefGoogle Scholar
  73. Lee Y, Park KH, Baik SH, Chi C. Attenuation of c-Fos basal expression in the cerebral cortex of aged rat. Neuroreport. 1998;9:2733–6.CrossRefGoogle Scholar
  74. Leist M, Jäättelä M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev. 2001;2:1–10.CrossRefGoogle Scholar
  75. Lohmann G, Stelzer J, Zuber V, Buschmann T, Margulies D, Bartels A, Scheffler K. Task-related edge density (TED)—a new method for revealing dynamic network formation in fMRI data of the human brain. PLoS One. 2016;11(6):e0158185.  https://doi.org/10.1371/journal.pone.0158185.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Maleeva NE, Ivolgina GL, Anokhin KV, Limborskaia SA. Analysis of the expression of the c-fos proto-oncogene in the rat cerebral cortex during learning. Genetika. 1989;25(6):1119–21. (in Russian).PubMedGoogle Scholar
  77. Manahan-Vaughan D, Behnish T, Reymann KG. ACPD-mediated slow-onset potentiation is associated with cell death in the rat CA1 region in vivo. Neuropharmacology. 1999;38:487–94.CrossRefGoogle Scholar
  78. Mceachern JC, Shaw CA. An alternative to the LTP orthodoxy: a plasticity-pathology continuum model. Brain Res Rev. 1996;22:51–92.CrossRefGoogle Scholar
  79. Mckenzie S, Eichenbaum H. Consolidation and reconsolidation: two lives of memories? Neuron. 2011;71:224–33.  https://doi.org/10.1016/j.neuron.2011.06.037.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Mckenzie S, Robinson NT, Herrera L, Churchill JC, Eichenbaum H. Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema. J Neurosci. 2013;33(25):10243–56.  https://doi.org/10.1523/JNEUROSCI.0879-13.2013.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Mcmahon DB, Jones AP, Bondar IV, Leopold DA. Face-selective neurons maintain consistent visual responses across months. Proc Natl Acad Sci U S A. 2014;111(22):8251–6.  https://doi.org/10.1073/pnas.1318331111.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Meyer RE. Physiologic measures of animal stress during transitional states of consciousness. Animals (Basel). 2015;5(3):702–16.  https://doi.org/10.3390/ani5030380.CrossRefGoogle Scholar
  83. Minatohara K, Akiyoshi M, Okuno H. Role of immediate-early genes in synaptic plasticity and neuronal ensembles underlying the memory trace. Front Mol Neurosci. 2016;8:78.  https://doi.org/10.3389/fnmol.2015.00078.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Moscovitch M, Cabeza R, Winocur G, Nadel L. Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rev Psychol. 2016;67:105–34.  https://doi.org/10.1146/annurev-psych-113011-143733.CrossRefPubMedPubMedCentralGoogle Scholar
  85. Nader K. Response to Arshavsky: challenging the old views. Trends Neurosci. 2003;26:466–8.CrossRefGoogle Scholar
  86. Nader K. Reconsolidation and the dynamic nature of memory. Cold Spring Harb Perspect Biol. 2015;7:1–16.  https://doi.org/10.1101/cshperspect.a021782.CrossRefGoogle Scholar
  87. Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 2000;406:722–6.CrossRefGoogle Scholar
  88. Neisser U. Cognition and reality: principles and implications of cognitive psychology. New York: Freeman; 1976.Google Scholar
  89. O’Keefe J. Place units in the hippocampus of the freely moving rat. Exp Neurol. 1976;51:78–109.CrossRefGoogle Scholar
  90. Paton JA, Nottebohm FN. Neurons generated in the adult brain are recruited into functional circuits. Science. 1984;225:1046–8.CrossRefGoogle Scholar
  91. Paxinos G, Watson C. The rat brain in stereotaxic co-ordinates. New York: Academic; 1997.Google Scholar
  92. Piaget J. Play, dreams, and imitation in childhood. New York: Norton; 1951.Google Scholar
  93. Prickaerts J, Koopmans G, Blokland A, Scheepens A. Learning and adult neurogenesis: survival with or without proliferation? Neurobiol Learn Mem. 2004;81:1–11.CrossRefGoogle Scholar
  94. Ranganath C, Rainer G. Neural mechanisms for detecting and remembering novel events. Nat Rev Neurosci. 2003;4:193–202.CrossRefGoogle Scholar
  95. Raoul C, Pettmann B, Henderson CE. Active killing of neurons during development and following stress: a role for p75NTR and Fas? Curr Opin Neurobiol. 2000;10:111–7.CrossRefGoogle Scholar
  96. Rose S. The making of memory: from molecules to mind. London: Bantam Books; 1993.Google Scholar
  97. Sara SJ. Retrieval and reconsolidation: toward a neurobiology of remembering. Learn Mem. 2000;7:73–84.CrossRefGoogle Scholar
  98. Schmidt EM, Bak MJ, Mcintosh JS. Long-term chronic recordings from cortical neurons. Exp Neurol. 1976;52:496–506.CrossRefGoogle Scholar
  99. Sherstnev VV, Gruden MA, Alexandrov YI, Storozheva ZI, Golubeva ON, Proshin AT. Different populations of neurons in relevant brain structures are selectively engaged in the functioning of long-term spatial memory. Neurochem J. 2013;7(4):278–83.CrossRefGoogle Scholar
  100. Shima K, Mushiake H, Saito N, Tanji J. Role for cells in the presupplementary motor area in updating motor plans. Proc Natl Acad Sci U S A. 1996;93:8694–8.CrossRefGoogle Scholar
  101. Shors TJ, Matzel LD. Long-term potentiation [LTP]: what’s learning got to do with it? Behav Brain Sci. 1997;20:597–655.PubMedGoogle Scholar
  102. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature. 2001;410:372–6.CrossRefGoogle Scholar
  103. Shvyrkov VB. Behavioral specialization of neurons and the system-selection hypothesis of learning. In: Klix F, Hagendorf H, editors. Human memory and cognitive capabilities. Amsterdam: Elsevier; 1986. p. 599–611.Google Scholar
  104. Smith DM, Barredo J, Mizumori SJY. Complimentary roles of the hippocampus and retrosplenial cortex in behavioral context discrimination. Hippocampus. 2012;22:1121–33.  https://doi.org/10.1002/hipo.20958.CrossRefPubMedGoogle Scholar
  105. Sozinov AA, Kazymaev SA, Grinchenko YV, Alexandrov YI. Percent of task-specialized cingulate cortex neurons does not change during training. FENS Abstr. 2012;6:114.08.Google Scholar
  106. Stone EA, Zhang Y, John S, Filer D, Bing G. Effect of locus coeruleus lesion on c-fos expression in the cerebral cortex caused by yohimbine injection or stress. Brain Res. 1993;603:181–5.CrossRefGoogle Scholar
  107. Strassmann JE, Zhu Y, Queller DC. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature. 2000;408:965–7.CrossRefGoogle Scholar
  108. Svarnik OE, Alexandrov YI, Gavrilov VV, Grinchenko YV, Anokhin KV. Fos expression and task-related neuronal activity in rat cerebral cortex after instrumental learning. Neuroscience. 2005;136:33–42.CrossRefGoogle Scholar
  109. Svarnik OE, Bulava AI, Alexandrov YI. Expression of c-Fos in the rat retrosplenial cortex during instrumental re-learning of appetitive bar-pressing depends on the number of stages of previous training. Front Behav Neurosci. 2013;7:78.  https://doi.org/10.3389/fnbeh.2013.00078.CrossRefPubMedPubMedCentralGoogle Scholar
  110. Swadlow HA, Hicks TP. Subthreshold receptive ields and baseline excitability of “silent” S1 callosal neurons in awake rabbits: contributions of AMPA/kainate and NMDA receptors. Exp Brain Res. 1997;115:403–9.CrossRefGoogle Scholar
  111. Thompson LT, Best PJ. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 1990;509:299–308.CrossRefGoogle Scholar
  112. Tischmeyer W, Kaczmarek L, Strauss M, Jork R, Matthies H. Accumulation of c-fos mRNA in rat hippocampus during acquisition of a brightness discrimination. Behav Neural Biol. 1990;54(2):165–71.CrossRefGoogle Scholar
  113. Tolman EC. Cognitive maps in rats and men. Psychol Rev. 1948;55(4):189–208.CrossRefGoogle Scholar
  114. Tracy J, Flanders A, Madi S, Laskas J, Stoddard E, Pyrros A, Natale P, Delvecchio N. Regional brain activation associated with different performance patterns during learning of a complex motor skill. Cereb Cortex. 2003;13:904–10.CrossRefGoogle Scholar
  115. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RGM. Schemas and memory consolidation. Science. 2007;316:76–82.CrossRefGoogle Scholar
  116. Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, Bito H, Morris RGM. Schema-dependent gene activation and memory encoding in neocortex. Science. 2011;333:891–5.  https://doi.org/10.1126/science.1205274.CrossRefPubMedGoogle Scholar
  117. Vetere G, Restivo L, Novembre G, Aceti M, Lumaca M, Ammassari-Teule M. Extinction partially reverts structural changes associated with remote fear memory. Learn Mem. 2011;18:554–7.  https://doi.org/10.1101/lm.2246711.CrossRefPubMedGoogle Scholar
  118. Vikman KS, Duggan AW, Siddall PJ. Increased ability to induce long-term potentiation of spinal dorsal horn neurons in monoarthritic rats. Brain Res. 2003;990:51–7.CrossRefGoogle Scholar
  119. Vogt BA, Sikers RW, Swaldow HA, Weyand TG. Rabbit cingulate cortex: cytoarchitecture, physiological border with visual cortex, and different cortical connections of visual, motor, postsubicular and intracingulate origin. J Comp Neurol. 1986;248:74–94.CrossRefGoogle Scholar
  120. von Stein A, Chiang C, König P. Top-down processing mediated by interareal synchronization. Proc Natl Acad Sci. 2000;97(26):14748–53.  https://doi.org/10.1073/pnas.97.26.14748.CrossRefGoogle Scholar
  121. Weber A, Prokazov Y, Zuschratter W, Hauser MJB. Desynchronisation of glycolytic oscillations in yeast cell populations. PLoS One. 2012;7(9):e43276.CrossRefGoogle Scholar
  122. Weible AP, Rowland DC, Pang R, Kentros C. Neural correlates of novel object and novel location recognition behavior in the mouse anterior cingulate cortex. J Neurophysiol. 2009;102:2055–68.  https://doi.org/10.1152/jn.00214.2009.CrossRefPubMedGoogle Scholar
  123. Weible AP, Rowland DC, Monaghan CK, Wolfgang NT, Kentros CG. Neural correlates of long-term object memory in the mouse anterior cingulate cortex. J Neurosci. 2012;32:5598–608.  https://doi.org/10.1523/JNEUROSCI.5265-11.2012.CrossRefPubMedGoogle Scholar
  124. Whishaw IQ, Sarna JR, Pellis SM. Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav Brain Res. 1998;96:79–91.CrossRefGoogle Scholar
  125. Williams JC, Rennaker RL, Kipke DR. Stability of chronic multichannel neural recordings: implications for a long-term neural interface. Neurocomputing. 1999;26:1069–76.CrossRefGoogle Scholar
  126. Wilson MA, Mcnaughton BL. Dynamics of the hippocampal ensemble code for space. Science. 1993;261:1055–8.CrossRefGoogle Scholar
  127. Wirth S, Yanike M, Frank LM, Smith AC, Brown EN, Wendy AS. Single neurons in the monkey hippocampus and learning new associations. Science. 2003;300:1578–81.CrossRefGoogle Scholar
  128. Wright R. The moral animal: evolutionary psychology and everyday life. New York: Vintage Books; 1995.Google Scholar
  129. Xue ZM. The studies on neurogenesis induced by brain injury in adult ring dove. Cell Res. 1998;8:151–62.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Yuri I. Alexandrov
    • 1
    • 2
  • Alexey A. Sozinov
    • 2
    • 3
  • Olga E. Svarnik
    • 2
  • Alexander G. Gorkin
    • 2
  • Evgeniya A. Kuzina
    • 2
  • Vladimir V. Gavrilov
    • 2
  1. 1.Department of PsychologyNational Research University Higher School of EconomicsMoscowRussia
  2. 2.Shvyrkov’s LabNeural Bases of Mind, Institute of Psychology, Russian Academy of SciencesMoscowRussia
  3. 3.Faculty of PsychologyNational Academic University of HumanitiesMoscowRussia

Personalised recommendations