Abstract
According to our suggested hypothesis, long-term memory is a collection of “gnostic units,” selectively tuned to past events. The formation of long-term memory occurs with the involvement of constantly appearing new neurons which differentiate from stem cells during the process of neurogenesis, in particular in adults. Conversion of precursor neurons into “gnostic units” selective in relation to ongoing events, supplemented by the involvement of hippocampal “novelty neurons,” which increase the flow of information needing to be fixed in long-term memory. “Gnostic units” form before the informational processes occurring in the ventral (“what?”) and dorsal (“where?”) systems. Formation of new “gnostic units” selectively tuned to a particular event results from the combination of excitation of the detector for stimulus characteristics and the novelty signal generated by “novelty neurons” in the hippocampus.
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REFERENCES
K. V. Anokhin, “Molecular scenarios for the consolidation of longterm memory,”; Zh. Vyssh. Nerv. Deyat., 47, No. 2, 261–279 (1997).
K. V. Anokhin, A. É. Ryabinin, and K. V. Sudakov, “Expression of the c-fos gene in mice during acquisition of defensive behavioral habits,”; Zh. Vyssh. Nerv. Deyat., 50, No. 8, 88–94 (2000).
O. S. Vinogradova, The Hippocampus and Memory [in Russian], Nauka, Moscow (1975).
J. M. R. Delgado, Brain and Consciousness [Russian translation], Mir, Moscow (1971).
A. R. Luriya, The Bases of Neuropsychology [in Russian], Moscow State University, Moscow (1973).
O. E. Svarnik, K. V. Anokhin, and Yu. I. Aleksandrov, “Distribution of behaviorally specialized neurons and the expression of the c-Fos transcription factor in the rat cerebral cortex during learning,”; Zh. Vyssh. Nerv. Deyat., 51, No. 6, 758–761 (2001).
E. N. Sokolov, "The question of gestalt in neurobiology, Zh. Vyssh. Nerv. Deyat., 46, No. 2, 229–240 (1996).
E. N. Sokolov, “Vector coding and neural maps,”; Zh. Vyssh. Nerv. Deyat., 46, No. 1, 7–13 (1996).
E. N. Sokolov, N. I. Nezlina, V. B. Polyanskii, and D. V. Evtikhin, “The orientation reflex: the 'aiming reaction' and the 'projector of attention,”; Zh. Vyssh. Nerv. Deyat., 51, No. 4, 421–437 (2001).
V. V. Sherstnev, “Neurochemical characterization of 'silent' neurons in the cortex of the brain,” Dokl. Akad. Nauk SSSR, 202, No. 6, 1473–1476 1972
J. Altman, “Are new neurons formed in the brains of adult mammals?” Science, 135, 1127–1128 (1962).
J. Altman, “Proliferation and migration of undifferentiated precursor cells in the rat during postnatal gliogenesis,” Exptl. Neurol., 16, No. 3, 263–278 (1966).
P. O. Bishop, “Neurophysiology of binocular single and stereopsis,” in: Handbook of Sensory Physiology. Central Processing of Visual Information, R. Jung (ed.), Springer-Verlag, Berlin, Heidelberg, New York (1973), Vol. 7/3, pp. 255–305.
J. M. Brezun and A. Daszuta, “Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats,” Neurosci., 89, No. 4, 999–1002 (1999).
H. A. Cameron and R. D. McKay, “Restoring production of hippocampal neurons in old age,” Nat. Neurosci., 2, No. 10, 894–897 (1999).
H. A. Cameron and R. D. McKay, “Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus,” J. Comp. Neurol., 435, No. 4, 406–417 (2001).
H. A. Cameron, C. S. Woolley, B. S. McEwen, and E. Gould, “Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat,” Neurosci., 56, No. 2, 337–344 (1993).
L. N. Chiang, I. M. Grenier, L. Ettwiller, et al., “An orchestrated gene expression component of neuronal programmed cell death revealed by cDNA array analysis,” Proc. Natl. Acad. Sci. USA, 98, No. 5, 2815–2819 (2001).
J. M. Conner, M. A. Darracq, J. Roberts, and M. H. Tuszynski, “Nontropic action of neurotrophins: subcortical nerve growth factor gene delivery reverses age-related degeneration of primate cortical cholinergic innervation,” Proc. Natl. Acad. Sci. USA, 98, No. 4, 1941–1946 (2001).
M. Cynader and D. Regan, “Neurons in cat parastriate cortex sensitive to the direction of motion in three-dimensional space,” J. Physiol. (London), 274, 549–569 (1978).
B. E. Derrick, A. D. York, and J. L. Martinez, Jr., “Increased granule cell neurogenesis in the adult dentate gyrus following mossy fiber stimulation sufficient to induce long-term potentiation,” Brain Res., 857, No. 1-2, 300–307 (2000).
A. Dosemeci, J. H. Tao-Cheng, L. Vinade, et al., “Glutamateinduced transient modification of the postsynaptic density,” Proc. Natl. Acad. Sci. USA, 98, No. 18, 10428–10432 (2001).
G. Edelman, Neural Darwinism: The Theory of Neuronal Group Selection, Basic Books, New York (1987).
P. S. Eriksson, E. Perfilieva, T. Bjork-Eriksson, et al., “Neurogenesis in the adult hippocampus,” Nat. Med., 4, No. 11, 1313–1317 (1998).
R. Feng, C. Rampon, Y. P. Tang, et al., “Deficient neurogenesis in forebrain-specific Presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces,” Neuron, 32, No. 5, 911–926 (2001).
E. Fuchs, G. Flugge, F. Ohl, et al., “Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus,” Physiol. Behav., 73, No. 3, 285–291 (2001).
C. Gheusi, H. Cremer, H. McLean, et al., “Importance of newly generated neurons in the adult olfactory bulb for odor discrimination,” Proc. Natl. Acad. Sci. USA, 97, No. 4, 1823–1828 (2000).
S. A. Goldman, “Adult neurogenesis: from canaries to the clinic,” J. Neurobiol., 36, No. 2,267–268 (1998).
M. A. Goodale, “Different spaces and different times for perception and action,” Progr. Brain Res., 134, 313–331 (2001).
E. Gould, A. Beylin, P. Tanapat, et al., “Learning enhances adult neurogenesis in the hippocampal formation,” Nat. Neurosci., 2, No. 3, 260–265 (1999).
E. Gould, N. Vail, M. Wagers, and C. G. Gross, “Adult generated hippocampal and neocortical neurogenesis in macaques have a transient existence,” Proc. Natl. Acad. Sci. USA, 98, No. 19, 10910–10917 (2001).
P. P. C. Graciadei and J. A. Monti-Graciadei, “Regeneration in the olfactory system of vertebrates,” Ann. J. Otolaryngol., 4, No. 4, 228–233 (1983).
C. G. Gross, “Neurogenesis in the brain: death of a dogma,” Nat. Rev. Neurosci., 1, No. 1, 67–73 (2000).
F. H. Hubel and T. N. Wiesel, “Brain mechanisms of vision,” Sci. Am., 241, 130–144 (1979).
K. Jin, M. Minami, I. Q. Lan, et al., “Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat,” Proc. Natl. Acad. Sci. USA, 98, No. 8, 4711–4715 (2001).
C. Because. Johansson, S. Momma, D. L. Clarke, et al., “Identification of neural stem cells in the adult mammalian central nervous system,” Cell, 98, No. 1, 25–34 (1999).
M. S. Kaplan, “Neurogenesis in the 3-month-age rat visual cortex,” J. Comp. Neurol., 195, No. 2, 323–338 (1981).
G. Kempermann, E. P. Brandon, and F. N. Gage, “Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus,” Curr. Biol., 8, No. 16, 939–942 (1998).
G. Kempermann, H. G. Kuhn, and Family. H. Gage, “More hippocampal neurons in adult mice living in an enriched environment,” Nature (London), 386, No. 6624, 493–495 (1997).
G. Kempermann, H. van Praag, and F. H. Gage, “Activity-dependent regulation of neuronal plasticity and self repair,” Prog. Brain Res., 127, 35–48 (2000).
J. Konorski, Integrative Activity of the Brain: An Interdisciplinary Approach, Chicago University Press, Chicago (1967).
D. R. Kornack and P. Rakic, “The generation, migration, and differentiation of olfactory neurons in the adult primate brain,” Proc. Natl. Acad. Sci. USA, 98, 4752–4757 (2001).
F. S. Lee and M. V. Chao, “Activation of TrK neurotrophin receptors in the absence of neurotrophins,” Proc. Natl. Acad. Sci. USA, 98, No. 6, 3555–3560 (2001).
V. Lemaire, C. Aurousseau, M. le Moal, and D. N. Abrous, “Behavioural trait of reactivity to novelty is related to hippocampal neurogenesis,” Eur. J. Neurosci., 11, No. 11, 4006–4014 (1999).
V. Lemaire, M. Koehl, M. le Moal, and D. N. Abrous, “Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus,” Proc. Natl. Acad. Sci. USA, 97, No. 20, 11032–11037 (2000).
J. P. Liu, K. Solway, R. O. Messing, and F. R. Sharp, “Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils,” J. Neurosci., 18, No. 19, 7768–7778 (1998).
C. Lopez-Garcia, A. Molowny, J. M. Garcia-Verdugo, and I. Ferrer, “Delayed postnatal neurogenesis in the cerebral cortex of lizards,” Brain Res., 471, 167–174 (1988).
M. B. Luskin, “Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate,” J. Neurobiol., 36, No. 2, 221–233 (1998).
B. S. McEwen, “Stress and hippocampal plasticity,” Ann. Rev. Neurosci., 22, 105–122 (1999).
B. S. McEwen, “The neurobiology of stress: from serendipity to clinical relevance,” Brain Res., 886, No. 1-2, 172–189 (2000).
D. E. McGuire and R. L. Davis, “Presenilin-1 and memories of the forebrain,” Neuron, 32, No. 5, 763–765 (2001).
R. McKay, “Stem cells in the central nervous system” Science, 276, No. 5309, 66–71 (1997).
S. E. McKay, A. L. Pursell, and T. J. Carew, “Regulation of synaptic function by neurotrophic factors in vertebrates and invertebrates: implications for development and learning,” Learn. Mem., 6, No. 3, 193–215 (1999).
A. Messinger, L. R. Squire, S. M. Zola, and T. D. Albright, “Neuronal representations of stimulation associations develop in the temporal lobe during learning,” Proc. Natl. Acad. Sci. USA, 98, No. 21, 12239–12244 (2001).
Y. Miyashita, K. Sakai, S.-I. Higuchi, and N. Masui, “Localization of primal long-term memory in the primate temporal cortex,” in: Memory: Organization and Locus of Change, L. R. Squire et al. (eds.), Oxford University Press, New York, Oxford (1991), pp. 239–249.
Y. Naya, M. Yoshida, and Y. Miyashita, “Backward spreading of memory-retrieval signal in the primate temporal cortex,” Science, 291, No. 5504, 661–664 (2001).
M. Nilsson, E. Perfilieva, U. Johansson, et al., “Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory,” J. Neurobiol., 39, No. 4, 569–578 (1999).
N. A. O'Rourke, “Neuronal chain gangs: homotypic contacts support migration into the olfactory bulb,” Neuron, 16, 1061–1064 (1996).
W. Penfield and Th. Rasmussen, The Cerebral Cortex of Man, Macmillan, New York (1950).
S. Pollmann and D. Y. von Cramon, “Object working memory and visuospatial processing: functional neuroanatomy analyzed by event-related fMRI,” Exptl. Brain Res., 133, No. 1, 12–22 (2000).
H. van Praag, B. R. Christie, T. J. Sejnowski, and F. H. Gage, “Running enhances neurogenesis, learning, and long-term potentiation in mice,” Proc. Natl. Acad. Sci. USA, 96, No. 23, 13427–13431 (1999).
H. van Praag, A. F. Schinder, B. R. Christie, et al., “Functional neurogenesis in the adult hippocampus,” Nature, 415, No. 6875, 1030–1034 (2002).
A. Privat and C. P. Leblond, “The subependymal layer and neighboring reaction in the brain of the young rat,”J. Comp. Neurol., 146, No. 3, 277–302 (1972).
S. C. Rao, G. Rainer, and E. K. Miller, “Integration of what and where in the primate prefrontal cortex,” Science, 276, No. 5313, 821–824 (1997).
E. T. Rolls, “Memory systems in the brain,” Ann. Rev. Psychol., 51, 599–630 (2000).
S. Rose, The Making of Memory from Molecules to Mind, Bantam Press, London, New York, Toronto, Sidney, Auckland (1992) (Russian translation from English: Mir, Moscow (1995)).
C. Scharff, “Chasing fate and function of new neurons in adult brains,” Curr. Opin. Neurobiol., 10, No. 6, 774–783 (2000).
G. E. Schneiger, “Two visual systems,” Science, 163, No. 3870, 895–902 (1969).
B. W. Scott, J. M. Wojtowicz, and W. M. Burnham, “Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures,” Exptl. Neurol., 165, No. 2, 231–236 (2000).
B. J. Shiasson, V. Tropepe, C. M. Morshead, and D. van der Kooy, “Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neuronal stem cell characteristics,” J. Neurosci., 19, No. 11, 4462–4471 (1999).
T. J. Shors, G. Miesegaes, A. Beylin, et al., “Neurogenesis in the adult is involved in the formation of trace memories,” Nature, 410, No. 6826, 372–376 (2001).
J. S. Snyder, N. Kee, and J. M. Woitowich, “Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus,” J. Neurophysiol., 85, No. 6, 2423–2431 (2001).
H. J. Song, and M. M. Poo, “Signal transduction underlying growth cone guidance by diffusible factors,” Curr. Opin. Neurobiol., 9, No. 3, 355–363 (1999).
L. R. Squire, “The neuropsychology of human memory,” Ann. Rev. Neurosci., 5, 241–273 (1987).
S. Temple and A. Alvarez-Buylla, “Stem cells in the adult mammalian central nervous system” Curr. Opin. Neurobiol., 9, 135–141 (1999).
H. Tomasiewicz, K. Ono, D. Yee, et al., “Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system” Neuron, 11, 1163–1174 (1993).
E. Tulving, “Concepts of human memory,” in: Memory Organization and Locus of Change, L. R. Squire, et al. (eds.), Oxford University Press, New York (1991), pp. 3–32.
L. G. Underleider and M. Mishkin, “Two cortical visual systems,” in: Analysis of Visual Behavior, D. I. Ingle, M. A. Goodale, and R. J. Mansfield (eds.), MIT Press, Cambridge, MA (1982), pp. 549–586.
B. M. Williams, Y. Luo, C. Ward, et al., “Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity,” Physiol. Behav., 73, No. 4, 649–658 (2001).
E. J. Yang, Y. S. Ahn, and K. C. Chung, “Protein kinase Dyrk 1 activates cAMP response element-binding protein during neuronal differentiation in hippocampal progenitor cells,” J. Biol. Chem., 276, No. 43, 39819–39824 (2001).
S. Yoshimura, Y. Takagai, I. Harada, et al., “FGF regulation of neurogenesis in adult hippocampus after brain injury,” Proc. Natl. Acad. Sci. USA, 98, No. 10, 5874–5879 (2001).
G. M. Young and S. W. Levison, “Persistence of multipotential progenitors in the juvenile rat subventricular zone,” Devl. Neurosci., 18, No. 4, 255–256 (1996).
D. Young, P. A. Lawlor, P. Leone, et al., “Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective,” Nat. Med., 5, No. 4, 448–453 (1999).
S. Zeki, “Colour coding in the cerebral cortex: the responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition,” Neurosci., 9, No. 4, 767–781 (1983).
S. Zeki, “Localization and globalization in conscious vision,” Ann. Rev. Neurosci., 24, 57–86 (2001).
S. C. Zhang, B. Ge, and I. D. Duncan, “Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity,” Proc. Natl. Acad. Sci. USA, 96, No. 7, 4089–4094 (1999).
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Sokolov, E.N., Nezlina, N.I. Long-Term Memory, Neurogenesis, and Signal Novelty. Neurosci Behav Physiol 34, 847–857 (2004). https://doi.org/10.1023/B:NEAB.0000038138.75801.85
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DOI: https://doi.org/10.1023/B:NEAB.0000038138.75801.85