Skip to main content
Log in

A review of cell assemblies

  • Review
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Since the cell assembly (CA) was hypothesised, it has gained substantial support and is believed to be the neural basis of psychological concepts. A CA is a relatively small set of connected neurons, that through neural firing can sustain activation without stimulus from outside the CA, and is formed by learning. Extensive evidence from multiple single unit recording and other techniques provides support for the existence of CAs that have these properties, and that their neurons also spike with some degree of synchrony. Since the evidence is so broad and deep, the review concludes that CAs are all but certain. A model of CAs is introduced that is informal, but is broad enough to include, e.g. synfire chains, without including, e.g. holographic reduced representation. CAs are found in most cortical areas and in some sub-cortical areas, they are involved in psychological tasks including categorisation, short-term memory and long-term memory, and are central to other tasks including working memory. There is currently insufficient evidence to conclude that CAs are the neural basis of all concepts. A range of models have been used to simulate CA behaviour including associative memory and more process- oriented tasks such as natural language parsing. Questions involving CAs, e.g. memory persistence, CAs’ complex interactions with brain waves and learning, remain unanswered. CA research involves a wide range of disciplines including biology and psychology, and this paper reviews literature directly related to the CA, providing a basis of discussion for this interdisciplinary community on this important topic. Hopefully, this discussion will lead to more formal and accurate models of CAs that are better linked to neuropsychological data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. An atomic CA is not composed of other CAs.

  2. Statistical mechanics can be used to describe CAs, with a set of firing neurons being an attractor basin. The Hopfield model (Hopfield 1982 and see Sect. 5.1.3) is a particularly good example of attractor basins with a particular set of neurons firing and then continuing to fire in response to a particular input. The firing pattern moves from the initial input state, down an energy slope to a new firing state, which has attracted the activity.

  3. If a language is Turing complete, anything that can be programmed can be programmed in it. So, to some degree, CAs are equivalent to Java.

References

  • Abbott L (1999) Lapicque’s introduction of the integrate-and-fire model neuron (1907). Brain Res 50:303–304

    CAS  Google Scholar 

  • Abbott L, Nelson S (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3:1178–1183

    Article  CAS  PubMed  Google Scholar 

  • Abeles M, Bergman H, Margalit E, Vaadia E (1993) Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J Neurophysiol 70(4):1629–1638

    CAS  PubMed  Google Scholar 

  • Ackley D, Hinton G, Sejnowski T (1985) A learning algorithm for boltzmann machines. Cogn Sci 9:147–169

    Article  Google Scholar 

  • Amari S (1977) Neural theory of association and concept-formation. Biol Cybern 26:175–185

    Article  CAS  PubMed  Google Scholar 

  • Amit D (1989) Modelling brain function: the world of attractor neural networks. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Amit D, Brunel N (1995) Learning internal representations in an attractor neural network with analogue neurons. Netw Comput Neural Syst 6:359–388

    Article  Google Scholar 

  • Anderson J, Lebiere C (1998) The atomic components of thought. Lawrence Erlbaum, New Jersey

  • Assad W, Rainer G, Miller E (2000) Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 84:451–459

    Google Scholar 

  • Auseng P, Grismayr B, Freunberger R, Klimesch W (2010) Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci Biobehav Rev 34:1015–1022

    Article  Google Scholar 

  • Averbeck B, Latham P, Pouget A (2006a) Neural correlations, population coding and computation. Nat Rev Neurosci 7:358–366

    Article  CAS  PubMed  Google Scholar 

  • Averbeck B, Sohn J, Lee D (2006b) Activity in prefrontal cortex during dynamic selection of action sequences. Nat Neurosci 9(2): 276–282

    Google Scholar 

  • Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4:829–839

    Article  CAS  PubMed  Google Scholar 

  • Baeg E, Kim Y, Kim J, Ghim J, Kim J, Jung M (2007) Learning-induced enduring changes in functional connectivity among prefrontal cortical neurons. J Neurosci 27(4):909–918

    Article  CAS  PubMed  Google Scholar 

  • Barlow H (1972) Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1:371–394

    Article  CAS  PubMed  Google Scholar 

  • Belavkin R, Huyck C (2010) Conflict resolution and learning probability matching in a neural cell-assembly architecture. Cogn Syst Res 12:93–101

    Article  Google Scholar 

  • Bendor D, Wang X (2008) Neural response properties of primary, rostral, and rostraltemporal core fields in the auditory cortex of marmoset monkeys. J Neurophysiol 100:888–906

    Article  PubMed  Google Scholar 

  • Bennett B, Callaway J, Wilson C (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20(22):8493–8503

    CAS  PubMed  Google Scholar 

  • Bertschinger N, Natschlager T (2004) Real-time computation at the edge of chaos in recurrent neural networks. Neural Comput 16(7):1413–1436

    Article  PubMed  Google Scholar 

  • Beurle R (1956) Properties of a mass of cells capable of regenerating pulses. Trans R Soc Lond B 240:55–94

    Article  Google Scholar 

  • Bevan M, Wilson C (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19:7617–7628

    CAS  PubMed  Google Scholar 

  • Bi G, Poo M (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10464–10472

    Google Scholar 

  • Bichot N, Schall J (1999) Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci 2(6):549–554

    Article  CAS  PubMed  Google Scholar 

  • Bieser A, Muller-Preuss P (1996) Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds. Exp Brain Res 108:273–284

    Article  CAS  PubMed  Google Scholar 

  • Bisley J, Zaksas D, Droll J, Pasternak T (2004) Activity of neurons in cortical area MT during a memory for motion task. J Neurophysiol 91:286–300

    Article  PubMed  Google Scholar 

  • Bogacz R (2007) Optimal decision network with distributed representation. Neural Netw 20:564–576

    Article  PubMed  Google Scholar 

  • Booth J, Burman D, Meyer J, Gitelman D, Parrish T (2004) Development of brain mechanisms for processing orthographic and phonologic representations. J Cogn Neurosci 16(7):1234–1249

    Article  PubMed  Google Scholar 

  • Braitenberg V (1978) Cell assemblies in the cerebral cortex. In: Heim R, Palm G (eds) Theoretical Approaches to Complex Systems. Lecture Notes in Biomathematics, vol 21. Springer, Berlin, pp 171–188

  • Braitenberg V (1989) Some arguments for a theory of cell assemblies in the cerebral cortex. In: Nadel C, Culicover H (eds) Neural connections, mental computation. MIT Press, Cambridge

  • Brecht M, Schneider M, Sakmann B, Margrie T (2004) Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427:704–710

    Article  CAS  PubMed  Google Scholar 

  • Bressler S (1995) Large-scale cortical networks and cognition. Brain Res Rev 20:288–304

    Article  CAS  PubMed  Google Scholar 

  • Brette R, Rudolph M, Carnevale T, Hines M, Beeman D, Bower J, Diesmann M, Morrison A, Goodman P, Harris F, Zirpe M, Natschalager T, Pecevski D, Ermentrout B, Djurfeldt M, Lansner A, Rochel O, Vieville T, Muller E, Dafison A, ElBoustani S, Destexhe A (2007) Simulation of networks of spiking neurons: a review of tools and strategies. J Comput Neurosci 23:349–398

    Article  PubMed  Google Scholar 

  • Bruno R, Sakmann B (2006) Cortex is driven by weak by synchronously active thalamocortical synapses. Science 312:1622–1627

    Article  CAS  PubMed  Google Scholar 

  • Buckner R, Wheeler M (2001) The cognitive neuroscience of remembering. Nat Rev Neurosci 2:624–634

    Article  CAS  PubMed  Google Scholar 

  • Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198

    Article  CAS  PubMed  Google Scholar 

  • Buonomano D, Merzenich M (1998) Cortical plasticity: from synapses to maps. Ann Rev Neurosci 21:149–186

    Google Scholar 

  • Burgess N, Hitch G (2005) Computational models of working memory: putting long-term memory into context. Trends Cogn Sci 9(11):535–541

    Article  PubMed  Google Scholar 

  • Burkitt A (2006) A review of the integrate-and-fire neuron model: I. homogeneous synaptic input. Biol Cybern 95(1):1–19

    Article  CAS  PubMed  Google Scholar 

  • Butt S, Harris-Warrick R, Kiehn O (2002) Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J Neurosci 22(22):9961–9971

    CAS  PubMed  Google Scholar 

  • Buzaski G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929

    Article  CAS  Google Scholar 

  • Byrne E, Huyck C (2010) Processing with cell assemblies. Neurocomputing 74:76–83

    Article  Google Scholar 

  • Cho J, Sharp P (2001) Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115(1):3–25

    Article  CAS  PubMed  Google Scholar 

  • Christian K, Thompson R (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem 10:427–455

    Article  PubMed  Google Scholar 

  • Chrobak J, Buzaski G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18(1):388–398

    CAS  PubMed  Google Scholar 

  • Churchland P, Sejnowski T (1999) The computational brain. MIT Press, Cambridge

  • Constantinidis C, Procyk E (2004) The primate working memory networks. Cogn Affect Behav Neurosci 4(4):444–465

    Article  PubMed  Google Scholar 

  • Cossart R, Aronov D, Yuste R (2003) Attractor dynamics of network up states in the neocortex. Nature 423:283–288

    Article  CAS  PubMed  Google Scholar 

  • Cowan N (1988) Evolving conceptions of memory storage, selective attention, and their mutual constraints within the human information-processing system. Psychol Bull 1–4(2):163–191

    Article  Google Scholar 

  • Crowe D, Averbeck B, Chafee M (2008) Neural ensemble decoding reveals a correlate of viewer-to-object-centered spatial transformation in monkey parietal cortex. J Neurosci 28(20):5218–5228

    Article  CAS  PubMed  Google Scholar 

  • Crutcher M, Russo G, Ye S, Backus D (2004) Target-, limb-, and context-dependent neural activity in cingulate and supplementary motor areas of the monkey. Exp Brain Res 158:278–288

    Article  CAS  PubMed  Google Scholar 

  • Curtis C, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7(9):415–423

    Article  PubMed  Google Scholar 

  • Deco G, Rolls E (2005) Sequential memory: a putative neural and synaptic dynamical mechanism. J Cogn Neurosci 17(2):294–307

    Article  PubMed  Google Scholar 

  • Desimone R, Albright T, Gross C, Bruce C (1984) Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci 4(8):2051–2062

    CAS  PubMed  Google Scholar 

  • D’Esposito M (2007) From cognitive to neural models of working memory. Philos Trans R Soc 362:761–772

    Article  Google Scholar 

  • deVries P (2004) Effects of binning in the identification of objects. Psychol Res 69:41–66

    Google Scholar 

  • Diester I, Nider A (2007) Semantic associations between signs and numerical categories in prefrontal cortex. PLOS Biol 5(11):2684–2695

    Article  CAS  Google Scholar 

  • Douglas R, Martin K (1991) A functional microcircuit for cat visual cortex. J Physiol 440:735–769

    CAS  PubMed  Google Scholar 

  • Douglas R, Martin K (2004) Neuronal circuits of the neocortex. Ann Rev Neurosci 27:419–451

    Article  CAS  PubMed  Google Scholar 

  • Dragoi G, Buzaski G (2006) Temporal encoding of place sequences in hippocampal cell assemblies. Neuron 50:145–157

    Article  CAS  PubMed  Google Scholar 

  • Dragoi G, Tonegawa S (2011) Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469:397–401

    Article  CAS  PubMed  Google Scholar 

  • Durstewitz D, Seamans J, Sejnowski T (2000) Neurocomputational models of working memory. Nat Neurosci Suppl 3:1184–1191

    Article  CAS  Google Scholar 

  • Egorov A, Hamam B, Fransen E, Hasselmo M, Alonso A (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173–178

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50

    Article  CAS  PubMed  Google Scholar 

  • Eliasmith C, Thagard P (2001) Integrating structure and meaning: a distributed model of analogical mapping. Cogn Sci 25:245–286

    Article  Google Scholar 

  • Engel A, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716

    Article  CAS  PubMed  Google Scholar 

  • Engel R, Tuholski S, Laughlin J, Conway A (1999) Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. J Exp Psychol 12(3):309–331

    Article  Google Scholar 

  • Field D (1994) What is the goal of sensory coding. Neural Comput 6:559–601

    Article  Google Scholar 

  • Fischer B, Boch R, Bach M (1981) Stimulus versus eye movements: comparison of neural activity in the striate and prelunate visual cortex (a17 and a19) of trained rhesus monkey. Exp Brain Res 43:69–77

    Article  CAS  PubMed  Google Scholar 

  • Fransen E, Lansner A, Liljenstrom H (1992) A model of cortical associative memory based on hebbian cell assemblies. In: Niklasson L, Boden M (eds) Connectionism in a broad perspective. Ellis Horwood, London; Springer, Berlin, pp 165–171

  • Freedman D, Assad J (2006) Experience-dependent representation of visual categories in parietal cortex. Nature 433:85–88

    Article  CAS  Google Scholar 

  • Freiwald W, Kreiter A, Singer W (2001) Synchronization and assembly formation in the visual cortex. In: Nicolelis M (ed) Progress in brain research, vol 130. Elsevier, Amsterdam

  • Fujii H, Hiroyuke I, Aihara K, Ichinose N, Tsukada M (1996) Dynamical cell assembly hypothesis—theoretical possibility of spatio-temporal coding in the cortex. Neural Netw 9(8):1303–1350

    Article  PubMed  Google Scholar 

  • Funahashi S (2001) Neuronal mechanisms of executive control by the prefrontal cortex. Neurosci Res 39:147–165

    Article  CAS  PubMed  Google Scholar 

  • Fusi S (2008) A quiescent working memory. Science 319:1495–1496

    Article  CAS  PubMed  Google Scholar 

  • Fuster J, Alexander G (1971) Neuron activity related to short-term memory. Science 173:652–654

    Article  CAS  PubMed  Google Scholar 

  • Fuster J, Bodner M, Kroger J (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405:347–351

    Article  CAS  PubMed  Google Scholar 

  • Fyfe C (2005) Hebbian learning and negative feedback networks. Springer, Berlin

  • Gallese V, Lakoff G (2005) The brain’s concepts: the role of the sensory motor system in conceptual knowledge. Cogn Neuropsychol 22(3/4):455–479

    Article  PubMed  Google Scholar 

  • Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609

    Article  PubMed  Google Scholar 

  • Gargnani M, Wennekers T, Pulvermuller F (2007) A neuronal model of the language cortex. Neurocomputing 70:1914–1919

    Article  Google Scholar 

  • Gazzaley A, Rissman J, D’Esposito M (2004) Functional connectivity during working memory maintenance. Cogn Affect Behav Neurosci 4(4):580–599

    Article  PubMed  Google Scholar 

  • Georgopoulos A, Schwartz A, Kettner R (1986) Neuronal populations coding of movement direction. Science 233:1416–1419

    Article  CAS  PubMed  Google Scholar 

  • Gerstner W, Kistler W (2002) Mathematical formulations of hebbian learning. Biol Cybern 87:404–415

    Article  PubMed  Google Scholar 

  • Gochin P, Colombo M, Dorfman G, Gerstein G, Gross C (1994) Neural ensemble coding in inferior temporal cortex. J Neurophysiol 71(6):2325–2337

    CAS  PubMed  Google Scholar 

  • Golari G, Ghahremani D, Whitfield-Gabrieli S, Reiss A, Eberhardt J, Gabrieli J, Grill-Spector K (2007) Differential development of high-level visual cortex correlates with category-specific recognition memory. Nat Neurosci 10(4):512–522

    Google Scholar 

  • Goldman-Rakic P (1995) Cellular basis of working memory. Neuron 14:477–485

    Article  CAS  PubMed  Google Scholar 

  • Goldman-Rakic P (1996) Regional and cellular fractionation of working memory. PNAS 93:13473–13480

    Google Scholar 

  • Gray C, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. PNAS 86:1698–1702

    Article  CAS  PubMed  Google Scholar 

  • Grill-Spector K, Golarai G, Gabrieli J (2008) Developmental neuroimaging of the human ventral visual cortex. Trends Cogn Sci 12:152–162

    Article  PubMed  Google Scholar 

  • Grinvald A, Arieli A, Tsodyks M, Kenet T (2003) Neuronal assemblies: single cortical neurons are obedient members of a huge orchestra. Biopolymers 68:422–436

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez R, Carmena J, Nicolelis M, Simon S (2006) Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J Neurophysiol 95:119–133

    Article  PubMed  Google Scholar 

  • Harnad S (1990) The symbol grounding problem. Phys D 42:335–346

    Article  Google Scholar 

  • Harris K (2005) Neural signatures of cell assembly organization. Nat Rev Neurosci 6:399–407

    Article  CAS  PubMed  Google Scholar 

  • Harris K, Csicsvari J, Hirase H, Dragoi G, Buzsaki G (2003) Organization of cell assemblies in the hippocampus. Nature 424: 552–556

    Google Scholar 

  • Harrison S, Tong F (2009) Decoding reveals the contents of visual working memory in early visual areas. Nature 458:632–635

    Article  CAS  PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York

  • Hempel C, Hartman K, Wang X, Turrigiano G, Nelson S (2000) Multiple forms of short-term plasticity at excitatory in rat medial prefrontal cortex. J Neurophysiol 83:3031–3041

    CAS  PubMed  Google Scholar 

  • Henson R, Rugg M, Shallice T, Josephs O, Dolan R (1999) Recollection and familiarity in recognition in memory: an event-related functional magnetic resonance imaging study. J Neurosci 19(10): 3962–3972

    Google Scholar 

  • Hetherington P, Shapiro M (1993) Simulating hebb cell assemblies: the necessity for partitioned dendritic trees and a post-net-pre ltd rule. Netw Comput Neural Syst 4:135–153

    Google Scholar 

  • Histed M, Pasupathy A, Miller E (2009) Learning substrates in the primate prefrontal cortex and striatum: sustained activity related to successful actions. Neuron 63(2):244–253

    Article  CAS  PubMed  Google Scholar 

  • Hochberg L, Serruya M, Friehs G, Mukand J, Saleh M, Caplan A, Branner A, Chen D, Penn R, Dooghue J (2006) Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442(13):164–171

    Article  CAS  PubMed  Google Scholar 

  • Hodgkin A, Huxley A (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544

    CAS  PubMed  Google Scholar 

  • Hofstadter D (1979) Godel, escher and bach: an eternal golden braid. Basic Books, New York

  • Hopfield J (1982) Neural nets and physical systems with emergent collective computational abilities. Proc Natl Acad Sci USA 79:2554–2558

    Article  CAS  PubMed  Google Scholar 

  • Hoshino O, Miyamoto M, Zheng M, Kuroiwa K (2002) A neural network model for encoding and perception of vowel sounds. Neurocomputing 44–46:435–442

    Article  Google Scholar 

  • Howard M, Volkov I, Mirsky R, Garell P, Noh M, Granner M, Damasio H, Steinschneider M, Reale R, Hind J, Brugge J (2000) Auditory cortex on the human posterior superior temporal gyrus. J Comp Neurol 416:79–92

    Article  CAS  PubMed  Google Scholar 

  • Hubel D, Wiesel T (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154

    CAS  PubMed  Google Scholar 

  • Humphries M, Wood R, Gurney K (2009) Dopamine-modulated dynamic cell assemblies generated by the GABAergic striatal microcircuit. Neural Netw 22:1174–1188

    Article  PubMed  Google Scholar 

  • Huyck C (2007) Creating hierarchical categories using cell assemblies. Connect Sci 19(1):1–24

    Article  Google Scholar 

  • Huyck C (2009) A psycholinguistic model of natural language parsing implemented in simulated neurons. Cogn Neurodyn 3(4):316–330

    Article  Google Scholar 

  • Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D, Yuste R (2004) Synfire chains and cortical songs: temporal modules of cortical activity. Science 304(23):559–564

    Article  CAS  PubMed  Google Scholar 

  • Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T (2009) Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12(12):1586–1593

    Article  CAS  PubMed  Google Scholar 

  • Ito M (1989) Long-term depression. Ann Rev Neurosci 12:85–102

    Article  CAS  PubMed  Google Scholar 

  • Iyer L, Doboli S, Minai A, Brown V, Levine D, Paulus P (2009) Neural dynamics of idea generation and the effects of priming. Neural Netw 22:674–686

    Article  PubMed  Google Scholar 

  • Izhikevich E (2004) Which model to use for cortical spiking neurons? IEEE Trans Neural Netw 15(5):1063–1070

    Article  PubMed  Google Scholar 

  • Jackendoff R (2002) Foundations of language: brain, meaning, grammar, evolution. Oxford University Press, Oxford

    Google Scholar 

  • James W (1892) Psychology: the briefer course. University of Notre Dame Press, USA

  • Jezek K, Henriksen E, Treves A, Moser E, Moser M (2011) Theta-paced flickering between place-cell maps in the hippocampus. Nature 478:246–249

    Article  CAS  PubMed  Google Scholar 

  • Jonides J, Smith E, Koeppe R, Awh E, Minoshima S, Mintun M (1993) Spatial working memory in humans as revealed by pet. Nature 363:623–625

    Article  CAS  PubMed  Google Scholar 

  • Just M, Chherkassky V, Aryal S, Mitchell T (2010) A neurosemantic theory of concrete noun representation based on the underlying brain code. PLoS ONE 5(1):e8622

    Article  PubMed  CAS  Google Scholar 

  • Kaplan S, Weaver M, French R (1990) Active symbols and internal models: towards a cognitive connectionism. AI Soc 4:51–71

    Article  Google Scholar 

  • Kaplan S, Sontag M, Chown E (1991) Tracing recurrent activity in cognitive elements (trace): a model of temporal dynamics in a cell assembly. Connect Sci 3:179–206

    Article  Google Scholar 

  • Katz D, Simon S, Nicolelis M (2002) Taste-specific neuronal ensembles in the gustatory cortex of awake rats. J Neurosci 22(5):1850–1857

    CAS  PubMed  Google Scholar 

  • Keri S (2003) The cognitive neuroscience of category learning. Brain Res Rev 43:85–109

    Article  PubMed  Google Scholar 

  • Klausberger T, Magill P, Marton L, Roberts J, Cobden P, Buzaski G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848

    Article  CAS  PubMed  Google Scholar 

  • Kleinsmith L, Kaplan S (1963) Paired-associate learning as a function of arousal and interpolated interval. J Exp Psychol 65(2): 190–193

    Google Scholar 

  • Knoblauch A, Markert H, Palm G (2004) An associative model of cortical language and action processing. In: Proceedings of the ninth neural computation and psychology workshop

  • Knoblauch A, Kupper R, Gewaltig M, Korner U, Korner E (2007) A cell assembly based model for the cortical microcircuitry. Neurocomputing 70:1838–1842

    Article  Google Scholar 

  • Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13–24

    Article  CAS  PubMed  Google Scholar 

  • Kreiman G, Koch C, Fried I (2000) Imagery neurons in the human brain. Nature 408:357–361

    Article  CAS  PubMed  Google Scholar 

  • Kreiter A, Singer W (1996) Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J Neurosci 16(7):2381–2396

    CAS  PubMed  Google Scholar 

  • Kuo C, Chiou R, Liang K, Yen C (2009) Differential involvement of the anterior cingulate and primary sensorimotor cortices in sensory and affective functions of pain. J Neurophysiol 101:1201–1210

    Article  PubMed  Google Scholar 

  • Lamme V, Super H, Spekreijse H (1998) Feedforward, horizontal, and feedback processing in the visual cortex. Curr Opin Biol 8:525–535

    Article  Google Scholar 

  • Lansner A (2009) Associative memory models: from the cell-assembly theory to biophysically detailed cortex simulations. Trends Neurosci 32(3):178–186

    Article  CAS  PubMed  Google Scholar 

  • Lapish C, Durstewitz D, Chandler L, Seamans J (2008) Successful choice behavior is associated with distinct and coherent network states in anterior cingulate cortex. PNAS 105:33:11963–11968

    Google Scholar 

  • Larimer P, Strowbridge B (2009) Representing information in cell assemblies: persistent activity mediated by semilunar granule cells. Nat Neurosci 13:213–222

    Article  PubMed  CAS  Google Scholar 

  • Laubach M, Wessberg J, Nicolelis M (2000) Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405:567–570

    Article  CAS  PubMed  Google Scholar 

  • LeBihan D, Turner R, Zeffiro T, Cuenod C, Jezzard P, Bonnerot V (1993) Activation of human primary visual cortex during visual recall: a magnetic resonance imaging study. PNAS 90:11802–11805

    Google Scholar 

  • Levy N, Horn D, Meilijson I, Ruppin E (2001) Distributed synchrony in a cell assembly of spiking neurons. Neural Netw 14:815–824

    Article  CAS  PubMed  Google Scholar 

  • Liebenthal E, Uhlmann O, Camhi J (1994) Critical parameters of the pike trains in a cell assembly: coding of turn direction by giant interneurons of the cockroach. J Comp Physiol A 174:281–296

    Article  CAS  PubMed  Google Scholar 

  • Logothetis N, Pauls J, Poggio T (1995) Shape representation in the inferior temporal cortex of monkeys. Curr Biol 5(5):552–563

    Article  CAS  PubMed  Google Scholar 

  • Lundqvist M, Rehn M, Djurfeldt M, Lansner A (2006) Attractor dynamics in a modular neural network model of neocortex. Netw Comput Neural Syst 17:253–276

    Google Scholar 

  • Macaluso E, Frith C, Driver J (2000) Modulation of human visual cortex by crossmodal spatial attention. Science 289:1206–1208

    Article  CAS  PubMed  Google Scholar 

  • Malenka R, Nicoll R (1999) Long-term potentiation—a decade of progress? Science 285:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Maquet P (2001) The role of sleep in learning and memory. Science 10:1048–1052

    Article  Google Scholar 

  • Markram H (2006) The blue brain project. Nat Rev Neurosci 7:153–160

    Article  CAS  PubMed  Google Scholar 

  • Martini F (2001) Fundamentals of anatomy and physiology. Prentice Hall, New Jersey

    Google Scholar 

  • Maunsell J, Van Essen D (1983) Functional properties of neurons in the middle temporal visual area of the macaque monkey. I. selectivity for stimulus direction, speed and orientation. J Neurophysiol 49(5):1127–1147

    CAS  PubMed  Google Scholar 

  • McCoy A, Platt M (2005) Risk-sensitive neurons in the macaque posterior cingulate cortex. Nat Neurosci 8(9):1220–1227

    Article  CAS  PubMed  Google Scholar 

  • McCulloch W, Pitts W (1943) A logical calculus of ideas immanent in nervous activity. Bull Math Biophys 5:115–133

    Article  Google Scholar 

  • McIntosh A, Cabeza R, Lobaugh N (1998) Analysis of neural interactions explains the activation of occipital cortex by an auditory stimulus. J Am Physiol Soc 90:2790–2796

    Google Scholar 

  • McNaughton B, Battaglia F, Jensen O, Moser E, Moser M (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678

    Google Scholar 

  • Miller E, Erickson C, Desimone R (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16(16):5154–5167

    CAS  PubMed  Google Scholar 

  • Milner P (1957) The cell assembly: mark II. Psychol Rev 64(4):242–252

    Article  CAS  PubMed  Google Scholar 

  • Minsky M (1986) The society of mind. Simon and Schuster, New York

    Google Scholar 

  • Miyake A, Friedman N, Emerson M, Witzki A, Howeter A, Wager T (2000) The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol 41:49–100

    Article  CAS  PubMed  Google Scholar 

  • Mongillo G, Barak O, Tsodyks M (2008) Synaptic theory of working memory. Science 319:1543–1546

    Article  CAS  PubMed  Google Scholar 

  • Moore C, Nelson S (1998) Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol 80:2882–2892

    CAS  PubMed  Google Scholar 

  • Morrison J, Hof P (1997) Life and death of neurons in the aging brain. Science 278:412–419

    Article  CAS  PubMed  Google Scholar 

  • Nakamura K, Matsumoto K, Mikami A, Kubota K (1994) Visual response properties of single neurons in the temporal pole of behaving monkeys. J Neurophysiol 71(3):1206–1221

    CAS  PubMed  Google Scholar 

  • Nakamura K, Chung H, Graziano M, Gross C (1999) Dynamic representation of eye position in the parieto-occipital sulcus. J Neurophysiol 81:2374–2385

    CAS  PubMed  Google Scholar 

  • Naya Y, Sakai K, Miyashita Y (1996) Activity of primate inferotemporal neurons related to a sought target in pair-association task. PNAS 93:2664–2669

    Article  CAS  PubMed  Google Scholar 

  • Nee D, Jonides J (2008) Neural correlates of access to short-term memory. PNAS 105:37:14228–14233

    Google Scholar 

  • Nicolelis M, Lin R, Woodward D, Chapin J (1993) Dynamic and distributed properties of many-neuron ensembles in the ventral posterior medial thalamus of awake rats. PNAS 90:2212–2216

    Article  CAS  PubMed  Google Scholar 

  • Nicolelis M, Baccala L, Lin R, Chapin J (1995) Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268:1353–1358

    Article  CAS  PubMed  Google Scholar 

  • Nishimura M, Scherf S, Behrmann M (2009) Development of object recognition in humans. F1000 Biol Rep 1:56

    Google Scholar 

  • Nitz D, Cowen S (2008) Crossing borders: sleep reactivation as a window on cell assembly formation. Nat Neurosci 11:126–128

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell P, Grace A (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15:3622–3639

    PubMed  Google Scholar 

  • Ohl F, Scheich H, Freeman W (2001) Change in pattern of ongoing cortical activity with auditory category learning. Nature 412:733–736

    Article  CAS  PubMed  Google Scholar 

  • Olufsen M, Whittington M, Camperi M, Kopell N (2003) New roles for the gamma rhythm: population tuning and preprocessing for the beta rhythm. Comput Neurosci 14:33–54

    Article  Google Scholar 

  • O’Neill J, Senior T, Allen K, Huxter J, Csicsvari J (2008) Reactivation of experience-dependent cell assembly patterns in hippocampus. Nat Neurosci 11:209–215

    Article  PubMed  CAS  Google Scholar 

  • O’Reilly R (1999) Six principles for biologically-based computational models of cortical cognition. Trends Cogn Sci 2:455–462

    Article  Google Scholar 

  • O’Reilly R, Noelle D, Braver T, Cohen J (2002) Prefrontal cortex and dynamic categorization tasks: representational organization and neuromodulatory control. Cereb Cortex 12:62–101

    Article  Google Scholar 

  • Paller K (1997) Consolidating dispersed neocortical memories: the missing link in amnesia. Memory 5(1/2):73–88

    Article  CAS  PubMed  Google Scholar 

  • Palm G, Sommer F (1995) Associative data storage and retrieval in neural networks. In: Domany E, van Hemmen J, Schulten K (eds) Models of neural networks III. Springer, Berlin

  • Pastalkova E, Itskov V, Amarsingham A, Buzaski G (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322–1327

    Article  CAS  PubMed  Google Scholar 

  • Pasternak T, Greenlee M (2005) Working memory in primate sensory systems. Nat Rev Neurosci 6:97–107

    Article  CAS  PubMed  Google Scholar 

  • Pasupathy A, Connor C (2002) Population coding of shape in area v4. Nat Neurosci 5(12):1332–1338

    Article  CAS  PubMed  Google Scholar 

  • Plate T (1995) Holographic reduced representations. IEEE Trans Neural Netw 6(3):623–641

    Article  CAS  PubMed  Google Scholar 

  • Plenz D, Thiagarajan T (2007) The organizing principles of neuronal avalanches: cell assemblies in the cortex? Trends Neurosci 30(3):101–110

    Article  CAS  PubMed  Google Scholar 

  • Pogio G, Fischer B (1977) Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkeys. J Neurosci 40(6):1392–1405

    Google Scholar 

  • Ponzi A, Wickens J (1977) Input dependent cell assembly dynamics in a model of the striatal medium spiny neuron network. J Neurosci 40(6):1392–1405

    Google Scholar 

  • Procyk E, Tanaka Y, Joseph J (2000) Anterior cingulate activity during routine and non-routine sequential behaviours in macaques. Nat Neurosci 3:502–508

    Article  CAS  PubMed  Google Scholar 

  • Pulvermuller F (1999) Words in the brain’s language. Behav Brain Sci 22:253–336

    Article  CAS  PubMed  Google Scholar 

  • Purushothaman G, Bradley D (2005) Neural population code for fine perceptual decision in area MT. Nat Neurosci 8(1):99–106

    Article  CAS  PubMed  Google Scholar 

  • Qin Y, McNaughton B, Skaggs W, Barnes C (1997) Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos Trans R Soc B 352:1525–1533

    Article  CAS  Google Scholar 

  • Qiu F, von der Heydt R (2005) Figure and ground in the visual cortex: V2 combines stereoscopic cues with gestalt rules. Neuron 47:155–166

    Article  CAS  PubMed  Google Scholar 

  • Quintana J, Fuster J (1999) From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb Cortex 9:213–221

    Article  CAS  PubMed  Google Scholar 

  • Quiroga R, Reddy L, Kreiman G, Koch C, Fried I (2005) Invariant visual representation by single neurons in the human brain. Nature 435:1102–1107

    Article  CAS  PubMed  Google Scholar 

  • Raizada R, Grossberg S (2003) Towards a theory of the laminar architecture of cerebral cortex: computational clues from the visual system. Cereb Cortex 13(1):100–113

    Article  PubMed  Google Scholar 

  • Ranganath C, Cohen M, Brozinsky C (2005) Working memory maintenance contributes to long-term memory formation: neural and behavioral evidence. J Cogn Neurosci 17:994–1010

    Article  PubMed  Google Scholar 

  • Reinagel P, Reid R (2000) Temporal coding of visual information in the thalamus. J Neurosci 20(14):5392–5400

    CAS  PubMed  Google Scholar 

  • Rennaker R, Chen C, Ruyle A, Sloan A, Wilson D (2007) Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J Neurosci 27(7):1534–1542

    Article  CAS  PubMed  Google Scholar 

  • Repa J, Muller J, Apergis J, Desrochers T, Zhou Y, LeDoux J (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4(7):724–731

    Article  CAS  PubMed  Google Scholar 

  • Reynolds G, Richards J (2009) Cortical source localization of infant cognition. Dev Neuropsychol 34(3):312–329

    Article  PubMed  Google Scholar 

  • Riches I, Wilson F, Brown M (1991) The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate. J Neurosci 11(6):1763–1779

    CAS  PubMed  Google Scholar 

  • Riesen A (1947) The development of visual perception in man and chimpanzee. Science 106:107–108

    Article  CAS  PubMed  Google Scholar 

  • Rochester N, Holland J, Haibt L, Duda W (1956) Tests on a cell assembly theory of the action of the brain using a large digital computer. IRE Trans Inf Theory IT 2:80–93

    Google Scholar 

  • Roelfsma P, Engel A, Konig P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157–161

    Article  Google Scholar 

  • Rolls E (2008) Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion. Acta Physiolgica Hungarica 95(2):131–164

    Article  CAS  Google Scholar 

  • Rolls E, Inoue K, Browning A (2003) Activity of primate subgenual cingulate cortex neurons is related to sleep. J Neurophysiol 90:134–142

    Article  PubMed  Google Scholar 

  • Romanski L, Averbeck B, Diltz M (2004) Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurphysiol 93:734–747

    Article  Google Scholar 

  • Sadato N, Pascual-Leone A, Grafman J, Ibanez V, Deiber M, Dold G, Hallett M (1996) Activation of primary visual cortex by braille reading in blind subjects. Nature 380:526–528

    Article  CAS  PubMed  Google Scholar 

  • Sakai K, Miyashita Y (1991) Neural organization for the long-term memory of paired associates. Nature 354:152–155

    Article  CAS  PubMed  Google Scholar 

  • Sakurai Y (1998a) Cell-assembly coding in several memory processes. Neurobiol Learn Mem 70:212–225

    Article  CAS  PubMed  Google Scholar 

  • Sakurai Y (1998b) The search for cell assemblies in the working brain. Behav Brain Res 91:1–13

    Article  CAS  PubMed  Google Scholar 

  • Sakurai Y, Tuakahashi S, Inoue M (2004) Stimulus duration in working memory is represented by neuronal activity in the monkey prefrontal cortex. Eur J Neurosci 20:1069–1080

    Article  PubMed  Google Scholar 

  • Salihoglu U, Bersini H, Yamaguchi Y, Molter C (2009) Online unsupervised formation of cell assemblies for the encoding of multiple cognitive maps. Neural Netw 22:687–696

    Article  PubMed  Google Scholar 

  • Scherberger H, Jarvis M, Anderson R (2005) Cortical local field potential encodes movement intentions in the posterior parietal cortex. Neuron 46:347–354

    Article  CAS  PubMed  Google Scholar 

  • Schoenbaum G (1998) Cell assemblies and the ghost in the machine. In: Eichenbaum H, Davis J (eds) Neuronal ensembles, strategies for recording and decoding, Wiley, New York, pp 81–116

  • Seamans J, Nogueira L, Lavin L (2003) Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures. Cereb Cortex 13:1242–1250

    Article  PubMed  Google Scholar 

  • Setola P, Reilly R (2005) Words in the brain’s language: an experimental investigation. Brain Lang 94:251–259

    Article  PubMed  Google Scholar 

  • Shoham D, Glaser D, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, Grinvald A (1999) Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24:791–802

    Article  CAS  PubMed  Google Scholar 

  • Siegel G, Carter C, Thase M (2006) Use of fmri to predict recovery from unipolar depression with cognitive behavior therapy. Am J Psychiatry 163:735–738

    Article  Google Scholar 

  • Sigala N, Gabbiani F, Logothetis N (2002) Visual categorization and object representation in monkeys and humans. J Cogn Neurosci 14(2):187–198

    Article  CAS  PubMed  Google Scholar 

  • Sigala N, Kusunoki M, Nimmo-Smith I, Gaffan D, Duncan J (2008) Hierarchical coding for sequential task events in the monkey prefrontal cortex. PNAS Neurosci 105:33:11969–11974

    Google Scholar 

  • Silvanto J, Muggleton N (2008) New light through old windows: moving beyond the “virtual lesion” approach to transcranial magnetic stimulation. NeuroImage 39:549–552

    Article  PubMed  Google Scholar 

  • Singer W, Engel A, Kreiter A, Munk M, Neuenschwander S, Roelfsema P (1997) Neuronal assemblies: necessity, signature and detectability. Trends Cogn Sci 1(7):252–261

    Article  CAS  PubMed  Google Scholar 

  • Smith K (2010) Settling the great glia debate. Nature 468:160–162

    Article  CAS  PubMed  Google Scholar 

  • Sougne J (2001) Binding and multiple instantiation in a distributed network of spiking neurons. Connect Sci 13:99–126

    Article  Google Scholar 

  • Stackman R, Taube J (1998) Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J Neurosci 18(21):9020–9037

    CAS  PubMed  Google Scholar 

  • Steriade M, Nunez A, Amzica F (1993) A novel slow (\(<\)1 hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13(8):3252–3265

    CAS  PubMed  Google Scholar 

  • Stern E, Jaeger D, Wilson C (1998) Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 394:475–478

    Article  CAS  PubMed  Google Scholar 

  • Sutherland G, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10:180–186

    Article  CAS  PubMed  Google Scholar 

  • Taddeo M, Floridi L (2005) Solving the symbol grounding problem: a critical review of fifteen years of research. J Exp Theor Artif Intell 17(4):419–445

    Article  Google Scholar 

  • Talk A, Kang E, Gabriel M (2004) Independent generation of theta rhythm in the hippocampus and posterior cingulate cortex. Brain Res 1015:15–24

    Google Scholar 

  • Tark K, Curtis C (2009) Persistent neural actcivity in the human frontal cortex when maintaining space that is off the map. Nat Neurosci 12:1463–1468

    Google Scholar 

  • Terman D, Wang D (1995) Global competition and local cooperation in a network of neural oscillators. Phys D 81:148–176

    Google Scholar 

  • Tudusciuc O, Nieder A (2007) Neuronal population coding of continuous and discrete quantity in the primate posterior parietal cortex. PNAS 104(36):14513–14518

    Google Scholar 

  • Usher M, Donnelly N (1998) Visual synchrony affects binding and segmentation in perception. Nature 394:179–182

    Article  CAS  PubMed  Google Scholar 

  • Valiant L (2005) Memorization and association on a realistic neural model. Neural Comput 17:527–555

    Article  PubMed  Google Scholar 

  • van der Velde F, de Kamps M (2006) Neural blackboard architectures of combinatorial structures in cognition. Behav Brain Sci 29:1–72

    Google Scholar 

  • von der Malsburg C (1981) The correlation theory of brain function. Technical Report, Department of Neurobiology, Max-Planck-Institute for Biophyscial Chemistry

  • Wallace D, Kerr J (2010) Chasing the cell assembly. Curr Opin Neurobiol 20:296–305

    Article  CAS  PubMed  Google Scholar 

  • Wallis J, Anderson K, Miller E (2001) Single neurons in prefrontal cortex encode abstract rules. Nature 411:953–956

    Article  CAS  PubMed  Google Scholar 

  • Wang X (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24(8):455–463

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Markram H, Goodman P, Berger T, Ma J, Goldman-Rakic P (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci 9:534–542

    Article  CAS  PubMed  Google Scholar 

  • Webb S, Long J, Nelson C (2005) A longitudinal investigation of visual event-related potentials in the first year of life. Dev Sci 8(6):605–616

    Article  PubMed  Google Scholar 

  • Wennekers T, Palm G (2000) Cell assemblies, associative memory and temporal structure in brain signals. In: Miller R (ed) Time and the brain: conceptual advances in brain research, vol 2. Harwood Academic Publishers, Switzerland, pp 251–274

  • Wessberg J, Stambaugh C, Kralik J, Beck P, Laubach M, Chapin J, Kim J, Biggs S, Srinivasan M, Nicolelis M (2000) Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408:361–365

    Article  CAS  PubMed  Google Scholar 

  • Wichert A (2001) Pictorial reasoning with cell assemblies. Connect Sci 13(1):1–42

    Article  Google Scholar 

  • Wickelgren W (1999) Webs, cell assemblies, and chunking in neural nets. Can J Exp Psychol 53(1):118–131

    Article  CAS  PubMed  Google Scholar 

  • Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G (1995) Sharp wave-associated high-frequency oscillation (200hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15(1):30–46

    CAS  PubMed  Google Scholar 

  • Yoshida M, Hasselmo M (2009) Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29(15):4945–4952

    Article  CAS  PubMed  Google Scholar 

  • Yuste R, MacLean J, Smith J, Lansner A (2005) The cortex as a central pattern generator. Nat Rev Neurosci 6:477–483

    Article  CAS  PubMed  Google Scholar 

  • Zelano C, Montag J, Khan R, Sobel N (2009) A specialized odor memory buffer in primary olfactory cortex. PLOS One 4(3):e4965

    Google Scholar 

  • Zhou Y, Fuster J (1996) Mnemonic neuronal activity in somatosensory cortex. PNAS 93:10533–10537

    Google Scholar 

  • Zucker R, Regehr W (2002) Short-term synaptic plasticity. Ann Rev Physiol 64:355–405

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by EPSRC Grant EP/D059720. Thanks to Ray Adams, Eric Chown, Dan Diaper, Kailash Nadh and Pieter DeVries for comments on this paper, and Mark Dubin for the use of his Brodmann figures.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian R. Huyck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huyck, C.R., Passmore, P.J. A review of cell assemblies. Biol Cybern 107, 263–288 (2013). https://doi.org/10.1007/s00422-013-0555-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-013-0555-5

Keywords

Navigation