Long-term modification of cortical synapses improves sensory perception

Nature Neuroscience

Volumn 16, Issue 1, 2013, Pages 79-88

  Froemke, Robert C ^a,b,c   Carcea, Ioana ^a,b   Barker, Alison J ^c   Yuan, Kexin ^c   Seybold, Bryan A ^c   Martins, Ana Raquel O ^a,b,d   Zaika, Natalya ^a   Bernstein, Hannah ^a   Wachs, Megan ^e   Levis, Philip A ^e   Polley, Daniel B ^f   Merzenich, Michael M ^c   Schreiner, Christoph E ^c  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e Stanford University   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; FEMALE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; SENSORY STIMULATION; SOUND INTENSITY; SOUND PRESSURE; SYNAPSE; SYNAPTIC TRANSMISSION;

ACOUSTIC STIMULATION; ANESTHETICS; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; BASAL NUCLEUS OF MEYNERT; BIOPHYSICS; BRAIN MAPPING; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; FOOD DEPRIVATION; MODELS, NEUROLOGICAL; NEURONS; NONLINEAR DYNAMICS; PATCH-CLAMP TECHNIQUES; PSYCHOACOUSTICS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); SIGNAL DETECTION, PSYCHOLOGICAL; STATISTICS, NONPARAMETRIC; SYNAPSES;

EID: 84871720798     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3274     Document Type: Article

References (50)

1. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106-154 (1962).
2. Hirsch, J.A. & Martinez, L.M. Circuits that build visual cortical receptive fields. Trends Neurosci. 29, 30-39 (2006).
3. Huberman, A.D., Feller, M.B. & Chapman, B. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 31, 479-509 (2008).
4. Ye, C.Q., Poo, M.M., Dan, Y. & Zhang, X.H. Synaptic mechanisms of direction selectivity in primary auditory cortex. J. Neurosci. 30, 1861-1868 (2010).
5. Frégnac, Y., Shulz, D., Thorpe, S. & Bienenstock, E. A cellular analogue of visual cortical plasticity. Nature 333, 367-370 (1988).
6. Talwar, S.K. & Gerstein, G.L. Reorganization in awake rat auditory cortex by local microstimulation and its effect on frequency-discrimination behavior. J. Neurophysiol. 86, 1555-1572 (2001).
7. Meliza, C.D. & Dan, Y. Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49, 183-189 (2006).
8. Jacob, V., Brasier, D.J., Erchova, I., Feldman, D. & Shulz, D.E. Spike timing-dependent synaptic depression in the in vivo barrel cortex of the rat. J. Neurosci. 27, 1271-1284 (2007).
9. Katz, L.C. & Shatz, C.J. Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138 (1996).
10. Buonomano, D.V. & Merzenich, M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149-186 (1998).
11. Smith, G.B., Heynen, A.J. & Bear, M.F. Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex. Phil. Trans. R. Soc. Lond. B 364, 357-367 (2009).
12. Fritz, J., Shamma, S., Elhilali, M. & Klein, D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat. Neurosci. 6, 1216-1223 (2003).
13. Feldman, D.E. & Brecht, M. Map plasticity in somatosensory cortex. Science 310, 810-815 (2005).
14. Dan, Y. & Poo, M.M. Spike timing-dependent plasticity: from synapse to perception. Physiol. Rev. 86, 1033-1048 (2006).
15. de Villers-Sidani, E., Chang, E.F., Bao, S. & Merzenich, M.M. Critical period window for spectral tuning defined in the primary auditory cortex (A1) of the rat. J. Neurosci. 27, 180-189 (2007).
16. Li, Y., Van Hooser, S.D., Mazurek, M., White, L.E. & Fitzpatrick, D. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456, 952-956 (2008).
17. Dorrn, A.L., Yuan, K., Barker, A.J., Schreiner, C.E. & Froemke, R.C. Developmental sensory experience balances cortical excitation and inhibition. Nature 465, 932-936 (2010).
18. Dahmen, J.C., Hartley, D.E. & King, A.J. Stimulus-timing-dependent plasticity of cortical frequency representation. J. Neurosci. 28, 13629-13639 (2008).
19. Greuel, J.M., Luhmann, H.J. & Singer, W. Pharmacological induction of use-dependent receptive field modifications in the visual cortex. Science 242, 74-77 (1988).
20. Metherate, R. & Ashe, J.H. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 14, 132-143 (1993).
21. Bakin, J.S. & Weinberger, N.M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 93, 11219-11224 (1996).
22. Froemke, R.C., Merzenich, M.M. & Schreiner, C.E. A synaptic memory trace for cortical receptive field plasticity. Nature 450, 425-429 (2007).
23. Goard, M. & Dan, Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12, 1444-1449 (2009).
24. Reed, A. et al. Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70, 121-131 (2011).
25. Fritz, J., Elhilali, M. & Shamma, S. Active listening: task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex. Hear. Res. 206, 159-176 (2005).
26. Shuler, M.G. & Bear, M.F. Reward timing in the primary visual cortex. Science 311, 1606-1609 (2006).
27. Martin, S.J., Grimwood, P.D. & Morris, R.G.M. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711 (2000).
28. Hübener, M. & Bonhoeffer, T. Searching for engrams. Neuron 67, 363-371 (2010).
29. Brown, M., Irvine, D.R. & Park, V.N. Perceptual learning on an auditory frequency discrimination task by cats: association with changes in primary auditory cortex. Cereb. Cortex 14, 952-965 (2004).
30. Edeline, J.-M. & Weinberger, N.M. Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav. Neurosci. 107, 82-103 (1993).
31. McLin, D.E. III, Miasnikov, A.A. & Weinberger, N.M. Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 99, 4002-4007 (2002).
32. Han, Y.K., Köver, H., Insanally, M.N., Semerdijan, J.H. & Bao, S. Early experience impairs perceptual discrimination. Nat. Neurosci. 10, 1191-1197 (2007).
33. Abbott, L.F. & Nelson, S.B. Synaptic plasticity: taming the beast. Nat. Neurosci. 3, 1178-1183 (2000).
34. Toyoizumi, T. & Miller, K.D. Equalization of ocular dominance columns induced by an activity-dependent learning rule and the maturation of inhibition. J. Neurosci. 29, 6514-6525 (2009).
35. Desai, N.S., Cudmore, R.H., Nelson, S.B. & Turrigiano, G.G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat. Neurosci. 5, 783-789 (2002).
36. Royer, S. & Paré, D. Conservation of total synaptic weight through balanced synaptic potentiation and depression. Nature 422, 518-522 (2003).
37. Rumsey, C.C. & Abbott, L.F. Equalization of synaptic efficacy by activity-and timing-dependent synaptic plasticity. J. Neurophysiol. 91, 2273-2280 (2004).
38. Deweese, M.R. & Zador, A.M. Shared and private variability in the auditory cortex. J. Neurophysiol. 92, 1840-1855 (2004).
39. Lee, M.G., Hassani, O.K., Alonso, A. & Jones, B.E. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci. 25, 4365-4369 (2005).
40. Hasselmo, M.E. & Sarter, M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36, 52-73 (2011).
41. Zaborszky, L., Pang, K., Somogyi, J., Nadasdy, Z. & Kallo, I. The basal forebrain corticopetal system revisited. Ann. NY Acad. Sci. 877, 339-367 (1999).
42. Lin, S.C. & Nicolelis, M.A. Neuronal ensemble bursting in the basal forebrain encodes salience irrespective of valence. Neuron 59, 138-149 (2008).
43. Fries, P., Reynolds, J.H., Rorie, A.E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560-1563 (2001).
44. Averbeck, B.B., Latham, P.E. & Pouget, A. Neural correlations, population coding and computation. Nat. Rev. Neurosci. 7, 358-366 (2006).
45. Cohen, M.R. & Maunsell, J.H. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12, 1594-1600 (2009).
46. Elhilali, M., Fritz, J.B., Chi, T.S. & Shamma, S. Auditory cortical receptive fields: stable entities with plastic abilities. J. Neurosci. 27, 10372-10382 (2007).
47. Tanner, W.P. & Swets, J.A. A decision-making theory of visual detection. Psychol. Rev. 61, 401-409 (1954).
48. Liu, R.C. & Schreiner, C.E. Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol. 5, e173 (2007).
49. Polley, D.B., Heiser, M.A., Blake, D.T., Schreiner, C.E. & Merzenich, M.M. Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proc. Natl. Acad. Sci. USA 101, 16351-16356 (2004).
50. Wright, B.A., Sabin, A.T., Zhang, Y., Marrone, N. & Fitzgerald, M.B. Enhancing perceptual learning by combining practice with periods of additional sensory stimulation. J. Neurosci. 30, 12868-12877 (2010).