Advertisement

Biological Cybernetics

, Volume 100, Issue 6, pp 427–446 | Cite as

Neural coding and contextual influences in the whisker system

  • Rasmus S. Petersen
  • Stefano Panzeri
  • Miguel Maravall
Review
First Online:
Received:
Accepted:

Abstract

A fundamental problem in neuroscience, to which Prof. Segundo has made seminal contributions, is to understand how action potentials represent events in the external world. The aim of this paper is to review the issue of neural coding in the context of the rodent whiskers, an increasingly popular model system. Key issues we consider are: the role of spike timing; mechanisms of spike timing; decoding and context-dependence. Significant insight has come from the development of rigorous, information theoretic frameworks for tackling these questions, in conjunction with suitably designed experiments. We review both the theory and experimental studies. In contrast to the classical view that neurons are noisy and unreliable, it is becoming clear that many neurons in the subcortical whisker pathway are remarkably reliable and, by virtue of spike timing with millisecond-precision, have high bandwidth for conveying sensory information. In this way, even small (~200 neuron) subcortical modules are able to support the sensory processing underlying sophisticated whisker-dependent behaviours. Future work on neural coding in cortex will need to consider new findings that responses are highly dependent on context, including behavioural and internal states.

Keywords

Neural coding Barrel cortex Information theory Vibrissa 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adrian ED (1926) The impulses produced by sensory nerve endings: Part I. J Physiol 61: 49–72PubMedGoogle Scholar
  2. Ahissar E, Sosnik R, Haidarliu S (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406: 302–306PubMedCrossRefGoogle Scholar
  3. Ahissar E, Sosnik R, Bagdasarian K, Haidarliu S (2001) Temporal frequency of whisker movement. II. Laminar organization of cortical representations. J Neurophysiol 86: 354–367PubMedGoogle Scholar
  4. Ahrens KF, Kleinfeld D (2004) Current flow in vibrissa motor cortex can phase-lock with exploratory rhythmic whisking in rat. J Neurophysiol 92: 1700–1707PubMedCrossRefGoogle Scholar
  5. Alloway KD (2008) Information processing streams in rodent barrel cortex: the differential functions of barrel and septal circuits. Cereb Cortex 18: 979–989PubMedCrossRefGoogle Scholar
  6. Alonso JM (2006) Neuroscience. Neurons find strength through synchrony in the brain. Science 312: 1604–1605PubMedCrossRefGoogle Scholar
  7. Andermann ML, Ritt J, Neimark MA, Moore CI (2004) Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high-frequency stimuli. Neuron 42: 451–463PubMedCrossRefGoogle Scholar
  8. Anderson JS, Lampl I, Gillespie DC, Ferster D (2000) The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290: 1968–1972PubMedCrossRefGoogle Scholar
  9. Arabzadeh E, Petersen RS, Diamond ME (2003) Encoding of whisker vibration by rat barrel cortex neurons: implications for texture discrimination. J Neurosci 23: 9146–9154PubMedGoogle Scholar
  10. Arabzadeh E, Panzeri S, Diamond ME (2004) Whisker vibration information carried by rat barrel cortex neurons. J Neurosci 24: 6011–6020PubMedCrossRefGoogle Scholar
  11. Arabzadeh E, Zorzin E, Diamond ME (2005) Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol 3: e17PubMedCrossRefGoogle Scholar
  12. Arabzadeh E, Panzeri S, Diamond ME (2006) Deciphering the spike train of a sensory neuron: counts and temporal patterns in the rat whisker pathway. J Neurosci 26: 9216–9226PubMedCrossRefGoogle Scholar
  13. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273: 1868–1871PubMedCrossRefGoogle Scholar
  14. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21: 1133–1145PubMedCrossRefGoogle Scholar
  15. Axmacher N, Miles R (2004) Intrinsic cellular currents and the temporal precision of EPSP-action potential coupling in CA1 pyramidal cells. J Physiol 555: 713–725PubMedCrossRefGoogle Scholar
  16. Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209–2223PubMedGoogle Scholar
  17. Azouz R, Gray CM (2000) Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc Natl Acad Sci USA 97: 8110–8115PubMedCrossRefGoogle Scholar
  18. Beierlein M, Fall CP, Rinzel J, Yuste R (2002) Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate. J Neurosci 22: 9885–9894PubMedGoogle Scholar
  19. Belford GR, Killackey HP (1979) Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 183: 305–321PubMedCrossRefGoogle Scholar
  20. Bermejo R, Harvey M, Gao P, Zeigler HP (1996) Conditioned whisking in the rat. Somatosens Mot Res 13: 225–233PubMedCrossRefGoogle Scholar
  21. Bermejo R, Houben D, Zeigler HP (1998) Optoelectronic monitoring of individual whisker movements in rats. J Neurosci Methods 83: 89–96PubMedCrossRefGoogle Scholar
  22. Bermejo R, Szwed M, Friedman W, Ahissar E, Zeigler HP (2004) One whisker whisking: unit recording during conditioned whisking in rats. Somatosens Mot Res 21: 183–187PubMedCrossRefGoogle Scholar
  23. Bezdudnaya T, Keller A (2008) Laterodorsal nucleus of the thalamus: A processor of somatosensory inputs. J Comp Neurol 507: 1979–1989PubMedCrossRefGoogle Scholar
  24. Bialek W, Rieke F, de van Ruyter Steveninck RR, Warland D (1991) Reading a neural code. Science 252: 1854–1857PubMedCrossRefGoogle Scholar
  25. Brecht M (2007) Barrel cortex and whisker-mediated behaviors. Curr Opin Neurobiol 17: 408–416PubMedCrossRefGoogle Scholar
  26. Brecht M, Sakmann B (2002) Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction. J Physiol 538: 495–515PubMedCrossRefGoogle Scholar
  27. Brumberg JC, Pinto DJ, Simons DJ (1996) Spatial gradients and inhibitory summation in the rat whisker barrel system. J Neurophysiol 76: 130–140PubMedGoogle Scholar
  28. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312: 1622–1627PubMedCrossRefGoogle Scholar
  29. Bryant HL, Segundo JP (1976) Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260: 279–314PubMedGoogle Scholar
  30. Bullock TH (1993) Integrative systems research on the brain: resurgence and new opportunities. Annu Rev Neurosci 16: 1–15PubMedCrossRefGoogle Scholar
  31. Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638–2648PubMedGoogle Scholar
  32. Carvell GE, Simons DJ (1995) Task- and subject-related differences in sensorimotor behavior during active touch. Somatosens Mot Res 12: 1–9PubMedCrossRefGoogle Scholar
  33. Castro-Alamancos MA (2002a) Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. J Physiol 539: 567–578PubMedCrossRefGoogle Scholar
  34. Castro-Alamancos MA (2002b) Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J Neurophysiol 87: 946–953PubMedGoogle Scholar
  35. Castro-Alamancos MA (2002c) Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J Neurosci 22: 9651–9655PubMedGoogle Scholar
  36. Castro-Alamancos MA (2004) Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41: 455–464PubMedCrossRefGoogle Scholar
  37. Castro-Alamancos MA, Oldford E (2002) Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J Physiol 541: 319–331PubMedCrossRefGoogle Scholar
  38. Chapin JK, Woodward DJ (1981) Modulation of sensory responsiveness of single somatosensory cortical cells during movement and arousal behaviors. Exp Neurol 72: 164–178PubMedCrossRefGoogle Scholar
  39. Chapin JK, Woodward DJ (1982) Somatic sensory transmission to the cortex during movement: gating of single cell responses to touch. Exp Neurol 78: 654–669PubMedCrossRefGoogle Scholar
  40. Chung S, Li X, Nelson SB (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34: 437–446PubMedCrossRefGoogle Scholar
  41. Cover TM, Thomas JA (1991) Elements of information theory. Wiley, New YorkCrossRefGoogle Scholar
  42. Crochet S, Petersen CC (2006) Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat Neurosci 9: 608–610PubMedCrossRefGoogle Scholar
  43. de Ruyter van Steveninck RR, Lewen GD, Strong SP, Koberle R, Bialek W (1997) Reproducibility and variability in neural spike trains. Science 275: 1805–1808PubMedCrossRefGoogle Scholar
  44. Derdikman D, Yu C, Haidarliu S, Bagdasarian K, Arieli A, Ahissar E (2006) Layer-specific touch-dependent facilitation and depression in the somatosensory cortex during active whisking. J Neurosci 26: 9538–9547PubMedCrossRefGoogle Scholar
  45. Deschenes M, Timofeeva E, Lavallee P (2003) The relay of high- frequency sensory signals in the Whisker-to-barreloid pathway. J Neurosci 23: 6778–6787PubMedGoogle Scholar
  46. Deweese MR, Zador AM (2004) Shared and private variability in the auditory cortex. J Neurophysiol 92: 1840–1855PubMedCrossRefGoogle Scholar
  47. Diamond ME, Armstrong-James M, Budway MJ, Ebner FF (1992a) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J Comp Neurol 319: 66–84PubMedCrossRefGoogle Scholar
  48. Diamond ME, Armstrong-James M, Ebner FF (1992b) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus. J Comp Neurol 318: 462–476PubMedCrossRefGoogle Scholar
  49. Diamond ME, von Heimendahl M, Arabzadeh E (2008a) Whisker-mediated texture discrimination. PLoS Biol 6: e220PubMedCrossRefGoogle Scholar
  50. Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E (2008b) ‘Where’ and ‘what’ in the whisker sensorimotor system. Nat Rev Neurosci 9: 601–612PubMedCrossRefGoogle Scholar
  51. Diaz-Quesada M, Maravall M (2008) Intrinsic mechanisms for adaptive gain rescaling in barrel cortex. J Neurosci 28: 696–710PubMedCrossRefGoogle Scholar
  52. Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269: 981–985PubMedCrossRefGoogle Scholar
  53. Drew PJ, Feldman DE (2007) Representation of moving wavefronts of whisker deflection in rat somatosensory cortex. J Neurophysiol 98: 1566–1580PubMedCrossRefGoogle Scholar
  54. Ego-Stengel V, Melloe Souza T, Jacob V, Shulz DE (2005) Spatiotemporal characteristics of neuronal sensory integration in the barrel cortex of the rat. J Neurophysiol 93: 1450–1467PubMedCrossRefGoogle Scholar
  55. Erchova IA, Lebedev MA, Diamond ME (2002) Somatosensory cortical neuronal population activity across states of anaesthesia. Eur J Neurosci 15: 744–752PubMedCrossRefGoogle Scholar
  56. Erchova IA, Petersen RS, Diamond ME (2003) Effect of developmental sensory and motor deprivation on the functional organization of adult rat somatosensory cortex. Brain Res Bull 60: 373–386PubMedGoogle Scholar
  57. Fanselow EE, Nicolelis MA (1999) Behavioral modulation of tactile responses in the rat somatosensory system. J Neurosci 19: 7603–7616PubMedGoogle Scholar
  58. Fee MS, Mitra PP, Kleinfeld D (1997) Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J Neurophysiol 78: 1144–1149PubMedGoogle Scholar
  59. Ferezou I, Bolea S, Petersen CC (2006) Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50: 617–629PubMedCrossRefGoogle Scholar
  60. Foffani G, Tutunculer B, Moxon KA (2004) Role of spike timing in the forelimb somatosensory cortex of the rat. J Neurosci 24: 7266–7271PubMedCrossRefGoogle Scholar
  61. Fraser G, Hartings JA, Simons DJ (2006) Adaptation of trigeminal ganglion cells to periodic whisker deflections. Somatosens Mot Res 23: 111–118PubMedCrossRefGoogle Scholar
  62. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48: 315–327PubMedCrossRefGoogle Scholar
  63. Ganguly K, Kleinfeld D (2004) Goal-directed whisking increases phase-locking between vibrissa movement and electrical activity in primary sensory cortex in rat. Proc Natl Acad Sci USA 101: 12348–12353PubMedCrossRefGoogle Scholar
  64. Garabedian CE, Jones SR, Merzenich MM, Dale A, Moore CI (2003) Band-pass response properties of rat SI neurons. J Neurophysiol 90: 1379–1391PubMedCrossRefGoogle Scholar
  65. Garcia-Lazaro JA, Ho SS, Nair A, Schnupp JW (2007) Shifting and scaling adaptation to dynamic stimuli in somatosensory cortex. Eur J Neurosci 26: 2359–2368PubMedCrossRefGoogle Scholar
  66. Ghazanfar AA, Nicolelis MA (1997) Nonlinear processing of tactile information in the thalamocortical loop. J Neurophysiol 78: 506–510PubMedGoogle Scholar
  67. Gibson JM, Welker WI (1983) Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 1. Receptive field properties and threshold distributions. Somatosens Res 1: 51–67PubMedGoogle Scholar
  68. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23: 385–397PubMedCrossRefGoogle Scholar
  69. Goldreich D, Peterson BE, Merzenich MM (1998) Optical imaging and electrophysiology of rat barrel cortex. II. Responses to paired-vibrissa deflections. Cereb Cortex 8: 184–192PubMedCrossRefGoogle Scholar
  70. Gollisch T, Meister M (2008) Rapid neural coding in the retina with relative spike latencies. Science 319: 1108–1111PubMedCrossRefGoogle Scholar
  71. Guic-Robles E, Valdivieso C, Guajardo G (1989) Rats can learn a roughness discrimination using only their vibrissal system. Behav Brain Res 31: 285–289PubMedCrossRefGoogle Scholar
  72. Gutkin B, Ermentrout GB, Rudolph M (2003) Spike generating dynamics and the conditions for spike-time precision in cortical neurons. J Comput Neurosci 15: 91–103PubMedCrossRefGoogle Scholar
  73. Hartmann MJ, Johnson NJ, Towal RB, Assad C (2003) Mechanical characteristics of rat vibrissae: resonant frequencies and damping in isolated whiskers and in the awake behaving animal. J Neurosci 23: 6510–6519PubMedGoogle Scholar
  74. Harvey MA, Bermejo R, Zeigler HP (2001) Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks. Somatosens Mot Res 18: 211–222PubMedCrossRefGoogle Scholar
  75. Hasenstaub A, Sachdev RN, McCormick DA (2007) State changes rapidly modulate cortical neuronal responsiveness. J Neurosci 27: 9607–9622PubMedCrossRefGoogle Scholar
  76. Heil P (2004) First-spike latency of auditory neurons revisited. Curr Opin Neurobiol 14: 461–467PubMedCrossRefGoogle Scholar
  77. Hentschke H, Haiss F, Schwarz C (2006) Central signals rapidly switch tactile processing in rat barrel cortex during whisker movements. Cereb Cortex 16: 1142–1156PubMedCrossRefGoogle Scholar
  78. Higley MJ, Contreras D (2003) Nonlinear integration of sensory responses in the rat barrel cortex: an intracellular study in vivo. J Neurosci 23: 10190–10200PubMedGoogle Scholar
  79. Hipp J, Arabzadeh E, Zorzin E, Conradt J, Kayser C, Diamond ME, Konig P (2006) Texture signals in whisker vibrations. J Neurophysiol 95: 1792–1799PubMedCrossRefGoogle Scholar
  80. Hopfield JJ (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376: 33–36PubMedCrossRefGoogle Scholar
  81. Houweling AR, Brecht M (2008) Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451: 65–68PubMedCrossRefGoogle Scholar
  82. Huber D, Petreanu L, Ghitani N, Ranade S, Hromadka T, Mainen Z, Svoboda K (2008) Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451: 61–64PubMedCrossRefGoogle Scholar
  83. Huxter J, Burgess N, O’Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425: 828–832PubMedCrossRefGoogle Scholar
  84. Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7: 170–177PubMedCrossRefGoogle Scholar
  85. Jones LM, Depireux DA, Simons DJ, Keller A (2004a) Robust temporal coding in the trigeminal system. Science 304: 1986–1989PubMedCrossRefGoogle Scholar
  86. Jones LM, Lee S, Trageser JC, Simons DJ, Keller A (2004b) Precise temporal responses in whisker trigeminal neurons. J Neurophysiol 92: 665–668PubMedCrossRefGoogle Scholar
  87. Katz Y, Heiss JE, Lampl I (2006) Cross-whisker adaptation of neurons in the rat barrel cortex. J Neurosci 26: 13363–13372PubMedCrossRefGoogle Scholar
  88. Khatri V, Simons DJ (2007) Angularly nonspecific response suppression in rat barrel cortex. Cereb Cortex 17: 599–609PubMedCrossRefGoogle Scholar
  89. Khatri V, Hartings JA, Simons DJ (2004) Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. J Neurophysiol 92: 3244–3254PubMedCrossRefGoogle Scholar
  90. Kida H, Shimegi S, Sato H (2005) Similarity of direction tuning among responses to stimulation of different whiskers in neurons of rat barrel cortex. J Neurophysiol 94: 2004–2018PubMedCrossRefGoogle Scholar
  91. Kleinfeld D, Ahissar E, Diamond ME (2006) Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol 16: 435–444PubMedCrossRefGoogle Scholar
  92. Krupa DJ, Matell MS, Brisben AJ, Oliveira LM, Nicolelis MA (2001) Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci 21: 5752–5763PubMedGoogle Scholar
  93. Lak A, Arabzadeh E, Diamond ME (2008) Enhanced response of neurons in rat somatosensory cortex to stimuli containing temporal noise. Cereb Cortex 18: 1085–1093PubMedCrossRefGoogle Scholar
  94. Lampl I, Reichova I, Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22: 361–374PubMedCrossRefGoogle Scholar
  95. Land MF, Collett TS (1974) Chasing Behavior of Houseflies (Fannia-Canicularis)—Description and Analysis. J Comp Physiol 89: 331–357CrossRefGoogle Scholar
  96. Land PW, Simons DJ (1985) Metabolic and structural correlates of the vibrissae representation in the thalamus of the adult rat. Neurosci Lett 60: 319–324PubMedCrossRefGoogle Scholar
  97. Latham PE, Nirenberg S (2005) Synergy, redundancy, and independence in population codes, revisited. J Neurosci 25: 5195–5206PubMedCrossRefGoogle Scholar
  98. Lee KJ, Woolsey TA (1975) A proportional relationship between peripheral innervation density and cortical neuron number in the somatosensory system of the mouse. Brain Res 99: 349–353PubMedCrossRefGoogle Scholar
  99. Leiser SC, Moxon KA (2006) Relationship between physiological response type (RA and SA) and vibrissal receptive field of neurons within the rat trigeminal ganglion. J Neurophysiol 95: 3129–3145PubMedCrossRefGoogle Scholar
  100. Luna R, Hernandez A, Brody CD, Romo R (2005) Neural codes for perceptual discrimination in primary somatosensory cortex. Nat Neurosci 8: 1210–1219PubMedCrossRefGoogle Scholar
  101. MacKay D, McCulloch WS (1952) The limiting information capacity of a neuronal link. Bull Math Biophys 14: 127–135CrossRefGoogle Scholar
  102. MacLean JN, Watson BO, Aaron GB, Yuste R (2005) Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48: 811–823PubMedCrossRefGoogle Scholar
  103. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268: 1503–1506PubMedCrossRefGoogle Scholar
  104. Maravall M, Petersen RS, Fairhall AL, Arabzadeh E, Diamond ME (2007) Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biol 5: e19PubMedCrossRefGoogle Scholar
  105. Masri R, Bezdudnaya T, Trageser JC, Keller A (2008) Encoding of stimulus frequency and sensor motion in the posterior medial thalamic nucleus. J Neurophysiol 100: 681–689PubMedCrossRefGoogle Scholar
  106. Melzer P, Champney GC, Maguire MJ, Ebner FF (2006) Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex. Exp Brain Res 172: 370–386PubMedCrossRefGoogle Scholar
  107. Merhav N, Kaplan G, Lapidoth A, Shamai S (1994) On Information Rates for Mismatched Decoders. IEEE T Inform Theory 40: 1953–1967CrossRefGoogle Scholar
  108. Mirabella G, Battiston S, Diamond ME (2001) Integration of multiple-whisker inputs in rat somatosensory cortex. Cereb Cortex 11: 164–170PubMedCrossRefGoogle Scholar
  109. Montemurro MA, Panzeri S, Maravall M, Alenda A, Bale MR, Brambilla M, Petersen RS (2007a) Role of precise spike timing in coding of dynamic vibrissa stimuli in somatosensory thalamus. J Neurophysiol 98: 1871–1882PubMedCrossRefGoogle Scholar
  110. Montemurro MA, Senatore R, Panzeri S (2007b) Tight data-robust bounds to mutual information combining shuffling and model selection techniques. Neural Comput 19: 2913–2957PubMedCrossRefGoogle Scholar
  111. Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S (2008) Phase-of-firing coding of natural visual stimuli in primary visual cortex. Curr Biol 18: 375–380PubMedCrossRefGoogle Scholar
  112. Moore CI, Nelson SB (1998) Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol 80: 2882–2892PubMedGoogle Scholar
  113. Moore GP, Perkel DH, Segundo JP (1966) Statistical analysis and functional interpretation of neuronal spike data. Annu Rev Physiol 28: 493–522PubMedCrossRefGoogle Scholar
  114. Neimark MA, Andermann ML, Hopfield JJ, Moore CI (2003) Vibrissa resonance as a transduction mechanism for tactile encoding. J Neurosci 23: 6499–6509PubMedGoogle Scholar
  115. Panzeri S, Schultz SR (2001) A unified approach to the study of temporal, correlational, and rate coding. Neural Comput 13: 1311–1349PubMedCrossRefGoogle Scholar
  116. Panzeri S, Petersen RS, Schultz SR, Lebedev M, Diamond ME (2001) The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29: 769–777PubMedCrossRefGoogle Scholar
  117. Panzeri S, Pola G, Petersen RS (2003) Coding of sensory signals by neuronal populations: the role of correlated activity. Neuroscientist 9: 175–180PubMedCrossRefGoogle Scholar
  118. Panzeri S, Senatore R, Montemurro MA, Petersen RS (2007) Correcting for the sampling bias problem in spike train information measures. J Neurophysiol 98: 1064–1072PubMedCrossRefGoogle Scholar
  119. Peters A, Payne BR (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3: 69–78PubMedCrossRefGoogle Scholar
  120. Petersen CC (2007) The functional organization of the barrel cortex. Neuron 56: 339–355PubMedCrossRefGoogle Scholar
  121. Petersen RS, Diamond ME (2000) Spatial-temporal distribution of whisker-evoked activity in rat somatosensory cortex and the coding of stimulus location. J Neurosci 20: 6135–6143PubMedGoogle Scholar
  122. Petersen RS, Panzeri S (2003) A case study of population coding: stimulus localisation in the barrel cortex. In: Feng J (eds) Computational neuroscience: a comprehensive approach. CRC Press, West Palm BeachGoogle Scholar
  123. Petersen RS, Panzeri S, Diamond ME (2001) Population coding of stimulus location in rat somatosensory cortex. Neuron 32: 503–514PubMedCrossRefGoogle Scholar
  124. Petersen RS, Panzeri S, Diamond ME (2002) The role of individual spikes and spike patterns in population coding of stimulus location in rat somatosensory cortex. Biosystems 67: 187–193PubMedCrossRefGoogle Scholar
  125. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100: 13638–13643PubMedCrossRefGoogle Scholar
  126. Petersen RS, Brambilla M, Bale MR, Alenda A, Panzeri S, Montemurro MA, Maravall M (2008) Diverse and temporally precise kinetic feature selectivity in the VPm thalamic nucleus. Neuron 60: 890–903PubMedCrossRefGoogle Scholar
  127. Pierret T, Lavallee P, Deschenes M (2000) Parallel streams for the relay of vibrissal information through thalamic barreloids. J Neurosci 20: 7455–7462PubMedGoogle Scholar
  128. Pinto DJ, Brumberg JC, Simons DJ (2000) Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83: 1158–1166PubMedGoogle Scholar
  129. Puccini GD, Compte A, Maravall M (2006) Stimulus dependence of barrel cortex directional selectivity. PLoS ONE 1: e137PubMedCrossRefGoogle Scholar
  130. Reig R, Sanchez-Vives MV (2007) Synaptic transmission and plasticity in an active cortical network. PLoS ONE 2: e670PubMedCrossRefGoogle Scholar
  131. Reig R, Gallego R, Nowak LG, Sanchez-Vives MV (2006) Impact of cortical network activity on short-term synaptic depression. Cereb Cortex 16: 688–695PubMedCrossRefGoogle Scholar
  132. Rice FL, Munger BL (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. II. The common fur between the vibrissae. J Comp Neurol 252: 186–205PubMedCrossRefGoogle Scholar
  133. Rice FL, Mance A, Munger BL (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle-sinus complexes. J Comp Neurol 252: 154–174PubMedCrossRefGoogle Scholar
  134. Rieke F, Warland DK, de van Ruyter Steveninck RR, Bialek W (1997) Spikes: exploring the neural code. MIT Press, CambridgeGoogle Scholar
  135. Ritt JT, Andermann ML, Moore CI (2008) Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats. Neuron 57: 599–613PubMedCrossRefGoogle Scholar
  136. Sachdev RN, Ebner FF, Wilson CJ (2004) Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. J Neurophysiol 92: 3511–3521PubMedCrossRefGoogle Scholar
  137. Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr Opin Neurobiol 4: 569–579PubMedCrossRefGoogle Scholar
  138. Shimegi S, Ichikawa T, Akasaki T, Sato H (1999) Temporal characteristics of response integration evoked by multiple whisker stimulations in the barrel cortex of rats. J Neurosci 19: 10164–10175PubMedGoogle Scholar
  139. Shimegi S, Akasaki T, Ichikawa T, Sato H (2000) Physiological and anatomical organization of multiwhisker response interactions in the barrel cortex of rats. J Neurosci 20: 6241–6248PubMedGoogle Scholar
  140. Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41: 798–820PubMedGoogle Scholar
  141. Simons DJ (1985) Temporal and spatial integration in the rat SI vibrissa cortex. J Neurophysiol 54: 615–635PubMedGoogle Scholar
  142. Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61: 311–330PubMedGoogle Scholar
  143. Sosnik R, Haidarliu S, Ahissar E (2001) Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. J Neurophysiol 86: 339–353PubMedGoogle Scholar
  144. Strong SP, Koberle R, de Ruyter van Steveninck R, Bialek W (1998) Entropy and information in neural spike trains. Phys Rev Lett 80: 197–200CrossRefGoogle Scholar
  145. Stuttgen MC, Ruter J, Schwarz C (2006) Two psychophysical channels of whisker deflection in rats align with two neuronal classes of primary afferents. J Neurosci 26: 7933–7941PubMedCrossRefGoogle Scholar
  146. Szwed M, Bagdasarian K, Ahissar E (2003) Encoding of vibrissal active touch. Neuron 40: 621–630PubMedCrossRefGoogle Scholar
  147. Tolhurst DJ, Movshon JA, Dean AF (1983) The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23: 775–785PubMedCrossRefGoogle Scholar
  148. Trageser JC, Keller A (2004) Reducing the uncertainty: gating of peripheral inputs by zona incerta. J Neurosci 24: 8911–8915PubMedCrossRefGoogle Scholar
  149. Urbain N, Deschenes M (2007) A new thalamic pathway of vibrissal information modulated by the motor cortex. J Neurosci 27: 12407–12412PubMedCrossRefGoogle Scholar
  150. van der Loos H (1976) Barreloids in mouse somatosensory thalamus. Neurosci Lett 2: 1–6CrossRefGoogle Scholar
  151. Van Rullen R, Thorpe SJ (2001) Rate coding versus temporal order coding: what the retinal ganglion cells tell the visual cortex. Neural Comput 13: 1255–1283PubMedCrossRefGoogle Scholar
  152. von Heimendahl M, Itskov PM, Arabzadeh E, Diamond ME (2007) Neuronal activity in rat barrel cortex underlying texture discrimination. PLoS Biol 5: e305CrossRefGoogle Scholar
  153. Wark B, Lundstrom BN, Fairhall A (2007) Sensory adaptation. Curr Opin Neurobiol 17: 423–429PubMedCrossRefGoogle Scholar
  154. Webber RM, Stanley GB (2004) Nonlinear encoding of tactile patterns in the barrel cortex. J Neurophysiol 91: 2010–2022PubMedCrossRefGoogle Scholar
  155. Webber RM, Stanley GB (2006) Transient and steady-state dynamics of cortical adaptation. J Neurophysiol 95: 2923–2932PubMedCrossRefGoogle Scholar
  156. Welker E, Van der Loos H (1986) Quantitative correlation between barrel-field size and the sensory innervation of the whiskerpad: a comparative study in six strains of mice bred for different patterns of mystacial vibrissae. J Neurosci 6: 3355–3373PubMedGoogle Scholar
  157. Wilent WB, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8: 1364–1370PubMedCrossRefGoogle Scholar
  158. Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17: 205–242PubMedCrossRefGoogle Scholar
  159. Yang Y, DeWeese MR, Otazu GH, Zador AM (2008) Millisecond-scale differences in neural activity in auditory cortex can drive decisions. Nat Neurosci 11: 1262–1263PubMedCrossRefGoogle Scholar
  160. Zucker E, Welker WI (1969) Coding of somatic sensory input by vibrissae neurons in the rat’s trigeminal ganglion. Brain Res 12: 138–156PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Rasmus S. Petersen
    • 1
  • Stefano Panzeri
    • 1
    • 2
  • Miguel Maravall
    • 3
  1. 1.Faculty of Life SciencesUniversity of ManchesterManchesterUK
  2. 2.Robotics, Brain and Cognitive Sciences DepartmentItalian Institute of TechnologyGenoaItaly
  3. 3.Instituto de Neurociencias de Alicante UMH-CSICSant Joan d’AlacantSpain

Personalised recommendations

Cite article

Buy options