Biological Cybernetics

, Volume 97, Issue 4, pp 269–277

The role of cortical feedback in the generation of the temporal receptive field responses of lateral geniculate nucleus neurons: a computational modelling study

Original Paper

Abstract

The influence of cortical feedback on thalamic visual responses has been a source of much discussion in recent years. In this study we examine the possible role of cortical feedback in shaping the spatiotemporal receptive field (STRF) responses of thalamocortical (TC) cells in the lateral geniculate nucleus (LGN) of the thalamus. A population-based computational model of the thalamocortical network is used to generate a representation of the STRF response of LGN TC cells within the corticothalamic feedback circuit. The cortical feedback is shown to have little influence on the spatial response properties of the STRF organization. However, the model suggests that cortical feedback may play a key role in modifying the experimentally observed biphasic temporal response property of the STRF, that is, the reversal over time of the polarity of ON and OFF responses of the centre and surround of the receptive field, in particular accounting for the experimentally observed mismatch between retinal cells and TC cells in respect of the magnitude of the second (rebound) phase of the temporal response. The model results also show that this mismatch may result from an anti-phase corticothalamic feedback mechanism.

Keywords

Corticothalamic feedback Spatiotemporal receptive fields Lateral geniculate nulceus Computational modelling Wilson and cowan equations 

Abbreviations

LGN

Lateral geniculate nucleus

PY

Cortical pyramidal cell

RE

Reticular cell

RE nucleus

Thalamic reticular nucleus

RF

Receptive field

RGC

Retinal ganglion cell

STRF

Spatiotemporal receptive field

TC

Thalamocortical cell

V1

Primary visual cortex

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams NC, Lozsádi DA, Guillery RW (1997) Complexities in the thalamocortical and corticothalamic pathways. Eur J Neurosci 9(2):204–209PubMedCrossRefGoogle Scholar
  2. Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84(2):909–926PubMedGoogle Scholar
  3. Atick JJ, Redlich AN (1990) Towards a theory of early visual processing. Neural Comput 2:308–320CrossRefGoogle Scholar
  4. Bal T, Debay D, Destexhe A (2000) Cortical feedback controls the frequency and synchrony of oscillations in the visual thalamus. J Neurosci 20(19):7478–7488PubMedGoogle Scholar
  5. Bickle J, Bernstein M, Heatley M, Worley C, Stiehl S (1999) A functional hypothesis for LGN-V1-TRN connectivities suggested by computer simulation. J Comput Neurosci 6(3):251–261PubMedCrossRefGoogle Scholar
  6. Cai D, DeAngelis GC, Freeman RD (1997) Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. J Neurophysiol 78(2):1045–1061PubMedGoogle Scholar
  7. Castro-Alamancos MA, Calcagnotto ME (2001) High-pass filtering of corticothalamic activity by neuromodulators released in the thalamus during arousal: in vitro and in vivo. J Neurophysiol 85(4):1489–1497PubMedGoogle Scholar
  8. Contreras D, Curro Dossi R, Steriade M (1993) Electrophysiological properties of cat reticular thalamic neurones in vivo. J Physiol 470:273–294PubMedGoogle Scholar
  9. Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81(14):4586–4590PubMedCrossRefGoogle Scholar
  10. Dan Y, Atick J, Reid R (1996) Efficient coding of natural scenes in the lateral geniculate nucleus: experimental test of a computational theory. J Neurosci 16:3351–3362PubMedGoogle Scholar
  11. DeAngelis GC, Ohzawa I, Freeman RD (1993) Spatiotemporal organization of simple-cell receptive fields in the cat’s striate cortex. II. Linearity of temporal and spatial summation. J Neurophysiol 69(4):1118–1135PubMedGoogle Scholar
  12. DeAngelis GC, Ohzawa I, Freeman RD (1995) Receptive-field dynamics in the central visual pathways. Trends Neurosci 18(10):451–458PubMedCrossRefGoogle Scholar
  13. DeAngelis GC, Ghose GM, Ohzawa I, Freeman RD (1999) Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons. J Neurosci 19(10):4046–4064PubMedGoogle Scholar
  14. Denham MJ, Borisyuk RM (2000) A model of theta rhythm production in the septal-hippocampal system and its modulation by ascending brain stem pathways. Hippocampus 10(6):698–716PubMedCrossRefGoogle Scholar
  15. Destexhe A (1999) Can GABAA conductances explain the fast oscillation frequency of absence seizures in rodents?. Eur J Neurosc 11(6):2175–2181CrossRefGoogle Scholar
  16. Destexhe A, Contreras D, Steriade M (1998) Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol 79(2): 999–1016PubMedGoogle Scholar
  17. DiCarlo JJ, Johnson KO (2000) Spatial and temporal structure of receptive fields in primate somatosensory area 3b: effects of stimulus scanning direction and orientation. J Neurosci 20(1): 495–510PubMedGoogle Scholar
  18. Dong D, Atick J (1995) Temporal decorrelation: a theory of lagged and nonlagged responses in the lateral geniculate nucleus. Network 6:159–178CrossRefGoogle Scholar
  19. Gentet LJ, Ulrich D (2003) Strong, reliable and precise synaptic connections between thalamic relay cells and neurones of the nucleus reticularis in juvenile rats. J Physiol 546(3):801–811PubMedCrossRefGoogle Scholar
  20. Gilbert CD, Kelly JP (1975) The projections of cells in different layers of the cat’s visual cortex. J Comp Neurol 163(1):81–105PubMedCrossRefGoogle Scholar
  21. Ghazanfar AA, Nicolelis MA (2001) The structure and function of dynamic cortical and thalamic receptive fields. Cerebral Cortex 11(3):183–193PubMedCrossRefGoogle Scholar
  22. Golomb D, Kleinfeld D, Reid RC, Shapley RM, Shraiman BI (1994) On temporal codes and the spatiotemporal response of neurons in the lateral geniculate nucleus. J Neurophysiol 72(6):2990–3003PubMedGoogle Scholar
  23. Hayot F, Tranchina D (2001) Modeling corticofugal feedback and the sensitivity of lateral geniculate neurons to orientation discontinuity. Vis Neurosci 18(6):865–877PubMedGoogle Scholar
  24. Hirsch JA, Gallagher CA, Alonso JM, Martinez LM (1998) Ascending projections of simple and complex cells in layer 6 of the cat striate cortex. J Neurosci 18(19):8086–8094PubMedGoogle Scholar
  25. Hirsch JA, Martinez LM, Alonso M, Desai K, Pillai C, Pierre C (2002) Synaptic physiology of the flow of information in the cat’s visual cortex in vivo. J Physiol 540(1):335–350PubMedCrossRefGoogle Scholar
  26. Hubel D, Wiesel T (1961) Integrative action in the cat’s lateral geniculate body. J Physiol 155:385–398PubMedGoogle Scholar
  27. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154PubMedGoogle Scholar
  28. Huertas MA, Groff JR, Smith GD (2005) Feedback inhibition and throughput properties of an integrate-and-fire-or-burst network model of retinogeniculate transmission. J Computat Neurosci 19(2):147–80CrossRefGoogle Scholar
  29. Kirkland KL, Sillito AM, Jones HE, West DC, Gerstein GL (2000) Oscillations and long-lasting correlations in a model of the lateral geniculate nucleus and visual cortex. J Neurophysiol 84(4):1863–1868PubMedGoogle Scholar
  30. Landisman CE, Connors BW (2007) VPM and PoM nuclei of the rat somatosensory thalamus: intrinsic neuronal properties and corticothalamic feedback. Cerebr Cortex Advance Access published on 26 March 2007Google Scholar
  31. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW (2002) Electrical synapses in the thalamic reticular nucleus. J Neurosci 22(3):1002–1009PubMedGoogle Scholar
  32. Le Masson G, Renaud-Le Masson S, Debay D, Bal T (2002) Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 417(6891):854–858PubMedCrossRefGoogle Scholar
  33. Lesica NA, Stanley GB (2004) Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. J Neurosci 24:10731–10740PubMedCrossRefGoogle Scholar
  34. Liu XB, Jones EG (1999) Predominance of corticothalamic synaptic inputs to thalamic reticular nucleus neurons in the rat. J Comp Neurol 414(1):67–79PubMedCrossRefGoogle Scholar
  35. Mastronarde D (1987) Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. J Neurophysiol 57:357–380PubMedGoogle Scholar
  36. Marrocco R, McClurkin J, Alkire M (1996) The influence of the visual cortex on the spatiotemporal response properties of lateral geniculate nucleus cells. Brain Res 737:110–118PubMedCrossRefGoogle Scholar
  37. Mayer J, Schuster HG, Claussen JC (2006) Role of inhibitory feedback for information processing in thalamocortical circuits. Phys Rev E 73(3 Pt 1):031908CrossRefGoogle Scholar
  38. McAlonan K, Brown VJ, Bowman EM (2000) Thalamic reticular nucleus activation reflects attentional gating during classical conditioning. J Neurosci 20(23):8897–8901PubMedGoogle Scholar
  39. Miller LM, Escabi MA, Read HL, Schreiner CE (2002) Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J Neurophysiol 87(1):516–527PubMedGoogle Scholar
  40. Montero VM (1991) A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Exp Brain Res 86(2):257–270PubMedCrossRefGoogle Scholar
  41. Montero VM (2000) Attentional activation of the visual thalamic reticular nucleus depends on ‘top–down’ inputs from the primary visual cortex via corticogeniculate pathways. Brain Res 864(1): 95–104PubMedCrossRefGoogle Scholar
  42. Mukherjee P, Kaplan E (1995) Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. J Neurophysiol 74:1222–1243PubMedGoogle Scholar
  43. Murphy PC, Duckett SG, Sillito AM (1999) Feedback connections to the lateral geniculate nucleus and cortical response properties. Science 286(5444):1552–1554PubMedCrossRefGoogle Scholar
  44. Reid RC, Soodak RE, Shapley RM (1991) Directional selectivity and spatiotemporal structure of the receptive field of simple cells in cat striate cortex. J Neurophysiol 66:505–529PubMedGoogle Scholar
  45. Reid RC, Alonso JM (1995) Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378(6554):281–284PubMedCrossRefGoogle Scholar
  46. Reid RC, Shapley RM (2002) Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. J Neurosci 22(14):6158–6175PubMedGoogle Scholar
  47. Reid RC, Victor JD, Shapley RM (1997) The use of m-sequences in the analysis of visual neurons: linear receptive field properties. Vis Neurosci 14(6):1015–1027PubMedCrossRefGoogle Scholar
  48. Ringach DL (2004) Mapping receptive fields in primary visual cortex. J Physiol 558(3):717–728PubMedCrossRefGoogle Scholar
  49. Sillito AM, Jones HE (2002) Corticothalamic interactions in the transfer of visual information. Philos Trans R Soc Lond B Biol Sci 357:1739–1752PubMedCrossRefGoogle Scholar
  50. Suffczynski P, Kalitzin S, Pfurtscheller G, da Silva FH (2001) Computational model of thalamo-cortical networks: dynamical control of alpha rhythms in relation to focal attention. Int J Psychophysiol 43(1):25–40PubMedCrossRefGoogle Scholar
  51. Terman D, Bose A, Kopell N (1996) Functional reorganization in thalamocortical networks: transition between spindling and delta sleep rhythms. Proc Nat Acad Sci USA 93(26):15417–15422PubMedCrossRefGoogle Scholar
  52. Truccolo W, Dong D (2001) Dynamic temporal decorrelation: an information-theoretic and biophysical model of the functional role of the lateral geniculate nucleus. Neurocomput 38–40:993–1001CrossRefGoogle Scholar
  53. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL (1997) Paradoxical effects of external modulation of inhibitory interneurons. J Neurosci 17(11):4382–4388PubMedGoogle Scholar
  54. Turner JP, Anderson CM, Williams SR, Crunelli V (1997) Morphology and membrane properties of neurons in the cat ventrobasal thalamus in vitro. J Physiol 505(3):707–726PubMedCrossRefGoogle Scholar
  55. Uhlrich DJ, Tamamaki N, Sherman SM (1990) Brainstem control of response modes in neurons of the cat’s lateral geniculate nucleus. Proc Nat Acad Sci USA 87(7):2560–2563PubMedCrossRefGoogle Scholar
  56. Ulrich D, Huguenard JR (1996) Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: a dynamic clamp study. Proc Nat Acad Sci USA 93(23):13245–13249PubMedCrossRefGoogle Scholar
  57. Usrey WM, Reppas JB, Reid RC (1999) Specificity and strength of retinogeniculate connections. J Neurophysiol 82:3527–3540PubMedGoogle Scholar
  58. Van Horn SC, Erisir A, Sherman SM (2000) Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 416(4):509–520PubMedCrossRefGoogle Scholar
  59. Wang S, Bickford ME, Van Horn SC, Erisir A, Godwin DW, Sherman SM (2001) Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat. J Comp Neurol 440(4):321–341PubMedCrossRefGoogle Scholar
  60. Wang W, Jones HE, Andolina IM, Salt TE, Sillito AM (2006) Functional alignment of feedback effects from visual cortex to thalamus. Nat Neurosci 9(10):1330–1336PubMedCrossRefGoogle Scholar
  61. Weese GD, Phillips JM, Brown VJ (1999) Attentional orienting is impaired by unilateral lesions of the thalamic reticular nucleus in the rat. J Neurosci 19(22):10135–10139PubMedGoogle Scholar
  62. Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12(1):1–24PubMedGoogle Scholar
  63. Yousif NAB, Denham MJ (2005) A population-based model of the nonlinear dynamics of the thalamocortical feedback network displays intrinsic oscillations in the spindling (7–14 Hz) range. Eur J Neurosc 22:3179–3187CrossRefGoogle Scholar
  64. Zhu J, Uhlrich D, Lytton W (1999) Burst firing in identified rat geniculate interneurons. Neuroscience 91:1445–1460PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Centre for Computational and Theoretical NeuroscienceUniversity of PlymouthPlymouthUK

Personalised recommendations