The information regarding visual stimulus is encoded in spike trains at the output of retina by retinal ganglion cells (RGCs). Among these, the directional selective cells (DSRGC) are signaling the direction of stimulus motion. DSRGCs' spike trains show accentuated periods of short interspike intervals (ISIs) framed by periods of isolated spikes. Here we use two types of visual stimulus, white noise and drifting bars, and show that short ISI spikes of DSRGCs spike trains are more often correlated to their preferred stimulus feature (that is, the direction of stimulus motion) and carry more information than longer ISI spikes. Firstly, our results show that correlation between stimulus and recorded neuronal response is best at short ISI spiking activity and decrease as ISI becomes larger. We then used grating bars stimulus and found that as ISI becomes shorter the directional selectivity is better and information rates are higher. Interestingly, for the less encountered type of DSRGC, known as ON-DSRGC, short ISI distribution and information rates revealed consistent differences when compared with the other directional selective cell type, the ON-OFF DSRGC. However, these findings suggest that ISI-based temporal filtering integrates a mechanism for visual information processing at the output of retina toward higher stages within early visual system. 1. Introduction The information regarding visual stimulus is encapsulated initially in spike trains at the output of retina by retinal ganglion cells [1–4]. In some of mammals (though not general to mammals), the direction of stimulus motion is already signaled by the well-known directional selective retinal ganglion cells (DSRGCs) [5, 6]. They respond vigorously to the movement of stimulus at the preferred direction and are silent when stimulus movement is toward the opposite null direction [7]. In rabbit retina, one type of DSRGCs, known as the ON-OFF DSRGCs, has been already very well characterized [5, 6, 8–12]. They respond at the beginning and the end of an increasing or decreasing light stimulus and project to the dorsal lateral geniculate nucleus (LGN) and to the superior colliculus [11, 13]. Receptive fields (RFs) become progressively more sophisticated along the synaptic hierarchies from retina to cortex. However, for the LGN cells the center-surround RFs are similar to those of retinal afferents [14–16]. With this advantage in mind, together with the fact that the receptive field centers of LGN cells receive their main input from only one retinal ganglion cell (RGC) [17–19], the retinogeniculate
References
[1]
W. R. Levick, “Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina,” The Journal of Physiology, vol. 188, no. 3, pp. 285–307, 1967.
[2]
R. W. Rodieck, “Informing the brain,” in The First Steps in Seeing, pp. 266–292, Sinauer Associates, Sunderland, Mass, USA, 1998.
[3]
M. Carandini, J. C. Horton, and L. C. Sincich, “Thalamic filtering of retinal spike trains by postsynaptic summation,” Journal of Vision, vol. 7, no. 14, article 20, 2007.
[4]
G. M. Zeck and R. H. Masland, “Spike train signatures of retinal ganglion cell types,” European The Journal of Neuroscience, vol. 26, no. 2, pp. 367–380, 2007.
[5]
H. B. Barlow and R. M. Hill, “Selective sensitivity to direction of movement in ganglion cells of the rabbit retina,” Science, vol. 139, no. 3553, pp. 412–414, 1963.
[6]
H. B. Barlow, R. M. Hill, and W. R. Levick, “Retinal ganglion cells responding selectively to direction and speed of,” The Journal of Physiology, vol. 173, pp. 377–407, 1964.
[7]
W. R. Levick, C. W. Oyster, and E. Takahashi, “Rabbit lateral geniculate nucleus: sharpener of directional information,” Science, vol. 165, no. 3894, pp. 712–714, 1969.
[8]
F. R. Amthor, C. W. Oyster, and E. S. Takahashi, “Morphology of on-off direction-selective ganglion cells in the rabbit retina,” Brain Research, vol. 298, no. 1, pp. 187–196, 1984.
[9]
F. R. Amthor, E. S. Takahashi, and C. W. Oyster, “Morphologies of rabbit retinal ganglion cells with complex receptive fields,” Journal of Comparative Neurology, vol. 280, no. 1, pp. 97–121, 1989.
[10]
T. Euler, P. B. Detwiler, and W. Denk, “Directionally selective calcium signals in dendrites of starburst amacrine cells,” Nature, vol. 418, no. 6900, pp. 845–852, 2002.
[11]
D. I. Vaney, W. R. Levick, and L. N. Thibos, “Rabbit retinal ganglion cells. Receptive field classification and axonal conduction properties,” Experimental Brain Research, vol. 44, no. 1, pp. 27–33, 1981.
[12]
D. I. Vaney, L. Peichi, H. Wassle, and R. B. Illing, “Almost all ganglion cells in the rabbit retina project to the superior colliculus,” Brain Research, vol. 212, no. 2, pp. 447–453, 1981.
[13]
B. G. Cleland, W. R. Levick, R. Morstyn, and H. G. Wagner, “Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex,” The Journal of Physiology, vol. 255, no. 1, pp. 299–320, 1976.
[14]
D. H. Hubel and T. N. Wiesel, “Receptive fields, binocular interaction and functional architecture in the cat's visual cortex,” The Journal of Physiology, vol. 160, pp. 106–154, 1962.
[15]
S. W. Kuffler , “Discharge patterns and functional organization of mammalian retina,” Journal of Neurophysiology, vol. 16, no. 1, pp. 37–68, 1953.
[16]
R. C. Reid and W. M. Usrey, “Functional connectivity in the pathway from retina to visual cortex,” in The Visual Neurosciences, L. M. Chalupa and J. S. Werner, Eds., pp. 673–679, MIT Press, Cambridge, Mass, USA, 2004.
[17]
B. G. Cleland, M. W. Dubin, and W. R. Levick, “Simultaneous recording of input and output of lateral geniculate neurones,” Nature, vol. 231, no. 23, pp. 191–192, 1971.
[18]
L. C. Sincich, D. L. Adams, J. R. Economides, and J. C. Horton, “Transmission of spike trains at the retinogeniculate synapse,” The Journal of Neuroscience, vol. 27, no. 10, pp. 2683–2692, 2007.
[19]
W. M. Usrey, J. B. Reppas, and R. C. Reid, “Specificity and strength of retinogeniculate connections,” Journal of Neurophysiology, vol. 82, no. 6, pp. 3527–3540, 1999.
[20]
A. Casti, F. Hayot, Y. Xiao, and E. Kaplan, “A simple model of retina-LGN transmission,” Journal of Computational Neuroscience, vol. 24, no. 2, pp. 235–252, 2008.
[21]
D. L. Rathbun, H. J. Alitto, T. G. Weyand, and W. M. Usrey, “Interspike interval analysis of retinal ganglion cell receptive fields,” Journal of Neurophysiology, vol. 98, no. 2, pp. 911–919, 2007.
[22]
D. L. Rathbun, D. K. Warland, and W. M. Usrey, “Spike timing and information transmission at retinogeniculate synapses,” The Journal of Neuroscience, vol. 30, no. 41, pp. 13558–13566, 2010.
[23]
L. C. Sincich, J. C. Horton, and T. O. Sharpee, “Preserving information in neural transmission,” The Journal of Neuroscience, vol. 29, no. 19, pp. 6207–6216, 2009.
[24]
W. M. Usrey, J. M. Alonso, and R. C. Reid, “Synaptic interactions between thalamic inputs to simple cells in cat visual cortex,” The Journal of Neuroscience, vol. 20, no. 14, pp. 5461–5467, 2000.
[25]
W. M. Usrey, J. B. Reppas, and R. C. Reid, “Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus,” Nature, vol. 395, no. 6700, pp. 384–387, 1998.
[26]
T. G. Weyand, “Retinogeniculate transmission in wakefulness,” Journal of Neurophysiology, vol. 98, no. 2, pp. 769–785, 2007.
[27]
M. W. Levine and B. G. Cleland, “An analysis of the effect of retinal ganglion cell impulses upon the firing probability of neurons in the dorsal lateral geniculate nucleus of the cat,” Brain Research, vol. 902, no. 2, pp. 244–254, 2001.
[28]
D. N. Mastronarde, “Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties,” Journal of Neurophysiology, vol. 57, no. 2, pp. 381–413, 1987.
[29]
R. Uglesich, A. Casti, F. Hayot, and E. Kaplan, “Stimulus size dependence of information transfer from retina to thalamus,” Frontiers in Systems Neuroscience, vol. 3, article 10, 2009.
[30]
W. R. Taylor and D. I. Vaney, “Diverse synaptic mechanisms generate direction selectivity in the rabbit retina,” The Journal of Neuroscience, vol. 22, no. 17, pp. 7712–7720, 2002.
[31]
A. V. Martiniuc and A. Knoll, “Sharpening of directional selectivity from neural output of rabbit retina,” Journal of Computational Neuroscience, vol. 30, no. 2, pp. 409–426, 2011.
[32]
R. E. Soodak and J. I. Simpson, “The accessory optic system of rabbit. I. Basic visual response properties,” Journal of Neurophysiology, vol. 60, no. 6, pp. 2037–2054, 1988.
[33]
J. M. Ackert, S. H. Wu, J. C. Lee et al., “Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina,” The Journal of Neuroscience, vol. 26, no. 16, pp. 4206–4215, 2006.
[34]
G. Yang and R. H. Masland, “Receptive fields and dendritic structure of directionally selective retinal ganglion cells,” The Journal of Neuroscience, vol. 14, no. 9, pp. 5267–5280, 1994.
[35]
A. Koizumi, T. C. Jakobs, and R. H. Masland, “Inward rectifying currents stabilize the membrane potential in dendrites of mouse amacrine cells: patch-clamp recordings and single-cell RT-PCR,” Molecular Vision, vol. 10, pp. 328–340, 2004.
[36]
R. C. Reid, J. D. Victor, and R. M. Shapley, “The use of m-sequences in the analysis of visual neurons: linear receptive field properties,” Visual Neuroscience, vol. 14, no. 6, pp. 1015–1027, 1997.
[37]
S. H. DeVries and D. A. Baylor, “Mosaic arrangement of ganglion cell receptive fields in rabbit retina,” Journal of Neurophysiology, vol. 78, no. 4, pp. 2048–2060, 1997.
[38]
L. Paninski, “Convergence properties of three spike-triggered analysis techniques,” Network, vol. 14, no. 3, pp. 437–464, 2003.
[39]
D. W. Godwin, J. W. Vaughan, and S. M. Sherman, “Metabotropic glutamate receptors switch visual response mode of lateral geniculate nucleus cells from burst to tonic,” Journal of Neurophysiology, vol. 76, no. 3, pp. 1800–1816, 1996.
[40]
W. Guido, S. M. Lu, J. W. Vaughan, D. W. Godwin, and S. Murray Sherman, “Receiver operating characteristics (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode,” Visual Neuroscience, vol. 12, no. 4, pp. 723–741, 1995.
[41]
H. Shimazaki and S. Shinomoto, “A method for selecting the bin size of a time histogram,” Neural Computation, vol. 19, no. 6, pp. 1503–1527, 2007.
[42]
S. P. Strong, R. Koberle, R. R. de Ruyter van Steveninck, and W. Bialek, “Entropy and information in neural spike trains,” Physical Review Letters, vol. 80, no. 1, pp. 197–200, 1998.
[43]
N. Brenner, S. P. Strong, R. Koberle, W. Bialek, and R. R. de Ruyter Van Steveninck, “Synergy in a neural code,” Neural Computation, vol. 12, no. 7, pp. 1531–1552, 2000.
[44]
B. A. Olshausen and D. J. Field, “Sparse coding of sensory inputs,” Current Opinion in Neurobiology, vol. 14, no. 4, pp. 481–487, 2004.
[45]
D. H. Hubel and T. N. Wiesel, “Integrative action in the cat's lateral geniculate body,” The Journal of Physiology, vol. 155, pp. 385–398, 1961.
[46]
E. Kaplan, K. Purpura, and R. M. Shapley, “Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus,” The Journal of Physiology, vol. 391, pp. 267–288, 1987.
[47]
D. M. Blitz and W. G. Regehr, “Retinogeniculate synaptic properties controlling spike number and timing in relay neurons,” Journal of Neurophysiology, vol. 90, no. 4, pp. 2438–2450, 2003.
[48]
A. L. Fairhall, C. A. Burlingame, R. Narasimhan, R. A. Harris, J. L. Puchalla, and M. J. Berry, “Selectivity for multiple stimulus features in retinal ganglion cells,” Journal of Neurophysiology, vol. 96, no. 5, pp. 2724–2738, 2006.
[49]
P. Kara, P. Reinagel, and R. C. Reid, “Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons,” Neuron, vol. 27, no. 3, pp. 635–646, 2000.
[50]
M. J. Berry, D. K. Warland, and M. Meister, “The structure and precision of retinal spike trains,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 10, pp. 5411–5416, 1997.
[51]
H. A. Swadlow and A. G. Gusev, “The impact of 'bursting' thalamic impulses at a neocortical synapse,” Nature Neuroscience, vol. 4, no. 4, pp. 402–408, 2001.
[52]
H. A. Swadlow, A. G. Gusev, and T. Bezdudnaya, “Activation of a cortical column by a thalamocortical impulse,” The Journal of Neuroscience, vol. 22, no. 17, pp. 7766–7773, 2002.
[53]
M. Carandini and D. Ferster, “Membrane potential and firing rate in cat primary visual cortex,” The Journal of Neuroscience, vol. 20, no. 1, pp. 470–484, 2000.
[54]
B. Jagadeesh, H. S. Wheat, L. L. Kontsevich, C. W. Tyler, and D. Ferster, “Direction selectivity of synaptic potentials in simple cells of the cat visual cortex,” Journal of Neurophysiology, vol. 78, no. 5, pp. 2772–2789, 1997.
[55]
N. J. Priebe and D. Ferster, “Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex,” Neuron, vol. 45, no. 1, pp. 133–145, 2005.
[56]
M. Volgushev, J. Pernberg, and U. T. Eysel, “Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex,” European The Journal of Neuroscience, vol. 12, no. 1, pp. 257–263, 2000.
[57]
C. W. Oyster, “The analysis of image motion by the rabbit retina,” The Journal of Physiology, vol. 199, no. 3, pp. 613–635, 1968.
