Figuring Space by Time

Sensory information is encoded both in space and in time. Spatial encoding is based on the identity of activated receptors, while temporal encoding is based on the timing of activation. In order to generate accurate internal representations of the external world, the brain must decode both types of encoded information, even when processing stationary stimuli. We review here evidence in support of a parallel processing scheme for spatially and temporally encoded information in the tactile system and discuss the advantages and limitations of sensory-derived temporal coding in both the tactile and visual systems. Based on a large body of data, we propose a dynamic theory for vision, which avoids the impediments of previous dynamic theories.

[1]  S. McKee,et al.  Finding the common bond: Stereoacuity and the other hyperacuities , 1990, Vision Research.

[2]  J. Kaas,et al.  Intrathalamic connections: a new way to modulate cortical plasticity? , 1998, Nature Neuroscience.

[3]  Michael S. Landy,et al.  Computational models of visual processing , 1991 .

[4]  Patrick Cavanagh,et al.  A jitter after-effect reveals motion-based stabilization of vision , 1998, Nature.

[5]  D J Simons,et al.  Cortical columnar processing in the rat whisker-to-barrel system. , 1999, Journal of neurophysiology.

[6]  E. Ahissar,et al.  A neuronal analogue of state-dependent learning , 2000, Nature.

[7]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[8]  D. Kleinfeld,et al.  Traveling Electrical Waves in Cortex Insights from Phase Dynamics and Speculation on a Computational Role , 2001, Neuron.

[9]  M. Shipley,et al.  Response characteristics of single units in the rat's trigeminal nuclei to vibrissa displacements. , 1974, Journal of neurophysiology.

[10]  F. Ebner,et al.  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 , 1992, The Journal of comparative neurology.

[11]  F. Ebner,et al.  Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. , 1999, Journal of neurophysiology.

[12]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[13]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[14]  D Kleinfeld,et al.  Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. , 1997, Journal of neurophysiology.

[15]  R. Shapley,et al.  Hyperacuity in cat retinal ganglion cells. , 1986, Science.

[16]  L. Arend.  Spatial differential and integral operations in human vision: implications of stabilized retinal image fading. , 1973, Psychological review.

[17]  Moshe Gur.  PII: S0042-6989(96)00182-4 , 1997 .

[18]  R. W. Ditchburn.  Eye-movements and visual perception , 1973 .

[19]  David Williams,et al.  Blurring by fixational eye movements , 1992, Vision Research.

[20]  M J Morgan,et al.  Evidence for positional coding in hyperacuity. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[21]  M. Goodale.  Visual pathways supporting perception and action in the primate cerebral cortex , 1993, Current Opinion in Neurobiology.

[22]  M. Mead,et al.  Cybernetics , 1953, The Yale Journal of Biology and Medicine.

[23]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[24]  J. G. Thomas,et al.  Studies on Human Ocular Tremor , 1973 .

[25]  Chuan Yi Tang,et al.  A 2.|E|-Bit Distributed Algorithm for the Directed Euler Trail Problem , 1993, Inf. Process. Lett..

[26]  M L Welton,et al.  Receptors , 2004, American journal of surgery.

[27]  L A RIGGS,et al.  Motions of the retinal image during fixation. , 1954, Journal of the Optical Society of America.

[28]  D Purves,et al.  The extraordinarily rapid disappearance of entoptic images. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Armstrong‐James,et al.  Flow of excitation within rat barrel cortex on striking a single vibrissa. , 1992, Journal of neurophysiology.

[30]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[31]  R. Nijhawan,et al.  Visual decomposition of colour through motion extrapolation , 1997, Nature.

[32]  J. R. Rosenberg,et al.  The origin of ocular microtremor in man , 1999, Experimental Brain Research.

[33]  Ehud Ahissar,et al.  Simultaneous multi-site recordings and iontophoretic drug and dye applications along the trigeminal system of anesthetized rats , 1999, Journal of Neuroscience Methods.

[34]  Leonard Matin,et al.  Vernier discrimination with sequentially-flashed lines: Roles of eye movements, retinal offsets and short-term memory , 1981, Vision Research.

[35]  R. Pritchard.  Stabilized images on the retina. , 1961, Scientific American.

[36]  H. B. Barlow,et al.  Reconstructing the visual image in space and time , 1979, Nature.

[37]  D. Snodderly,et al.  Studying striate cortex neurons in behaving monkeys: Benefits of image stabilization , 1987, Vision Research.

[38]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[39]  H. Barlow.  Eye movements during fixation , 1952, The Journal of physiology.

[40]  M. Diamond.  Somatosensory Thalamus of the Rat , 1995 .

[41]  M M Merzenich,et al.  Temporal information transformed into a spatial code by a neural network with realistic properties , 1995, Science.

[42]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[43]  A. Z. Meiri,et al.  The effects of exposure duration and luminance on the 3-dot hyperacuity task , 1984, Vision Research.

[44]  R. Carpenter,et al.  Movements of the Eyes , 1978 .

[45]  J. V. Gisbergen,et al.  Scatter in the metrics of saccades and properties of the collicular motor map , 1989, Vision Research.

[46]  Eberhard E. Fetz,et al.  Cortical mechanisms controlling limb movement , 1993, Current Opinion in Neurobiology.

[47]  E Ahissar,et al.  Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[48]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[49]  T A Woolsey,et al.  Local intra‐ and interlaminar connections in mouse barrel cortex , 1990, The Journal of comparative neurology.

[50]  C E Carr,et al.  Processing of temporal information in the brain. , 1993, Annual review of neuroscience.

[51]  Floyd M. Gardner,et al.  Phaselock techniques , 1984, IEEE Transactions on Systems, Man, and Cybernetics.

[52]  M. Meister,et al.  The Light Response of Retinal Ganglion Cells Is Truncated by a Displaced Amacrine Circuit , 1997, Neuron.

[53]  M. Nicolelis,et al.  Spatiotemporal structure of somatosensory responses of many-neuron ensembles in the rat ventral posterior medial nucleus of the thalamus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  D. Marr,et al.  An Information Processing Approach to Understanding the Visual Cortex , 1980 .

[55]  S. Wise.  Monkey motor cortex: movements, muscles, motoneurons and metrics , 1993, Trends in Neurosciences.

[56]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[57]  T. Poggio,et al.  Visual hyperacuity: spatiotemporal interpolation in human vision , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[58]  H. K. Hartline,et al.  THE RESPONSE OF SINGLE OPTIC NERVE FIBERS OF THE VERTEBRATE EYE TO ILLUMINATION OF THE RETINA , 1938 .

[59]  A. Georgopoulos.  On reaching. , 1986, Annual review of neuroscience.

[60]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[61]  S. Klein,et al.  Hyperacuity thresholds of 1 sec: theoretical predictions and empirical validation. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[62]  Jun Zhang,et al.  Flexible filaments in a flowing soap film as a model for one-dimensional flags in a two-dimensional wind , 2000, Nature.

[63]  R. W. Ditchburn.  The Brain and Regulation of Eye-movement , 1978 .

[64]  E Ahissar,et al.  Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[65]  D. Simons.  Neuronal Integration in the Somatosensory Whisker/Barrel Cortex , 1995 .

[66]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[67]  F. Ebner,et al.  Barrels and septa: Separate circuits in rat barrel field cortex , 1999, The Journal of comparative neurology.

[68]  R. Jaffard.  [Neurobiology of memory]. , 1991, La Revue du praticien.

[69]  R. Kötter,et al.  Laminar characteristics of functional connectivity in rat barrel cortex revealed by stimulation with caged-glutamate , 2000, Neuroscience Research.

[70]  A. Grishman.  Biomedical sciences instrumentation , 1964 .

[71]  D. McCormick,et al.  Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[72]  E Ahissar,et al.  Temporal frequency of whisker movement. II. Laminar organization of cortical representations. , 2001, Journal of neurophysiology.

[73]  Eileen Kowler.  Eye movements and their role in visual and cognitive processes. , 1990, Reviews of oculomotor research.

[74]  R. Clay Reid,et al.  Visually evoked calcium action potentials in cat striate cortex , 1995, Nature.

[75]  R. Pritchard,et al.  Small eye movements of the cat. , 1960, Canadian journal of psychology.

[76]  K. Naka,et al.  Dynamics of the ganglion cell response in the catfish and frog retinas , 1987, The Journal of general physiology.

[77]  A. Keller.  Synaptic Organization of the Barrel Cortex , 1995 .

[78]  L. Riggs,et al.  Involuntary motions of the eye during monocular fixation. , 1950, Journal of experimental psychology.

[79]  Remo Guidieri.  Res , 1995, RES: Anthropology and Aesthetics.

[80]  E Ahissar,et al.  Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. , 2001, Journal of neurophysiology.

[81]  L MATIN,et al.  THREE-DIMENSIONAL RECORDING OF ROTATIONAL EYE MOVEMENTS BY A NEW CONTACT-LENS TECHNIQUE. , 1964, Biomedical sciences instrumentation.

[82]  J. W. Gustafson,et al.  Behavioral and neural approaches to the function of the mystacial vibrissae. , 1977 .

[83]  R. J. Watt,et al.  On the failure of spatiotemporal interpolation: A filtering model , 1983, Vision Research.

[84]  W. Welker,et al.  Coding of somatic sensory input by vibrissae neurons in the rat's trigeminal ganglion. , 1969, Brain research.

[85]  Thomas A. Woolsey,et al.  Barrels, Vibrissae, and Topographic Representations , 1988 .

[86]  D. Hubel.  Eye, brain, and vision , 1988 .

[87]  D. Simons.  Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[88]  Patrick Cavanagh,et al.  Stabilizing the visual world: A jitter aftereffect reveals motion-based correction , 1998 .

[89]  D. Levi.  Progress and Paradigm Shifts in Spatial Vision over the 20 Years of Ecvp , 1997, Perception.

[90]  D C Van Essen,et al.  Shifter circuits: a computational strategy for dynamic aspects of visual processing. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[91]  M. Brecht,et al.  Functional architecture of the mystacial vibrissae , 1997, Behavioural Brain Research.

[92]  F. H. Adler,et al.  INFLUENCE OF FIXATION ON THE VISUAL ACUITY , 1934 .

[93]  D. Levi,et al.  Spatial localization without visual references , 1992, Vision Research.

[94]  A. Keller,et al.  Intrinsic circuitry and physiological properties of pyramidal neurons in rat barrel cortex , 1997, Experimental Brain Research.

[95]  G. Westheimer.  Diffraction Theory and Visual Hyperacuity* , 1976, American journal of optometry and physiological optics.

[96]  G Westheimer,et al.  The grain of visual space. , 1990, Cold Spring Harbor symposia on quantitative biology.

[97]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus , 1992, The Journal of comparative neurology.

[98]  I. Darian‐Smith,et al.  Peripheral neural representation of the spatial frequency of a grating moving across the monkey's finger pad. , 1980, The Journal of physiology.

[99]  P. E. Hallett,et al.  Power spectra for ocular drift and tremor , 1985, Vision Research.

[100]  D. Snodderly,et al.  Selective activation of visual cortex neurons by fixational eye movements: Implications for neural coding , 2001, Visual Neuroscience.

[101]  Michael S. Landy,et al.  Pattern Discrimination, Visual Filters, and Spatial Sampling Irregularity , 1991 .

[102]  Mingsha Zhang,et al.  Neuronal switching of sensorimotor transformations for antisaccades , 2000, Nature.

[103]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[104]  W. Welker.  Analysis of Sniffing of the Albino Rat 1) , 1964 .

[105]  D. Purves,et al.  The wagon wheel illusion in movies and reality. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[106]  C. Gray,et al.  Stimulus-Dependent Neuronal Oscillations and Local Synchronization in Striate Cortex of the Alert Cat , 1997, The Journal of Neuroscience.

[107]  Olof Bryngdahl,et al.  Effect of Retinal Image Motion on Visual Acuity , 1961 .

[108]  L A JEFFRESS,et al.  A place theory of sound localization. , 1948, Journal of comparative and physiological psychology.

[109]  U. T. Keesey.  Effects of involuntary eye movements on visual acuity. , 1960, Journal of the Optical Society of America.

[110]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[111]  E. Ahissar,et al.  Spatial organization of facial vibrissae and cortical barrels in the guinea pig and golden hamster , 1997, The Journal of comparative neurology.

[112]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[113]  Steinman Rm,et al.  The role of eye movement in the detection of contrast and spatial detail. , 1990 .

[114]  David Hubel,et al.  A big step along the visual pathway , 1996, Nature.

[115]  D. Burr,et al.  Seeing objects in motion , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[116]  F J VERHEIJEN,et al.  A simple after image method demonstrating the involuntary multidirectional eye movements during fixation. , 1961, Optica acta.

[117]  Christopher R. Stambaugh,et al.  Encoding of Tactile Stimulus Location by Somatosensory Thalamocortical Ensembles , 2000, The Journal of Neuroscience.

[118]  Hugh R. Wilson,et al.  Responses of spatial mechanisms can explain hyperacuity , 1986, Vision Research.

[119]  Karl F. Jensen,et al.  Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex , 1988, Brain Research.

[120]  L. Riggs,et al.  The disappearance of steadily fixated visual test objects. , 1953, Journal of the Optical Society of America.

[121]  M Zacksenhouse,et al.  Temporal and spatial coding in the rat vibrissal system. , 2001, Progress in brain research.

[122]  M. Cynader,et al.  Vernier acuity of neurones in cat visual cortex , 1986, Nature.

[123]  R. Eckhorn,et al.  Oscillatory and non-oscillatory synchronizations in the visual cortex and their possible roles in associations of visual features. , 1994, Progress in brain research.

[124]  M. Deschenes,et al.  Corticothalamic Projections from the Cortical Barrel Field to the Somatosensory Thalamus in Rats: A Single‐fibre Study Using Biocytin as an Anterograde Tracer , 1995, The European journal of neuroscience.

[125]  Ehud Ahissar,et al.  Temporal-Code to Rate-Code Conversion by Neuronal Phase-Locked Loops , 1998, Neural Computation.

[126]  R. Eckhorn,et al.  High frequency (60-90 Hz) oscillations in primary visual cortex of awake monkey. , 1993, Neuroreport.

[127]  A. L. I︠A︡rbus.  Eye Movements and Vision , 1967 .

[128]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[129]  Peter Hillman,et al.  Shape similarity and distance disparity as apparent motion correspondence cues , 1988, Vision Research.

[130]  S. McKee,et al.  Dichoptic hyperacuity: the precision of nonius alignment. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[131]  Michael A. Gresty,et al.  Minute Eye Movement and Brain Stem Function , 1984 .

[132]  Luc Gagnon,et al.  Nonlinear processing of phase vocoded speech , 1990 .

[133]  M A Nicolelis,et al.  Nonlinear processing of tactile information in the thalamocortical loop. , 1997, Journal of neurophysiology.

[134]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[135]  Ehud Ahissar,et al.  Transformation from temporal to rate coding in a somatosensory thalamocortical pathway , 2000, Nature.

[136]  John Ross,et al.  Visual processing of motion , 1986, Trends in Neurosciences.

[137]  D. Simons,et al.  Task- and subject-related differences in sensorimotor behavior during active touch. , 1995, Somatosensory & motor research.

[138]  D Kleinfeld,et al.  Anatomical loops and their electrical dynamics in relation to whisking by rat. , 1999, Somatosensory & motor research.

[139]  D. Simons,et al.  Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex , 1989, The Journal of comparative neurology.

[140]  D. Sholl.  The organization of the cerebral cortex , 1957 .

[141]  R. Lin,et al.  Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. , 1993, Somatosensory & motor research.

[142]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[143]  M. Armstrong‐James,et al.  Spatiotemporal convergence and divergence in the rat S1 “Barrel” cortex , 1987, The Journal of comparative neurology.

[144]  S. McKee,et al.  Exposure duration affects the sensitivity of vernier acuity to target motion , 1983, Vision Research.

[145]  R. Steinman,et al.  The role of eye movement in the detection of contrast and spatial detail. , 1990, Reviews of oculomotor research.