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Relating Temporal Properties of Spike Trains from Area MT Neurons to the Behavior of the Monkey

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Temporal Coding in the Brain

Part of the book series: Research and Perspectives in Neurosciences ((NEUROSCIENCE))

Summary

We investigated the temporal fine structure of spike trains recorded in extrastriate area MT of the trained macaque monkey. The data were recorded previously (Britten et al. 1992) while the monkey performed a near-threshold direction discrimination task so that both physiological and psychophysical data could be obtained on the same set of trials. We identified bursting cells and quantified their properties in relation to the behavior of the animal.

We computed the power spectrum and the distribution of interspikeintervals (ISI) associated with individual spike trains from 212 cells, averaging these quanties across similar trials. One third of the cells have a relatively flat power spectrum with a dip at low temporal frequencies, compatible with a Poisson process with refractory period. About two thirds of the cells have a peak in the 20-60 Hz frequency band. This peak strongly correlates with a tendency of the cell to respond in bursts, i.e., 2–4 spikes within 2–8 msec. For 93 % of cells, the shape of the power spectrum did not change dramatically with stimulus conditions. The ISI distribution and power spectrum of bursting cells are compatible with the notion that these cells fire Poisson distributed bursts, with a burst-related refractory period. We found no statistically significant relationship between the peak in the power spectrum and psychophysical measures of the monkeys’ performance. Using signal detection theory, we show that, for bursting cells, the “event” rate—where an event is either a single burst of spikes or an isolated spike—is on average a more sensitive measure of visual stimulus direction than the total number of spikes, used previously (Britten et al. 1992), implying that the number of spikes in a burst is less stimulus-dependent than theoverall firing rate or the rate of bursts.

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References

  • Abeles M (1990) Corticonics. Cambridge, Cambridge UP

    Google Scholar 

  • Agmon A, Connors BW (1992) Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12:319–329

    PubMed  CAS  Google Scholar 

  • Aertsen AMHJ, Gerstein GL, Habib MK, Palm G (1989) Dynamics of neuronal firing correlation: Modulation of “Effective Connectivity”. J Neurophysiol 61:900–917

    PubMed  CAS  Google Scholar 

  • Bair W, Koch C, Newsome W, Britten K (1992) Power spectrum analysis of MT neurons from awake monkey. Neurosci Abstr 18:12

    Google Scholar 

  • Bair W, Koch C, Newsome W, Britten K (1994) Power spectrum analysis of bursting cells in area MT in the behaving monkey. J Neurosci 14:2870–2892

    PubMed  CAS  Google Scholar 

  • Baranyi A, Szente MB, Woody CD (1993) Electrophysiological characterization of different types of neurons recorded in-vivo in the motor cortex of the cat I. patterns of firing activity and synaptic responses. J Neurophysiol 69:1850–1864

    CAS  Google Scholar 

  • Barlow HB (1972) Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1:371–394

    Article  PubMed  CAS  Google Scholar 

  • Barlow HB, Kaushal TP, Hawken M, Parker AJ (1987) Human contrast discrimination and the threshold of cortical-neurons. J Opt Soc A 4:2366–2371

    Article  CAS  Google Scholar 

  • Bialek W, Rieke F, Vansteveninck RRD, Warland D (1991) Reading a neural code. Science 252:1854–1857

    Article  PubMed  CAS  Google Scholar 

  • Bonds AB (1992) Dual inhibitory mechanisms for definition of receptive field characterisitcs in cat striate cortex. In: Mody JE, Hanson SJ, Lippmann RP (eds) Advances in neural information processing systems. Vol. 4. Morgan Kaufmann, San Mateo, Ca, pp 75–820

    Google Scholar 

  • Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12:4745–4765

    PubMed  CAS  Google Scholar 

  • Cattaneo A, Maffei L, Morrone C (1981 a) Two firing patterns in the discharge of complex cells encoding different attributes of the visual stimulus. Exp Brain Res 43:115–118

    Article  PubMed  CAS  Google Scholar 

  • Cattaneo A, Maffei L, Morrone C (1981b) Patterns in the discharge of simple and complex visual cortical cells. Proc Roy Soc Lond B 212:279–297

    Article  CAS  Google Scholar 

  • Chung SH, Raymond SA, Lettvin JY (1970) Multiple meaning in single visual units. Brain Behav Evol 3:72–101

    Article  PubMed  CAS  Google Scholar 

  • Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99–104

    Article  PubMed  CAS  Google Scholar 

  • Crick F (1984) Function of the thalamus reticular complex: the searchlight hypothesis. Proc. Natl. Acad. Sci. USA 81:4586–4590

    Article  PubMed  CAS  Google Scholar 

  • Crick F, Koch C (1990) Towards a neurobiological theory of consciousness. Sem Neurosci 2:263–275

    Google Scholar 

  • Crick F, Koch C (1992) The problem of consciousess. Sci Amer 267:152–159

    Article  PubMed  CAS  Google Scholar 

  • Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Biol Cybernetics 60:121–130

    Article  CAS  Google Scholar 

  • Eskandar EN, Richmond BJ, Optican LM (1992) Role of inferior temporal neurons in visual memory: I. Temporal encoding of information about visual images, recalled images and behavioral context. J Neurophysiol 68:1277–1295

    CAS  Google Scholar 

  • Ghose GM, Freeman RD (1992) Oscillatory discharge in the visual system: does is have a functional role? J Neurophysiol 68:1558–1574

    PubMed  CAS  Google Scholar 

  • Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702

    Article  PubMed  CAS  Google Scholar 

  • Gray CM, K’nig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337

    Article  PubMed  CAS  Google Scholar 

  • Kasper E, Larkman A, Blakemore C, Judge S (1991) Physiology and morphology of identified projection neurons in rat visual cortex studied in vitro. Soc Neurosci Abstr 17:114

    Google Scholar 

  • Knierim J, van Essen D (1992) Neuronal responses to static textural patterns in area V1 of the alert macaque monkey. J Neurophysiol 67:961–980

    PubMed  CAS  Google Scholar 

  • Koch C, Crick F (1994) Some further ideas about the neuronal basis of visual awareness. In: Koch C, Davis J (eds) Large scale neuronal theories of the brain. MIT Press, in press

    Google Scholar 

  • Kreiter AK, Singer W (1992) Oscillatory neuronal responses in the visual cortex of the awake macaque monkey. Eur J Neurosci 4:369–375

    Article  PubMed  Google Scholar 

  • Lettvin JP, Maturana HR, McCulloch WS, Pitts WH (1959) What the frog’s eye tells the frog’s brain. Proc Inst Rad Eng 47:1940–1951

    Google Scholar 

  • Magleby KL (1987) Short-term changes in synaptic efficacy. In: Edelman GM, Gall WE, Cowan WM (eds) Synaptic function. John Wiley, New York, pp 21–56

    Google Scholar 

  • Maunsell JHR, Van Essen D (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed and orientation. J Neurophysiol 49:1127–1147

    CAS  Google Scholar 

  • McCormick DA, Connors BW, Lighthall JA, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782–806

    PubMed  CAS  Google Scholar 

  • Newsome WT, Pare EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211

    PubMed  CAS  Google Scholar 

  • Newsome WT, Britten KH, Movshon JA (1989 a) Neuronal correlates of a perceptual decision. Nature 341:52–54

    Article  PubMed  CAS  Google Scholar 

  • Newsome WT, Britten KH, Movshon JA, Shadlen M (1989 b) Single neurons and the perception of visual motion. In: Lam D, Gilbert C (eds) Neural mechanism of visual perception, pp 171–198, The Woodlands, TX: Portfolio

    Google Scholar 

  • Optican LM, Richmond BJ (1987) Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. J Neurophysiol 57:162–178

    CAS  Google Scholar 

  • Parker A, Hawken M (1985) Capabilities of monkey cortical cells in spatial-resolution rasks. J Opt Soc Am 2:1101–1114

    Article  CAS  Google Scholar 

  • Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes I. the single spike train. Biophys 7:391–418

    CAS  Google Scholar 

  • Poggio GF, Viernstein LJ (1964) Time series analysis of impulse sequences of thalamic somatic sensory neurons. J Neurophysiol 27:517–545

    PubMed  CAS  Google Scholar 

  • Press HP, Flannery BP, Teukolsky SA, Vetterling WT (1988) Numerical recipes in C, the art of scientific computing. Cambridge, Cambridge University Press

    Google Scholar 

  • Richmond BJ, Optican LM (1992) The structure and interpretation of neuronal codes in the visual system. In: Wechsler H (ed) Neural networks for perception. Academic Press, Boston, pp 104–119

    Google Scholar 

  • Salzman CD, Murasugi CM, Britten KH, Newsome WT (1992) Microstimulation in visual area MT: effects on direction discrimination performance. J Neurosci 12:2331–2355

    PubMed  CAS  Google Scholar 

  • Smith DR, Smith DK (1965) A statistical analysis of the continual activity of single cortical neurones in the cat unanaesthetized isolated forebrain. Biophys J 5:47–74

    Article  PubMed  CAS  Google Scholar 

  • Snowden RJ, Treue S, Andersen RA (1992) The response of neurons in areas V1 and MT of the alert rhesus monkey to moving random dot patterns. Exp Brain Res 88:389–400

    Article  PubMed  CAS  Google Scholar 

  • Softky WR, Koch C (1992) Cortical cells should fire regularly, but do not. Neural Computation 4:643–646

    Article  Google Scholar 

  • Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334–350

    PubMed  CAS  Google Scholar 

  • Strehler BL, Lestienne R (1986) Evidence on precise time-coded symbols and memory of patterns in monkey cortical neuronal spike trains. Proc Natl Acad Sci USA 83:9812–9816

    Article  PubMed  CAS  Google Scholar 

  • Teich MC (1992) Fractal neuronal firing. In: McKenna T, Davis J, Zornetzer S (eds) Single neuron computation neural nets: foundations to applications. Academic Press, Inc., Boston, pp. 589–625

    Google Scholar 

  • Tolhurst D, Movshon J, Dean A (1983) The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23:775–785

    Article  PubMed  CAS  Google Scholar 

  • Usher M, Stemmler M, Koch C, Olami Z (1994) Network amplification of local fluctuations causes high spike rate variability, fractal patterns and oscillatory local field potentials. Neural Comp., in press

    Google Scholar 

  • Vogels R, Orban GA (1990) How well do response changes of striate neurons signal differences in orientation—a study in the discriminating monkey. J Neurosci 10:3543–3558

    PubMed  CAS  Google Scholar 

  • Vogels R, Spileers W, Orban GA (1989) The response variability of striate cortical neurons in the behaving monkey. Exp Brain Res 77:432–436

    Article  PubMed  CAS  Google Scholar 

  • von der Malsburg C (1981) The correlation theory of brain function. Internal report 81-2, Dept. of Neurobiology, MPI for Biophysical Chemistry Göttingen

    Google Scholar 

  • Werner G, Mountcastle VB (1963) The variability of central neural activity in a sensory system and its implications for the central reflection of sensory events. J Neurophysiol 26:958–977

    PubMed  CAS  Google Scholar 

  • Zeki SM (1974) Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol (Lond) 236:549–573

    CAS  Google Scholar 

  • Zipser D, Kehoe B, Littlewort G, Fuster J (1993) A spiking network model of shortterm active memory. J Neurosci, in press

    Google Scholar 

  • Zohary E, Hillman P, Hochstein S (1990) Time course of perceptual discrimination and single neuron reliability. Biol Cybern 62:475–486

    Article  PubMed  CAS  Google Scholar 

Download references

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© 1994 Springer-Verlag Berlin Heidelberg

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Bair, W., Koch, C., Newsome, W., Britten, K. (1994). Relating Temporal Properties of Spike Trains from Area MT Neurons to the Behavior of the Monkey. In: Buzsáki, G., Llinás, R., Singer, W., Berthoz, A., Christen, Y. (eds) Temporal Coding in the Brain. Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-85148-3_13

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  • DOI: https://doi.org/10.1007/978-3-642-85148-3_13

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-85150-6

  • Online ISBN: 978-3-642-85148-3

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