Abstract
Neural signals are corrupted by noise and this places limits on information processing. We review the processes involved in goal-directed movements and how neural noise and uncertainty determine aspects of our behaviour. First, noise in sensory signals limits perception. We show that, when localizing our hand, the central nervous system (CNS) integrates visual and proprioceptive information, each with different noise properties, in a way that minimizes the uncertainty in the overall estimate. Second, noise in motor commands leads to inaccurate movements. We review an optimal-control framework, known as 'task optimization in the presence of signal-dependent noise', which assumes that movements are planned so as to minimize the deleterious consequences of noise and thereby minimize inaccuracy. Third, during movement, sensory and motor signals have to be integrated to allow estimation of the body's state. Models are presented that show how these signals are optimally combined. Finally, we review how the CNS deals with noise at the neural and network levels. In all of these processes, the CNS carries out the tasks in such a way that the detrimental effects of noise are minimized. This shows that it is important to consider effects at the neural level in order to understand performance at the behavioural level.
Full Text
The Full Text of this article is available as a PDF (167.3 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abbott L. F., Dayan P. The effect of correlated variability on the accuracy of a population code. Neural Comput. 1999 Jan 1;11(1):91–101. doi: 10.1162/089976699300016827. [DOI] [PubMed] [Google Scholar]
- Atkeson C. G., Hollerbach J. M. Kinematic features of unrestrained vertical arm movements. J Neurosci. 1985 Sep;5(9):2318–2330. doi: 10.1523/JNEUROSCI.05-09-02318.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baraduc P., Guigon E., Burnod Y. Recoding arm position to learn visuomotor transformations. Cereb Cortex. 2001 Oct;11(10):906–917. doi: 10.1093/cercor/11.10.906. [DOI] [PubMed] [Google Scholar]
- Blakemore S. J., Frith C. D., Wolpert D. M. Spatio-temporal prediction modulates the perception of self-produced stimuli. J Cogn Neurosci. 1999 Sep;11(5):551–559. doi: 10.1162/089892999563607. [DOI] [PubMed] [Google Scholar]
- Blakemore S. J., Frith C. D., Wolpert D. M. The cerebellum is involved in predicting the sensory consequences of action. Neuroreport. 2001 Jul 3;12(9):1879–1884. doi: 10.1097/00001756-200107030-00023. [DOI] [PubMed] [Google Scholar]
- Blakemore S. J., Smith J., Steel R., Johnstone C. E., Frith C. D. The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring. Psychol Med. 2000 Sep;30(5):1131–1139. doi: 10.1017/s0033291799002676. [DOI] [PubMed] [Google Scholar]
- Blakemore S. J., Wolpert D. M., Frith C. D. Central cancellation of self-produced tickle sensation. Nat Neurosci. 1998 Nov;1(7):635–640. doi: 10.1038/2870. [DOI] [PubMed] [Google Scholar]
- Collewijn H., Erkelens C. J., Steinman R. M. Binocular co-ordination of human horizontal saccadic eye movements. J Physiol. 1988 Oct;404:157–182. doi: 10.1113/jphysiol.1988.sp017284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crutcher M. D., DeLong M. R. Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res. 1984;53(2):244–258. doi: 10.1007/BF00238154. [DOI] [PubMed] [Google Scholar]
- Deneve S., Latham P. E., Pouget A. Reading population codes: a neural implementation of ideal observers. Nat Neurosci. 1999 Aug;2(8):740–745. doi: 10.1038/11205. [DOI] [PubMed] [Google Scholar]
- Enderle J. D., Wolfe J. W. Time-optimal control of saccadic eye movements. IEEE Trans Biomed Eng. 1987 Jan;34(1):43–55. doi: 10.1109/tbme.1987.326014. [DOI] [PubMed] [Google Scholar]
- FITTS P. M. The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol. 1954 Jun;47(6):381–391. [PubMed] [Google Scholar]
- Festinger L., Canon L. K. Information about spatial location based on knowledge about efference. Psychol Rev. 1965 Sep;72(5):373–384. doi: 10.1037/h0022205. [DOI] [PubMed] [Google Scholar]
- Flash T., Hogan N. The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci. 1985 Jul;5(7):1688–1703. doi: 10.1523/JNEUROSCI.05-07-01688.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fortier P. A., Kalaska J. F., Smith A. M. Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J Neurophysiol. 1989 Jul;62(1):198–211. doi: 10.1152/jn.1989.62.1.198. [DOI] [PubMed] [Google Scholar]
- Georgopoulos A. P., Kalaska J. F., Caminiti R., Massey J. T. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci. 1982 Nov;2(11):1527–1537. doi: 10.1523/JNEUROSCI.02-11-01527.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Georgopoulos A. P., Kalaska J. F., Massey J. T. Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. J Neurophysiol. 1981 Oct;46(4):725–743. doi: 10.1152/jn.1981.46.4.725. [DOI] [PubMed] [Google Scholar]
- Guigon Emmanuel, Baraduc Pierre. A neural model of perceptual-motor alignment. J Cogn Neurosci. 2002 May 15;14(4):538–549. doi: 10.1162/08989290260045792. [DOI] [PubMed] [Google Scholar]
- Gómez C., Canals J., Torres B., Delgado-García J. M. Analysis of the fluctuations in the interspike intervals of abducens nucleus neurons during ocular fixation in the alert cat. Brain Res. 1986 Sep 3;381(2):401–404. doi: 10.1016/0006-8993(86)90099-5. [DOI] [PubMed] [Google Scholar]
- Harris C. M. Does saccadic undershoot minimize saccadic flight-time? A Monte-Carlo study. Vision Res. 1995 Mar;35(5):691–701. doi: 10.1016/0042-6989(94)00163-g. [DOI] [PubMed] [Google Scholar]
- Harris C. M. On the optimal control of behaviour: a stochastic perspective. J Neurosci Methods. 1998 Aug 31;83(1):73–88. doi: 10.1016/s0165-0270(98)00063-6. [DOI] [PubMed] [Google Scholar]
- Harris C. M., Wolpert D. M. Signal-dependent noise determines motor planning. Nature. 1998 Aug 20;394(6695):780–784. doi: 10.1038/29528. [DOI] [PubMed] [Google Scholar]
- Hepp K., Henn V. ISO-frequency curves of oculomotor neurons in the rhesus monkey. Vision Res. 1985;25(4):493–499. doi: 10.1016/0042-6989(85)90151-8. [DOI] [PubMed] [Google Scholar]
- Hogan N. An organizing principle for a class of voluntary movements. J Neurosci. 1984 Nov;4(11):2745–2754. doi: 10.1523/JNEUROSCI.04-11-02745.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacobs R. A. Optimal integration of texture and motion cues to depth. Vision Res. 1999 Oct;39(21):3621–3629. doi: 10.1016/s0042-6989(99)00088-7. [DOI] [PubMed] [Google Scholar]
- Kalaska J. F., Caminiti R., Georgopoulos A. P. Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex. Exp Brain Res. 1983;51(2):247–260. doi: 10.1007/BF00237200. [DOI] [PubMed] [Google Scholar]
- Keele S. W., Posner M. I. Processing of visual feedback in rapid movements. J Exp Psychol. 1968 May;77(1):155–158. doi: 10.1037/h0025754. [DOI] [PubMed] [Google Scholar]
- Lacquaniti F., Terzuolo C., Viviani P. The law relating the kinematic and figural aspects of drawing movements. Acta Psychol (Amst) 1983 Oct;54(1-3):115–130. doi: 10.1016/0001-6918(83)90027-6. [DOI] [PubMed] [Google Scholar]
- Mainen Z. F., Sejnowski T. J. Reliability of spike timing in neocortical neurons. Science. 1995 Jun 9;268(5216):1503–1506. doi: 10.1126/science.7770778. [DOI] [PubMed] [Google Scholar]
- Meyer D. E., Abrams R. A., Kornblum S., Wright C. E., Smith J. E. Optimality in human motor performance: ideal control of rapid aimed movements. Psychol Rev. 1988 Jul;95(3):340–370. doi: 10.1037/0033-295x.95.3.340. [DOI] [PubMed] [Google Scholar]
- Miall R. C., Weir D. J., Wolpert D. M., Stein J. F. Is the cerebellum a smith predictor? J Mot Behav. 1993 Sep;25(3):203–216. doi: 10.1080/00222895.1993.9942050. [DOI] [PubMed] [Google Scholar]
- Middlebrooks J. C., Green D. M. Sound localization by human listeners. Annu Rev Psychol. 1991;42:135–159. doi: 10.1146/annurev.ps.42.020191.001031. [DOI] [PubMed] [Google Scholar]
- Morasso P. Spatial control of arm movements. Exp Brain Res. 1981;42(2):223–227. doi: 10.1007/BF00236911. [DOI] [PubMed] [Google Scholar]
- Pouget A., Zhang K., Deneve S., Latham P. E. Statistically efficient estimation using population coding. Neural Comput. 1998 Feb 15;10(2):373–401. doi: 10.1162/089976698300017809. [DOI] [PubMed] [Google Scholar]
- Read H. L., Siegel R. M. The origins of aperiodicities in sensory neuron entrainment. Neuroscience. 1996 Nov;75(1):301–314. doi: 10.1016/0306-4522(96)00227-8. [DOI] [PubMed] [Google Scholar]
- SPERRY R. W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol. 1950 Dec;43(6):482–489. doi: 10.1037/h0055479. [DOI] [PubMed] [Google Scholar]
- Salinas E., Abbott L. F. Transfer of coded information from sensory to motor networks. J Neurosci. 1995 Oct;15(10):6461–6474. doi: 10.1523/JNEUROSCI.15-10-06461.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmidt R. A., Zelaznik H., Hawkins B., Frank J. S., Quinn J. T., Jr Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev. 1979 Sep;47(5):415–451. [PubMed] [Google Scholar]
- Stevens C. F., Zador A. M. Input synchrony and the irregular firing of cortical neurons. Nat Neurosci. 1998 Jul;1(3):210–217. doi: 10.1038/659. [DOI] [PubMed] [Google Scholar]
- Tillery S. I., Soechting J. F., Ebner T. J. Somatosensory cortical activity in relation to arm posture: nonuniform spatial tuning. J Neurophysiol. 1996 Oct;76(4):2423–2438. doi: 10.1152/jn.1996.76.4.2423. [DOI] [PubMed] [Google Scholar]
- Todorov Emanuel. Cosine tuning minimizes motor errors. Neural Comput. 2002 Jun;14(6):1233–1260. doi: 10.1162/089976602753712918. [DOI] [PubMed] [Google Scholar]
- Tsodyks M. V., Markram H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):719–723. doi: 10.1073/pnas.94.2.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uno Y., Kawato M., Suzuki R. Formation and control of optimal trajectory in human multijoint arm movement. Minimum torque-change model. Biol Cybern. 1989;61(2):89–101. doi: 10.1007/BF00204593. [DOI] [PubMed] [Google Scholar]
- Warren D. H., Schmitt T. L. Intermodal organization: a methodological localization study. Percept Mot Skills. 1980 Jun;50(3 Pt 2):1111–1118. doi: 10.2466/pms.1980.50.3c.1111. [DOI] [PubMed] [Google Scholar]
- Weiskrantz L., Elliott J., Darlington C. Preliminary observations on tickling oneself. Nature. 1971 Apr 30;230(5296):598–599. doi: 10.1038/230598a0. [DOI] [PubMed] [Google Scholar]
- Wolpert D. M., Ghahramani Z., Jordan M. I. An internal model for sensorimotor integration. Science. 1995 Sep 29;269(5232):1880–1882. doi: 10.1126/science.7569931. [DOI] [PubMed] [Google Scholar]
- Wolpert D. M., Miall R. C. Forward Models for Physiological Motor Control. Neural Netw. 1996 Nov;9(8):1265–1279. doi: 10.1016/s0893-6080(96)00035-4. [DOI] [PubMed] [Google Scholar]
- Zemel R. S., Dayan P., Pouget A. Probabilistic interpretation of population codes. Neural Comput. 1998 Feb 15;10(2):403–430. doi: 10.1162/089976698300017818. [DOI] [PubMed] [Google Scholar]
- van Beers R. J., Sittig A. C., Denier van der Gon J. J. How humans combine simultaneous proprioceptive and visual position information. Exp Brain Res. 1996 Sep;111(2):253–261. doi: 10.1007/BF00227302. [DOI] [PubMed] [Google Scholar]
- van Beers R. J., Sittig A. C., Denier van der Gon J. J. The precision of proprioceptive position sense. Exp Brain Res. 1998 Oct;122(4):367–377. doi: 10.1007/s002210050525. [DOI] [PubMed] [Google Scholar]
- van Beers R. J., Sittig A. C., Gon J. J. Integration of proprioceptive and visual position-information: An experimentally supported model. J Neurophysiol. 1999 Mar;81(3):1355–1364. doi: 10.1152/jn.1999.81.3.1355. [DOI] [PubMed] [Google Scholar]
- van Beers Robert J., Wolpert Daniel M., Haggard Patrick. When feeling is more important than seeing in sensorimotor adaptation. Curr Biol. 2002 May 14;12(10):834–837. doi: 10.1016/s0960-9822(02)00836-9. [DOI] [PubMed] [Google Scholar]
- van Sonderen J. F., Denier van der Gon J. J., Gielen C. C. Conditions determining early modification of motor programmes in response to changes in target location. Exp Brain Res. 1988;71(2):320–328. doi: 10.1007/BF00247492. [DOI] [PubMed] [Google Scholar]
- van Vreeswijk C., Sompolinsky H. Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science. 1996 Dec 6;274(5293):1724–1726. doi: 10.1126/science.274.5293.1724. [DOI] [PubMed] [Google Scholar]