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Dynamic updating of distributed neural representations using forward models

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Abstract

In this paper, we present a continuous attractor network model that we hypothesize will give some suggestion of the mechanisms underlying several neural processes such as velocity tuning to visual stimulus, sensory discrimination, sensorimotor transformations, motor control, motor imagery, and imitation. All of these processes share the fundamental characteristic of having to deal with the dynamic integration of motor and sensory variables in order to achieve accurate sensory prediction and/or discrimination. Such principles have already been described in the literature by other high-level modeling studies (Decety and Sommerville in Trends Cogn Sci 7:527–533, 2003; Oztop et al. in Neural Netw 19(3):254–271, 2006; Wolpert et al. in Philos Trans R Soc 358:593–602, 2003). With respect to these studies, our work is more concerned with biologically plausible neural dynamics at a population level. Indeed, we show that a relatively simple extension of the classical neural field models can endow these networks with additional dynamic properties for updating their internal representation using external commands. Moreover, an analysis of the interactions between our model and external inputs also shows interesting properties, which we argue are relevant for a better understanding of the neural processes of the brain.

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References

  • Amari S (1977) Dynamics of pattern formation in lateral-inhibition type neural fields. Biol Cybern 27:77–87

    Article  CAS  PubMed  Google Scholar 

  • Arbib MA (2002) The mirror system, imitation and the evolution of language. In: Imitation in animals and artefacts, a bradford book. MIT Press, Cambridge pp 229-80

  • Ben Hamed S, Duffy C, Pouget A (2003) MSTd neuronal basis functions for the population encoding of heading direction. J Neurophysiol 90:549–558

    Article  CAS  PubMed  Google Scholar 

  • Ben-Yishai R, Bar-Or RL, Sompolinsky H (1995) Theory of orientation tuning in visual cortex. Proc Nat Acad Sci USA 92:3844–3848

    Article  CAS  PubMed  Google Scholar 

  • Blanke O, Mohr C (2005) Out-of-body experience, heautoscopy, and autoscopic hallucination of neurological origin: implications for neurocognitive mechanisms of corporeal awareness and self-consciousness. Brain Res Rev 50(1):184–199

    Article  PubMed  Google Scholar 

  • Blanke O, Ortigue S, Landis T, Seeck M (2002) Stimulating illusory own body perceptions. Nature 419:269–270

    Article  CAS  PubMed  Google Scholar 

  • Burnod Y, Baraduc P, Battaglia-Mayer A, Guigon E, Koechlin E, Ferraina S, Laquaniti F, Caminiti R (1999) Parieto-frontal coding of reaching: an integrated framework. Exp Brain Res 129:325–346

    Article  CAS  PubMed  Google Scholar 

  • Chaminade T, Franklin D, Oztop E, Cheng G (2005) Motor interference between humans and humanoid robots: Effect of biological and artificial motion. In: Proceedings of the 4th IEEE International Conference on Development and Learning, Osaka, Japan pp 96-01

  • Cheng K, Hasegawa T, Kadharbatcha SS, Tanaka K (1994) Comparison of neuronal selectivity for stimulus speed, length, and contrast in the prestriate visual cortical areas V4 and MT of the macaque monkey. J Neurophysiol 71(6):2269–2280

    CAS  PubMed  Google Scholar 

  • Chey J, Grossberg S, Mingolla E (1998) Neural dynamics of motion processing and speed discrimination. Vision Res 38:2769–2786

    Article  CAS  PubMed  Google Scholar 

  • De Bruyn B, Orban GA (1988) Human velocity and direction discrimination measured with random dot patterns. Vision Res 28(12):1323–1335

    Article  CAS  PubMed  Google Scholar 

  • Decety J, Sommerville JA (2003) Shared representations between self and others: a social cognitive neuroscience view. Trends Cogn Sci 7:527–533

    Article  PubMed  Google Scholar 

  • Demiris Y, Hayes G (2002) Imitation as a dual process featuring predictive and learning components: A biologically plausible computational model. In: imitation in animals and artefacts, a bradford book, MIT Press, Cambridge pp 327-362

  • Deneve S, Latham PE, Pouget A (1999) Reading population codes: a neural implementation of ideal observers. Nat Neurosci 2(8):740–745

    Article  CAS  PubMed  Google Scholar 

  • Erlhagen W, Schöner G (2002) Dynamics field theory of movement preparation. Psychol Rev 109(3):545–572

    Article  PubMed  Google Scholar 

  • Fogassi L, Gallese V (2002) The neural correlates of action understanding in non-human primates. In Mirror Neurons and the Evolution of Brain and Language, Advances in Consciousness Research, John Benjamins Publishing pp 13-5

  • Fu QG, Flament D, Coltz JD, Ebner TJ (1997) Relationship of cerebellar purkinje cell simple spike discharge to movement kinematics in the monkey. J Neurophysiol 78(1):478-91

    Google Scholar 

  • Gallese V, Goldman A (1998) Mirror neurons and the simulation theory of mind-reading. Trends Cogn Sci 2:493–501

    Article  Google Scholar 

  • Georgopoulos AP (1996) On the translation of directional motor cortical commands to activation of muscles via spinal interneuronal systems. Cogn Brain Res 3:151–155

    Article  CAS  Google Scholar 

  • Giese M (2000) Neural model for the recognition of biological motion. In: Baratoff G, Neumann H (eds) dynamische perzeption 2, Infix Verlag, Berlin pp 105-10

  • Goodwin AW, Henry GH (1975) Direction selectivity of simple striate cells: properties and mechanisms. J Neurophysiol 38:1524–1540

    CAS  PubMed  Google Scholar 

  • Haggard P, Clarke S (2003) Intentional action: conscious experience and neural prediction. Conscious Cogn 12(4):695–707

    Article  PubMed  Google Scholar 

  • Hubel D, Wiesel T (1977) Ferrier lecture: functional architecture of the macaque monkey visual cortex. Proc R Soc Lon B 198:1–59

    Article  CAS  Google Scholar 

  • Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286:2526–2528

    Article  CAS  PubMed  Google Scholar 

  • Jeannerod M (2003) The mechanism of self-recognition in human. Behav Brain Res 142:1–15

    Article  PubMed  Google Scholar 

  • Jeannerod M, Decety J (1995) Mental motor imagery: a window into the representational stages of action. Curr Opin Neurobiol 5(6):727–732

    Article  CAS  PubMed  Google Scholar 

  • Jellema T, Maassen G, Perrett DI (2004) Single cell integration and aminate form, motion and location in the superior temporal cortex of the macaque monkey. Cereb Cortex 14:781–790

    Article  PubMed  Google Scholar 

  • Kettner RE, Schwartz AB Georgopoulos AP (1988) Primate motor cortex and free arm movements to visual targets in three- dimensional space. III. positional gradients and population coding of movement direction from various movement origins. J Neurosci 8(8):2938–2947

    CAS  PubMed  Google Scholar 

  • Keysers C, Perrett DI (2004) Demystifying social cognition: a hebbian perspective. Trends Cogn Sci 8(11):501–507

    Article  PubMed  Google Scholar 

  • Kilner JM, Paulignan Y, Blakemore SJ (2003) An interference effect of observed biological movement on action. Curr Biol 13:522–525

    Article  CAS  PubMed  Google Scholar 

  • Miall RC, Reckess GZ (2002) The cerebellum and the timing of coordinated eye and hand tracking. Brain Cogn 48:212–226

    Article  CAS  PubMed  Google Scholar 

  • Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Netw 9:1265–1279

    Article  PubMed  Google Scholar 

  • Mineiro P, Zipser D (1998) Analyis of direction selectivity arising from recurrent local interactions. Neural Comput 10:353–371

    Article  CAS  PubMed  Google Scholar 

  • Nakamura K, Colby CL (2002) Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc Nat Acad Sci USA 99(6):4026–4031

    Article  CAS  PubMed  Google Scholar 

  • Orban GA, Kennedy H, Bullier J (1986) Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey. J Neurophysiol 56(2):462–480

    CAS  PubMed  Google Scholar 

  • Oztop E, Kawato M, Arbib M (2006) Mirror neurons and imitation. Neural Netw 19(3):254–271

    Article  PubMed  Google Scholar 

  • Panzeri S, Rolls ET, Battaglia F, Lavis R (2001) Speed of feedforward and recurrent processing in multilayer networks of integrate-and-fire neurons. Netw Comput Neural Syst 12:423–440

    CAS  Google Scholar 

  • Porro CA, Francescato MP, Cettolo V, Diamond ME, Baraldi P, Zuiani C, Bazzocchi M, di Prampero PE (1996) Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J Neurosci 16(23):7688–7698

    CAS  PubMed  Google Scholar 

  • Raiguel SE, Xiao DK, Marcar VL, Orban GA (1999) Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. J Neurphysiol 82:1944–1956

    CAS  Google Scholar 

  • Redish DA, Elga AN, Touretzky DS (1996) A coupled attractor model of the rodent head direction system. Netw Comput Neural Syst 7(4):671–685

    Article  Google Scholar 

  • Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding of actions. Nat Rev Neurosci 2:661–670

    Article  CAS  PubMed  Google Scholar 

  • Roitman AV, Pasalar S, Johnson MTV, Ebner TJ (2005) Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J Neurosci 25(40):9244–9257

    Article  CAS  PubMed  Google Scholar 

  • Rougier N (2006) Dynamic beural field with local inhibition. Biol Cybern 94:169–179

    Article  PubMed  Google Scholar 

  • Salinas E, Thier P (2000) Gain modulation: a major computational principle of the central nervous system. Neuron 27:15–21

    Article  CAS  PubMed  Google Scholar 

  • Sauser EL, Billard AG (2005) Three dimensional frames of references transformations using recurrent populations of neurons. Neurocomputing 64:5–24

    Article  Google Scholar 

  • Sauser EL, Billard AG (2006) Parallel and distributed neural models of the ideomotor principle: an investigation of imitative cortical pathways. Neural Netw 19(3):285–298

    Article  PubMed  Google Scholar 

  • Scherberger H, Andresen RA (2003) Sensorimotor transformations. In: Chalupa LM, Werner JS (eds) The visual neurosciences. MIT Press, Cambridge, pp 1324–1336

    Google Scholar 

  • Schöner G (2002) Dynamical systems approaches to neural systems and behavior. Int Encyclopedia Soc Behav Sci pp 10571-0575

  • Schwartz A, Moran D (1999) Motor cortical activity during drawing movements: population representation during lemniscate tracing. J Neurophysiol 82:2705–2718

    CAS  PubMed  Google Scholar 

  • Schweigenhofer N, Arbib MA, Kawato M (1998) Role of the cerebellum in reaching movements in humans. I. distributed inverse dynamics control. Eur J Neurosci 10:86–94

    Article  Google Scholar 

  • Sharp PE, Blair HT, Cho J (2001) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24(5):289–294

    Article  CAS  PubMed  Google Scholar 

  • Stringer SM, Rolls ET Trappenberg TP (2004) Self-organizing continuous attractor networks with multiple activity packets and the representation of space. Neural Netw 17:5–27

    Article  CAS  PubMed  Google Scholar 

  • Todorov E (2000) Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci 3(4):391–398

    Article  CAS  PubMed  Google Scholar 

  • Unema MM, Goldberg ME (1997) Spatial processing in the monkey frontal eye field. I. predictive visual responses. J Neurophysiol 78:1373–1383

    Google Scholar 

  • Vercher JL, Gauthier GM (1988) Cerebellar involvement in the coordination control of the oculo-manual tracking system: effects of cerebellar dendate nucleus lesion. Exp Brain Res 73:155–166

    Article  CAS  PubMed  Google Scholar 

  • Vercher JL, Gauthier GM, Guedon O, Blouin J, Cole J, Lamarre Y (1996) Self-moved target eye tracking in control and deafferented subjects: roles of arm motor command and proprioception in arm-eye coordination. J Neurophysiol 76(2):1133–1144

    CAS  PubMed  Google Scholar 

  • Wersing H, Steil JJ, Ritter H (2001) A competitive-layer model for feature binding and sensory segmentation. Neural Comput 13:357–387

    Article  CAS  PubMed  Google Scholar 

  • Wilson H, Cowan J (1973) A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetic 13:55–80

    Article  CAS  Google Scholar 

  • Wise SP, Broussaoud D, Johnson PB, Caminiti R (1997) Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci 20:25–42

    Article  CAS  PubMed  Google Scholar 

  • Wolpert DM, Doya K, Kawato M (2003) A unifying computational framework for motor control and social interaction. Philos Trans R Soc 358:593–602

    Article  Google Scholar 

  • Wolpert DM, Kawato M (1998) Multiple paired forward and inverse models for motor control. Neural Netw 11(7–8):1317–1329

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Hahnloser R, Seung H (2002) Double-ring network model of the head-direction system. Phys Rev E 66:041902

    Article  Google Scholar 

  • Zhang K (1996) Representation of the spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16(6):2112–2126

    CAS  PubMed  Google Scholar 

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Correspondence to Eric L. Sauser.

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Sauser, E.L., Billard, A.G. Dynamic updating of distributed neural representations using forward models. Biol Cybern 95, 567–588 (2006). https://doi.org/10.1007/s00422-006-0131-3

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