Abstract
The locomotor system is a hierarchical mechanism consisting of several functional components, including the decision mechanism, navigation map, locomotion command, central pattern generators and the EMG muscle activity patterns. In this chapter we discuss the role of symmetry/asymmetry and symmetry breaking of neural states during the emergence of locomotion and movement. We review recent results that show that inhibition plays a critical role in decision making, in the formation of grid cells and place cells for navigation, the locomotor command and central pattern generators. We employ the analogy with symmetry breaking in physical systems where at a bifurcation point on the phase diagram, infinitesimal perturbations result in a transition to a new global attractor state. This observation may have major implications for both understanding normal locomotion and therapeutics of spinal cord injury, as triggered by neuromodulatory/inhibitory causes.
This is a preview of subscription content, log in via an institution.
References
Anderson PW (1997) Basic notions of condensed matter physics. Addison-Wesley Reading, Boston
Barbeau H, Rossignol S (1990) The effects of serotonergic drugs on the locomotor pattern and on cutaneous reflexes of the adult chronic spinal cat. Brain Res 514:55–67
Bras H, Jankowska E, Noga B, Skoog B (1990) Comparison of effects of various types of NA and 5-HT agonists on transmission from group II muscle afferents in the cat. Eur J Neurosci 2:1029–1039
Brocard F, Ryczko D, Fénelon K, Hatem R, Gonzales D, Auclair F, Dubuc R (2010) The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. J Neurosci 30:523–533
Buchanan JT, Grillner S (1991) 5-Hydroxytryptamine depresses reticulospinal excitatory postsynaptic potentials in motoneurons of the lamprey. Neurosci Lett 112:71–74
Chevalier G, Vacher S, Deniau JM (1984) Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behavior. Exp Brain Res 53:320–326
Cocchi M, Minuto C, Tonello L, Gabrielli F, Bernroider G, Tuszynski JA, Cappello F, Rasenick M (2017) Linoleic acid: is this the key that unlocks the quantum brain? Insights linking broken symmetries in molecular biology, mood disorders and personalistic emergentism. BMC Neurosci 18:38
Cocchi M, Minuto C, Tonello L, Tuszynski JA (2015) Connection between the linoleic acid and psychopathology: a symmetry-breaking phenomenon in the brain? Open J Depress 4:41–52
Dean P, Redgrave P, Sahibzada N, Tsuji K (1986) Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19:367–380
Deliagina TG, Beloozerova IN, Zelenin PV, Orlovsky GN (2008) Spinal and supraspinal postural networks. Brain Res Rev 57:212–221
Deliagina TG, Fagerstedt P (2000) Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs. J Neurophysiol 83:864–878
Deliagina TG, Grillner S, Orlovsky GN, Ullén F (1993) Visual input affects the response to roll in reticulospinal neurons of the lamprey. Exp Brain Res 95:421–428
Deliagina TG, Orlovsky GN, Grillner S, Wallén P (1992a) Vestibular control of swimming in lamprey. 2. Characteristics of spatial sensitivity of reticulospinal neurons. Exp Brain Res 90:489–498
Deliagina TG, Orlovsky GN, Grillner S, Wallén P (1992b) Vestibular control of swimming in lamprey. 3. Activity of vestibular afferents. Convergence of vestibular inputs on reticulospinal neurons. Exp Brain Res 90:499–507
Deliagina TG, Pavlova EL (2002) Modifications of vestibular responses of individual reticulospinal neurons in the lamprey caused by a unilateral labyrinthectomy. J Neurophysiol 87:1–14
Deliagina TG, Zelenin PV, Fagerstedt P, Grillner S, Orlovsky GN (2000) Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. J Neurophysiol 83:853–863
Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, Ullén F (2001) Lateral turns in the lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns. J Neurophysiol 86:2257–2265
Fagerstedt P, Ullén F (2001) Lateral turns in the lamprey. I. Patterns of motoneuron activity. J Neurophysiol 86:2246–2256
Fuhs MC, Touretzky DS (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26:4266–4276
Furigo IC, De Oliveira WF, De Oliveira AR, Colmoli E, Baldo MVC, Mota-Ortiz SR, Canteras NS (2010) The role of the superior colliculus in predatory hunting. Neurosci 165:1–15
Garcia-Rill E, Skinner RD (1987a) The mesencephalic locomotor region. I. Activation of a medullary projection site. Brain Res 411:1–12
Garcia-Rill E, Skinner RD (1987b) The mesencephalic locomotor region. II. Projections to reticulospinal neurons. Brain Res 411:13–20
Garcia-Rill E, Skinner RD, Gilmore SA (1981) Pallidal projections to the mesencephalic locomotor region (MLR) in the cat. Am J Anat 161:311–321
Garcia-Rill E, Skinner RD, Gilmore SA, Owings R (1983a) Connections of the mesencephalic locomotor region (MLR) II. Afferents and efferents. Brain Res Bull 10:63–71
Garcia-Rill E, Skinner RD, Jackson MB, Smith MM (1983b) Connections of the mesencephalic locomotor region (MLR) I. Substantia nigra afferents. Brain Res Bull 10:57–62
Graham Brown TG (1914) On the fundamental activity of the nervous centres: together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J Physiol (Lond) 48:18–41
Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology – the nervous system II. American Physiological Society, Bethesda, pp 1179–1236
Grillner S, Wallén P, Saitoh K, Kozlov A, Robertson B (2008) Neural bases of goal-directed locomotion in vertebrates - an overview. Brain Res Rev 57:2–12
Grillner S, Zangger P (1975) How detailed is the central pattern generation for locomotion? Brain Res 88:367–371
Guertin P, Angel MJ, Perreault M-C, McCrea DA (1995) Ankle extensor group I afferents excite extensors throughout the hindlimb during MLR-evoked fictive locomotion in the cat. J Physiol (Lond) 487:197–209
Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806
Harris-Warrick RM (1988) Chemical modulation of central pattern generators. In: Cohen AH, Rossignol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York, pp 285–332
Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953–978
Hikosaka O, Wurtz RH (1983) Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol 49:1285–1301
Hohenberg PC, Halperin BI (1977) Theory of dynamic critical phenomena. Rev Modern Phys 49(3):435–479
Hohenberg PC, Krekhov AP (2015) An introduction to the Ginzburg–Landau theory of phase transitions and nonequilibrium patterns. Phys Rep 572:1–42
Holstege G, Kuypers HGJM (1982) The anatomy of the brain stem pathways to the spinal cord in a cat. A labelled amino acid tracing study. Prog Brain Res 57:145–175
Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1988) Bistability of α-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol (Lond) 405:345–367
Huang S (2016) Where to go: breaking the symmetry in cell motility. PLoS Biol 14(5):e1002463
Iles JF, Coles SK (1991) Effects of loading on muscle activity during locomotion in rat. In: Armstrong DM, Bush BMH (eds) Locomotor neural mechanisms in arthropods and vertebrates. Manchester University Press, Manchester/New York, pp 196–201
Iles JF, Nicolopoulos-Stournaras S (1996) Fictive locomotion in the adult decerebrate rat. Exp Brain Res 109:393–398
Jankowska E, Jukes MGM, Lund S, Lundberg A (1967a) The effect of DOPA on the spinal cord: V. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand 70:369–388
Jankowska E, Jukes MGM, Lund S, Lundberg A (1967b) The effect of DOPA on the spinal cord. VI. Half-centre organization of interneurons transmitting effects from the flexor reflex afferents. Acta Physiol Scand 70:389–402
Jankowska E, Noga BR (1990) Contralaterally projecting lamina VIII interneurons in middle lumbar segments in the cat. Brain Res 535:327–330
Jensen O, Mosekilde E, Borckmans P, Dewel G (1996) Computer simulation of turing structures in the chloride-iodide-malonic acid system. Phys Scr 53:243–251
Jilkine A, Edelstein-Keshet L (2011) A comparison of mathematical models for polarization of single Eukaryotic cells in response to guided cues. PLoS Comput Biol 7(4):e1001121
Juvin L, Simmers J, Morin D (2007) Locomotor rhythmogenesis in the isolated rat spinal cord: a phase-coupled set of symmetrical flexion-extension oscillators. J Physiol (Lond) 583(1):115–128
Kausz M (1991) Arrangement of neurons in the medullary reticular formation and raphe nuclei projecting to thoracic, lumbar and sacral segments of the spinal cord in the cat. Anat Embryol 183:151–163
Kiehn O, Kjærulff O (1996) Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol 75:1472–1482
Kittel C (1971) Introduction to solid state physics, 4th edn. Wiley, New York
Kjaerulff O, Kiehn O (1997) Crossed rhythmic synaptic input to motoneurons during selective activation of the contralateral spinal locomotor network. J Neurosci 17:9433–9447
Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K, Kreitzer AC (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622–626
Kremer E, Lev-Tov A (1997) Localization of the spinal network associated with generation of hindlimb locomotion in the neonatal rat and organization of its transverse coupling system. J Neurophysiol 77:1155–1170
Kriellaars DJ, Brownstone RM, Noga BR, Jordan LM (1994) Mechanical entrainment of fictive locomotion in the decerebrate cat. J Neurophysiol 71:2074–2086
Kubicki M, McCarley R, Li R, Bowerman B (2010) Symmetry breaking in biology. Cold Spring Harb Perspect Biol 2(3):a003475. doi:10.1101/cshperspect.a003475
Lafreniere-Roula M, McCrea DA (2005) Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provide clues to the organization of the mammalian central pattern generator. J Neurophysiol 94:1120–1132
Li R, Bowerman B (2010) Symmetry breaking in biology. Cold Spring Harb Perspect Biol 2(3):a003475. https://doi.org/10.1101/cshperspect.a003475
Lundberg A (1981) Half-centres revisited. In: Szentagothai J, Palkovits M, Hamori J (eds) Regulatory functions of the CNS. Motion and organization principles. Advances in physiological sciences vol. 1. Pergamon Press, Akademiai Kiado, Budapest, pp 155–167
McCrea DA, Rybak IA (2007) Modeling the mammalian locomotor CPG: insights from mistakes and perturbations. Prog Brain Res 165:235–253
McCrea DA, Rybak IA (2008) Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57:134–146
McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7(8):663–678
Mergner T, Becker W (2003) A modeling approach to the human spatial orientation system. Ann N Y Acad Sci 1004:303–315
Merrywest SD, McDearmid JR, Kjaerulff O, Kiehn O, Sillar KT (2003) Mechanisms underlying the noradrenergic modulation of longitudinal coordination during swimming in Xenopus laevis tadpoles. Eur J Neurosci 17:1013–1022
Miller DM, DeMayo WM, Bourdages GH, Wittman SR, Yates BJ, McCall AA (2017) Neurons in the pontomedullary reticular formation receive convergin inpts from the hindlimb and labyrinth. Exp Brain Res 235:1195–1207
Mnyukh Y (2012) Ferromagnetic state and phase transitions. Am J Cond Mat Phys 2(5):109–115
Mullins D (2009) Symmetry breaking in biology. Cold Spring Harb Perspect Biol 2:a003392
Munro E, Bowerman B (2009) Cellular symmetry breaking during C. elegans development. Cold Spring Harb Perspect Biol 1:a003400
Murray JD (1989) Mathematical biology. Springer, Heidelberg
Noga BR, Fortier PA, Kriellaars DJ, Dai X, Detillieux GR, Jordan LM (1995) Field potential mapping of neurons in the lumbar spinal cord activated following stimulation of the mesencephalic locomotor region. J Neurosci 15:2203–2217
Noga BR, Johnson DMG, Riesgo MI, Pinzon A (2009) Locomotor-activated neurons of the cat. I. Serotonergic innervation and co-localization of 5-HT7, 5-HT2A and 5-HT1A receptors in the thoraco-lumbar spinal cord. J Neurophysiol 102:1560–1576. PMID: 19571190 937
Noga BR, Johnson DMG, Riesgo MI, Pinzon A (2011) Locomotor-activated neurons of the cat. II. Noradrenergic innervation and co-localization of NAα1A and NAα2B receptors in the thoraco-lumbar spinal cord. J Neurophysiol 105:1835–1849
Noga BR, Kettler J, Jordan LM (1988) Locomotion produced in mesencephalic cats by injections of putative transmitter substances and antagonists into the medial reticular formation and the pontomedullary locomotor strip. J Neurosci 8:2074–2086
Noga BR, Kriellaars DJ, Brownstone RM, Jordan LM (2003) Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region. J Neurophysiol 90:1464–1478. doi:10.1152/jn.00034.2003
Noga BR, Kriellaars DJ, Jordan LM (1991) The effect of selective brainstem or spinal cord lesions on treadmill locomotion evoked by stimulation of the mesencephalic or pontomedullary locomotor regions. J Neurosci 11:1691–1700
Noga BR, Opris I (2017) The hierarchical circuit for executive control of movement. (Chapter 5). In: Opris I, Casanova MF Physics of the mind and brain disorders: integrated neural circuits supporting the emergence of mind. Springer Series in Cognitive and Neural Systems, New York, NY. ISBN 978-3-319-29674-6
O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109
Opris I (2013) Inter-laminar microcircuits across the neocortex: repair and augmentation. Front Syst Neurosci 7:80
Opris I, Casanova MF (2014) Prefrontal cortical minicolumn: from executive control to disrupted cognitive processing. Brain 137(7):1863–1875. doi:10.1093/brain/awt359
Opris I, Fuqua JL, Huettl PF, Gerhardt GA, Berger TW, Hampson RE et al (2012b) Closing the loop in primate prefrontal cortex: inter-laminar processing. Front Neural Circ 6:88
Opris I, Hampson RE, Gerhardt GA, Berger TW, Deadwyler SA (2012a) Columnar processing in primate pFC: evidence for executive control microcircuits. J Cogn Neurosci 24:2334–2347
Opris I, Hampson RE, Stanford TR, Gerhardt GA, Deadwyler SA (2011) Neural activity in frontal cortical cell layers: evidence for columnar sensorimotor processing. J Cogn Neurosci 23:1507–1521
Opris I, Santos LM, Song D, Gerhardt GA, Berger TW, Hampson RE et al (2013) Prefrontal cortical microcircuits bind perception to executive control. Sci Rep 3:2285
Orlovsky GN (1969) Electrical activity in the brainstem and descending pathways in guided locomotion. Fiziol Zh (SSSR) 55:437–444
Orlovsky GN (1970a) Connexions of the reticulo-spinal neurons with the “locomotor sections” of the brainstem. Biophysics 15:178–186
Orlovsky GN (1970b) Work of the reticulospinal neurons during locomotion. Biophysics 15:761–771
Pavlova EL, Popova LB, Orlovsky GN, Deliagina TF (2004) Vestibular compensation in lampreys: restoration of symmetry in reticulospinal commands. J Exp Biol 207:4595–5603
Perreault M-C, Angel MJ, Guertin P, McCrea DA (1995) Effects of stimulation of hindlimb flexor group II muscle afferents during fictive locomotion. J Physiol 487:211–220
Perreault M-C, Drew T, Rossignol S (1993) Activity of medullary reticulospinal neurons during fictive locomotion. J Neurophysiol 69:2232–2247
Peterson BW, Abzug C (1975) Properties of projections from vestibular nuclei to medial reticular formation in the cat. J Neurophysiol 38:1421–1435
Roseberry TK, Lee AM, Lalive AL, Wilbrecht L, Bonci A, Kreitzer AC (2016) Cell-type-specific control of brainstem locomotor circuits by basal ganglia. Cell 164:526–537
Rybak IA, Stecina K, Shevtsova NA, McCrea DA (2006) Modelling spinal circuitry involved in locomotor pattern generation: insights from the effects of afferent stimulation. J Physiol 577:641–658
Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870–3896
Spardy LE, Markin SN, Shevtsova NA, Prilutsky BI, Rybak IA, Rubin JE (2011b) A dynamical systems analysis of afferent control in a neuromechanical model of locomotion: I. Rhythm generation. J Neural Eng 8:065003
Spardy LE, Markin SN, Shevtsova NA, Prilutsky BI, Rybak IA, Rubin JE (2011a) A dynamical systems analysis of afferent control in a neuromechanical model of locomotion: II. Phase asymmetry. J Neural Eng 8:065004
Stecina K, Quevedo J, McCrea DA (2005) Parallel reflex pathways from flexor muscle afferents evoking resetting and flexion-enhancement during fictive locomotion in the cat. J Physiol 569:275–290
Steeves JD, Jordan LM (1980) Localization of a descending pathway in the spinal cord which is necessary for controlled treadmill locomotion. Neurosci Lett 20(283):288
Steeves JD, Jordan LM (1984) Autoradiographic demonstration of the projections from the mesencephalic locomotor region. Brain Res 307:263–276
Swindale NV (1980) A model for the formation of ocular dominance stripes. Proc R Soc Lond B Biol Sci 208:243–264
Takakusaki K (2017) Functional neuroanatomy for posture and gait control. J Mov Disord 10:1–17
Tohyama M, Sakai K, Salvert D, Touret M, Jouvet M (1979) Spinal projections from the lower brain stem in the cat as demonstrated by the horseradish peroxidase technique. I. Origins of the reticulospinal tracts and their funicular trajectories. Brain Res 173:383–403
Turing AM (1953) The chemical basis of morphogenesis. Phil Trans R Soc B 237:37–72. Reprinted in Bull Math Biol 52, 153–197 (1990)
Van der Gucht J, Sykes C (2009) Physical model of cellular symmetry breaking. Cold Spring Harb Perspect Biol 1:a001909
Wang X-J (2002) Probabilistic decision making by slow reverberation in cortical circuits. Neuron 36:955–968
Wang XJ (2012) Neural dynamics and circuit mechanisms of decision-making. Curr Opin Neurobiol 22:1039–1046
Wannier T, Deliagina TG, Orlovsky GN, Grillner S (1998) Differential effects of the reticulospinal system on locomotion in lamprey. J Neurophysiol 80:103–112
Whelan P, Bonnot A, O’Donovan MJ (2000) Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J Neurophysiol 84:2821–2933
Wilson KG, Kogut J (1974) The renormalization group and the ϵ expansion. Phys Rep 12:75–199
Wimmer K, Nykamp DQ, Constantinidis C, Compte A (2014) Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory. Nat Neurosci 17:431–439
Yakovenko S, McCrea DA, Stecina K, Prochazka A (2005) Control of locomotor cycle durations. J Neurophysiol 94:1057–1065
Yamaguchi T (1987) Monopodal fictive locomotion evoked by cervical cord stimulation in decerebrate cats. Neurosci Lett 74(69):74
Yoshimura M, Furue H (2006) Mechanisms for the anti-nociceptive actions of the descending noradrenergic and serotonergic systems in the spinal cord. J Pharmacol Sci 101:107–117
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Noga, B.R., Opris, I. (2017). From Symmetry to Symmetry-Breaking in Locomotion. In: Opris, I., Casanova, M.F. (eds) The Physics of the Mind and Brain Disorders. Springer Series in Cognitive and Neural Systems, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-319-29674-6_7
Download citation
DOI: https://doi.org/10.1007/978-3-319-29674-6_7
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-29672-2
Online ISBN: 978-3-319-29674-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)