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Neural responses in multiple basal ganglia regions during spontaneous and treadmill locomotion tasks in rats

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Abstract

To investigate the role of basal ganglia in locomotion, a multiple-channel, single-unit recording technique was used to record neural activity simultaneously in the dorsal lateral striatum (STR), globus pallidus (GP), subthalamic nucleus (STN) and substantia nigra pars reticulata (SNr) during spontaneous and treadmill locomotion tasks in freely moving rats. Active and quiescent phases appeared alternately in a spontaneous movement session that lasted 60 min. Principal component analysis of the ensemble neural activity from each region revealed a close correlation with spontaneous motor activity. Most of the neurons in these four basal ganglia areas increased their firing rates during the active phase. In the treadmill locomotion task, the firing rates of neurons in all recording areas, especially in the STN, increased significantly during locomotion. In addition, neural responses related to tone cue, initiation and termination of treadmill were observed in a subset of neurons in each basal ganglia region. Detailed video analysis revealed a limb movement related neural firing, predominantly in the STR and the GP, during treadmill walking. However, the proportion of neurons exhibiting limb movement related firing was significantly greater only in the STR. A few neurons in the STR (4.8%) and the GP (3.4%) discharged in an oscillatory pattern during treadmill walking, and the oscillatory frequency was similar to the frequency of the step cycle. This study demonstrates a variety of neural responses in the major basal ganglia regions during spontaneous and forced locomotion. General activation of all major basal ganglia regions during locomotion is more likely to provide a dynamic background for cortical signal processing rather than to directly control precise movements. Implications of these findings in the model of basal ganglia organization are discussed.

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References

  • Alexander GE, Crutcher MD (1990a) Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J Neurophysiol 64:133–150

    CAS  PubMed  Google Scholar 

  • Alexander GE, Crutcher MD (1990b) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266–271

    CAS  PubMed  Google Scholar 

  • Alexander GE, Crutcher MD, Delong MR (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, ‘prefrontal’ and ‘limbic’ functions. Prog Brain Res 85:119–146

    PubMed  Google Scholar 

  • Allers KA, Kreiss DS, Walters JR (2000) Multisecond oscillations in the subthalamic nucleus: effects of apomorphine and dopamine cell lesion. Synapse 38:38–50

    Article  CAS  PubMed  Google Scholar 

  • Anderson ME, Horak FB (1985) Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information. J Neurophysiol 54:433–448

    CAS  PubMed  Google Scholar 

  • Apicella P, Scarnati E, Ljungberg T, Schultz W (1992) Neuronal activity in monkey striatum related to the expectation of predictable environmental events. J Neurophysiol 68:945–960

    CAS  PubMed  Google Scholar 

  • Basso MA, Wurtz RH (2002) Neuronal activity in substantia nigra pars reticulata during target selection. J Neurosci 22:1883–1894

    CAS  PubMed  Google Scholar 

  • Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, Benabid AL (2000) Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience 99:289–295

    Article  CAS  PubMed  Google Scholar 

  • Bergman H, Wichmann T, Karmon B, DeLong MR (1994) Neuronal activity in the MPTP model of parkinsonism: the primate subthalamic nucleus II. J Neurophysiol 72:507–520

    CAS  PubMed  Google Scholar 

  • Burbaud P, Gross C, Benazzouz A, Coussemacq M, Bioulac B (1995) Reduction of apomorphine-induced rotational behaviour by subthalamic lesion in 6-OHDA lesioned rats is associated with a normalization of firing rate and discharge pattern of pars reticulata neurons. Exp Brain Res 105:48–58

    CAS  PubMed  Google Scholar 

  • Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA (1988) Somatosensory inputs to the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 458:53–64

    Article  CAS  PubMed  Google Scholar 

  • Chapin JK, Loeb GE, Woodward DJ (1980) A simple technique for determination of footfall patterns of animals during treadmill locomotion. J Neurosci Methods 2:97–102

    Article  CAS  PubMed  Google Scholar 

  • Cho J, West MO (1997) Distributions of single neurons related to body parts in the lateral striatum of the rat. Brain Res 756:241–246

    Article  CAS  PubMed  Google Scholar 

  • Cohen AH, Gans C (1975) Muscle activity in rat locomotion: movement analysis and electromyography of the flexors and extensors of the elbow. J Morphol 146:177–196

    CAS  PubMed  Google Scholar 

  • Crutcher MD, DeLong MR (1984a) Single cell studies of the primate putamen II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53:244–258

    Google Scholar 

  • Crutcher MD, DeLong MR (1984b) Single cell studies of the primate putamen I. Functional organization. Exp Brain Res 53:233–243

    CAS  PubMed  Google Scholar 

  • DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285

    CAS  PubMed  Google Scholar 

  • DeLong MR, Crutcher MD, Georgopoulos AP (1983) Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J Neurosci 3:1599–1606

    CAS  PubMed  Google Scholar 

  • Deniau JM, Thierry AM (1997) Anatomical segregation of information processing in the rat substantia nigra pars reticulata. Adv Neurol 74:83–96

    CAS  PubMed  Google Scholar 

  • Dolbakyan E, Hernandez-Mesa N, Bures J (1977) Skilled forelimb movements and unit activity in motor cortex and caudate nucleus in rats. Neuroscience 2:73–80

    Article  CAS  PubMed  Google Scholar 

  • Donoghue JP, Herkenham M (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 365:397–403

    CAS  PubMed  Google Scholar 

  • Ebrahimi A, Pochet R, Roger M (1992) Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat. Neurosci Res 14:39–60

    CAS  PubMed  Google Scholar 

  • Ericson E, Samuelsson J, Ahlenius S (1991) Photocell measurements of rat motor activity. A contribution to sensitivity and variation in behavioral observations J Pharmacol Methods 25:111–122

    Article  CAS  Google Scholar 

  • Fujimoto K, Kita H (1992) Responses of rat substantia-nigra pars-reticulata units to cortical stimulation. Neurosci Lett 142:105–109

    Article  CAS  PubMed  Google Scholar 

  • Gardiner TW, Kitai ST (1992) Single-unit activity in the globus pallidus and neostriatum of the rat during performance of a trained head movement. Exp Brain Res 88:517–530

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP, DeLong MR, Crutcher MD (1983) Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J Neurosci 3:1586–1598

    CAS  PubMed  Google Scholar 

  • Grofova I, Deniau JM, Kitai ST (1982) Morphology of the substantia nigra pars reticulata projection neurons intracellularly labeled with HRP. J Comp Neurol 208:352–368

    CAS  PubMed  Google Scholar 

  • Gulley JM, Kuwajima M, Mayhill E, Rebec GV (1999) Behavior-related changes in the activity of substantia nigra pars reticulata neurons in freely moving rats. Brain Res 845:68–76

    Article  CAS  PubMed  Google Scholar 

  • Haracz JL, Tschanz JT, Greenberg J, Rebec GV (1989) Amphetamine-induced excitations predominate in single neostriatal neurons showing motor-related activity. Brain Res 489:365–368

    Article  CAS  PubMed  Google Scholar 

  • Hikosaka O, Wurtz RH (1983) Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J Neurophysiol 49:1230–1253

    CAS  PubMed  Google Scholar 

  • Hutchison WD, Lozano AM, Tasker RR, Lang AE, Dostrovsky JO (1997) Identification and characterization of neurons with tremor-frequency activity in human globus pallidus. Exp Brain Res 113:557–563

    CAS  PubMed  Google Scholar 

  • Kita H, Kitai ST (1991) Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res 564:296–305

    Article  CAS  PubMed  Google Scholar 

  • Kitai ST, Denian JM (1981) Cortical input to the subthalamus: intracellular analysis. Brain Res 214:411–415

    Article  CAS  PubMed  Google Scholar 

  • Kolomiets BP, Deniau JM, Mailly P, Menetrey A, Glowinski J, Thierry AM (2001) Segregation and convergence of information flow through the cortico-subthalamic pathways. J Neurosci 21:5764–5772

    CAS  PubMed  Google Scholar 

  • Maurice N, Deniau JM, Glowinski J, Thierry AM (1999) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the cortico-nigral circuits. J Neurosci 19:4674–4681

    CAS  PubMed  Google Scholar 

  • McGeorge AJ, Faull RL (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503–537

    CAS  PubMed  Google Scholar 

  • Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425

    PubMed  Google Scholar 

  • Mink JW, Thach WT (1991) Basal ganglia motor control. III. Pallidal ablation: normal reaction time, muscle cocontraction, and slow movement. J Neurophysiol 65:330–351

    CAS  PubMed  Google Scholar 

  • Mitchell SJ, Richardson RT, Baker FH, DeLong MR (1987) The primate globus pallidus: neuronal activity related to direction of movement. Exp Brain Res 68:491–505

    CAS  PubMed  Google Scholar 

  • Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res 43:111–117

    Article  PubMed  Google Scholar 

  • Obeso JA, Rodriquez MC, DeLong MR (1997) Pathophysiology of the basal ganglia: a critical review. Adv Neurol 74:3–18

    CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, San Diego

  • Rebec GV, White IM, Puotz JK (1997) Responses of neurons in dorsal striatum during amphetamine-induced focused stereotypy. Psychopharmacology 130:343–351

    Article  CAS  PubMed  Google Scholar 

  • Romo R, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. III. Neuronal activity in the supplementary motor area. Exp Brain Res 91:396–407

    CAS  PubMed  Google Scholar 

  • Ryan LJ, Clark KB (1991) The role of the subthalamic nucleus in the response of globus-pallidus neurons to stimulation of the prelimbic and agranular frontal cortices in rats. Exp Brain Res 86:641–651

    CAS  PubMed  Google Scholar 

  • Sato M, Hikosaka O (2002) Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement. J Neurosci 22:2363–2373

    CAS  PubMed  Google Scholar 

  • Schultz W, Romo R (1988) Neuronal activity in the monkey striatum during the initiation of movements. Exp Brain Res 71:431–436

    CAS  PubMed  Google Scholar 

  • Schultz W, Romo R (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp Brain Res 91:363–384

    CAS  PubMed  Google Scholar 

  • Steriade M (1999) Coherent oscillations and short-term plasticity in corticothalamic networks. Trends Neurosci 22:337–345

    CAS  PubMed  Google Scholar 

  • Trimmel M, Mikowitsch A, Grollknapp E, Haider M (1990) Occurrence of infraslow potential oscillations in relation to task, ability to concentrate and intelligence. Int J Psychophysiol 9:167–170

    Article  CAS  PubMed  Google Scholar 

  • Trytek ES, White IM, Schroeder DM, Heidenreich BA, Rebec GV (1996) Localization of motor- and nonmotor-related neurons within the matrix-striosome organization of rat striatum. Brain Res 707:221–227

    Article  CAS  PubMed  Google Scholar 

  • Wannier T, Liu J, Morel A, Jouffrais C, Rouiller EM (2002) Neuronal activity in primate striatum and pallidum related to bimanual motor actions. Neuroreport 13:143–147

    PubMed  Google Scholar 

  • West MO, Carelli RM, Pomerantz M, Cohen SM, Gardner JP, Chapin JK, Woodward DJ (1990) A region in the dorsolateral striatum of the rat exhibiting single-unit correlations with specific locomotor limb movements. J Neurophysiol 64:1233–1246

    CAS  PubMed  Google Scholar 

  • West MO, Peoples LL, Michael AJ, Chapin JK, Woodward DJ (1997) Low-dose amphetamine elevates movement-related firing of rat striatal neurons. Brain Res 745:331–335

    CAS  PubMed  Google Scholar 

  • White IM, Rebec GV (1993) Responses of rat striatal neurons during performance of a lever-release version of the conditioned avoidance response task. Brain Res 616:71–82

    Article  CAS  PubMed  Google Scholar 

  • Wichmann T, Bergman H, DeLong MR (1994a) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 400:521–530

    Google Scholar 

  • Wichmann T, Bergman H, DeLong MR (1994b) The primate subthalamic nucleus. I. Functional properties in intact animals. J Neurophysiol 72:494–506

    CAS  PubMed  Google Scholar 

  • Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR (1999) Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp Brain Res 125:397–409

    Article  CAS  PubMed  Google Scholar 

  • Wichmann T, Kliem MA, Soares J (2002) Slow oscillatory discharge in the primate basal ganglia. J Neurophysiol 87:1145–1148

    PubMed  Google Scholar 

  • Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13:3802–3817

    CAS  PubMed  Google Scholar 

  • Wilson CJ, Chang HT, Kitai ST (1982) Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra. Exp Brain Res 45:157–167

    CAS  PubMed  Google Scholar 

  • Wise SP, Jones EG (1977) Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol 175:129–157

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by NIH grants NS-43441 and NS-45826 to JYC and NS-19608 and AA-10337 to DJW. We thank Ms. Susan Giegel for editing the manuscript.

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  1. Department of Physiology and Pharmacology, School of Medicine, Wake Forest University, Winston-Salem, NC 27157, USA

    L. H. Shi, F. Luo, D. J. Woodward & J. Y. Chang

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  1. L. H. Shi
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  2. F. Luo
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  3. D. J. Woodward
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  4. J. Y. Chang
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Correspondence to J. Y. Chang.

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Shi, L.H., Luo, F., Woodward, D.J. et al. Neural responses in multiple basal ganglia regions during spontaneous and treadmill locomotion tasks in rats. Exp Brain Res 157, 303–314 (2004). https://doi.org/10.1007/s00221-004-1844-y

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  • DOI: https://doi.org/10.1007/s00221-004-1844-y

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