Motor outputs from the primate reticular formation to shoulder muscles as revealed by stimulus-triggered averaging.

The motor output of the medial pontomedullary reticular formation (mPMRF) was investigated using stimulus-triggered averaging (StimulusTA) of EMG responses from proximal arm and shoulder muscles in awake, behaving monkeys (M. fascicularis). Muscles studied on the side ipsilateral (i) to stimulation were biceps (iBic), triceps (iTri), anterior deltoid (iADlt), posterior deltoid (iPDlt), and latissimus dorsi (iLat). The upper and middle trapezius were studied on the ipsilateral and contralateral (c) side (iUTr, cUTr, iMTr, cMTr). Of 133 sites tested, 97 (73%) produced a poststimulus effect (PStE) in one or more muscles; on average, 38% of the sampled muscles responded per effective site. For responses that were observed in the arm and shoulder, poststimulus facilitation (PStF) was prevalent for the flexors, iBic (8 responses, 100% PStF) and iADlt (13 responses, 77% PStF), and poststimulus suppression (PStS) was prevalent for the extensors, iTri (22 responses, 96% PStS) and iLat (16 responses, 81% PStS). For trapezius muscles, PStS of upper trapezius (iUTr, 49 responses, 73% PStS) and PStF of middle trapezius (iMTr, 22 responses, 64% PStF) were prevalent ipsilaterally, and PStS of middle trapezius (cMTr, 6 responses, 67% PStS) and PStF of upper trapezius (cUTr, 46 responses, 83% PStS) were prevalent contralaterally. Onset latencies were significantly earlier for PStF (7.0 +/- 2.2 ms) than for PStS (8.6 +/- 2.0 ms). At several sites, extremely strong PStF was evoked in iUTr, even though PStS was most common for this muscle. The anatomical antagonists iBic/iTri were affected reciprocally when both responded. The bilateral muscle pair iUTr/cUTr demonstrated various combinations of effects, but cUTr PStF with iUTr PStS was prevalent. Overall, the results are consistent with data from the cat and show that outputs from the mPMRF can facilitate or suppress activity in muscles involved in reaching; responses that would contribute to flexion of the ipsilateral arm were prevalent.

[1]  K. Takakusaki,et al.  Multi‐segmental innervation of single pontine reticulospinal axons in the cervico‐thoracic region of the cat: Anterograde PHA‐L tracing study , 1997, The Journal of comparative neurology.

[2]  W. Rymer,et al.  Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. , 1995, Brain : a journal of neurology.

[3]  H. Kuypers,et al.  Distribution of corticospinal neurons with collaterals to lower brain stem reticular formation in cat , 2004, Experimental Brain Research.

[4]  S. Sasaki.  Axonal branching and termination of cervical reticulospinal neurons in the cat brachial segments , 1997, Neuroscience Letters.

[5]  A. M. Degtyarenko,et al.  Disynaptic vestibulospinal and reticulospinal excitation in cat lumbosacral motoneurons: modulation during fictive locomotion , 1996, Experimental Brain Research.

[6]  P. Cheney,et al.  Characteristics of corticomotoneuronal postspike facilitation and reciprocal suppression of EMG activity in the monkey. , 1985, Journal of neurophysiology.

[7]  P. Cheney,et al.  Facilitation and suppression of wrist and digit muscles from single rubromotoneuronal cells in the awake monkey. , 1991, Journal of neurophysiology.

[8]  Trevor Drew,et al.  Strategies for the integration of posture and movement during reaching in the cat. , 2003, Journal of neurophysiology.

[9]  E. Fetz,et al.  Control of forelimb muscle activity by populations of corticomotoneuronal and rubromotoneuronal cells. , 1989, Progress in brain research.

[10]  Response of pontomedullary reticulospinal neurons to vestibular stimuli in vertical planes. Role in vertical vestibulospinal reflexes of the decerebrate cat. , 1992, Journal of neurophysiology.

[11]  T. Drew,et al.  Corticoreticular pathways in the cat. I. Projection patterns and collaterization. , 1998, Journal of neurophysiology.

[12]  P. Cheney,et al.  Distribution and characteristics of poststimulus effects in proximal and distal forelimb muscles from red nucleus in the monkey. , 1998, Journal of neurophysiology.

[13]  J. Buford.  A Preliminary Description of Movement-Related and Preparatory Activity in Primate Reticular Formation (Motor Function) , 1996 .

[14]  J. Tanji.  Sequential organization of multiple movements: involvement of cortical motor areas. , 2001, Annual review of neuroscience.

[15]  M. Taussig.  The Nervous System , 1991 .

[16]  P. Cheney,et al.  Consistent Features in the Forelimb Representation of Primary Motor Cortex in Rhesus Macaques , 2001, The Journal of Neuroscience.

[17]  S. Rossignol,et al.  Functional organization within the medullary reticular formation of intact unanesthetized cat. II. Electromyographic activity evoked by microstimulation. , 1990, Journal of neurophysiology.

[18]  B. W. Peterson,et al.  Reticulospinal connections with limb and axial motoneurons , 1979, Experimental Brain Research.

[19]  E. Fetz,et al.  Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimuli in primates: evidence for functional groups of CM cells. , 1985, Journal of neurophysiology.

[20]  B. L. Clarke,et al.  Walking on a level surface , 1961 .

[21]  B W Peterson,et al.  Reticulospinal projections to spinal motor nuclei. , 1979, Annual review of physiology.

[22]  E. Fetz,et al.  Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. , 1980, Journal of neurophysiology.

[23]  Trevor Drew,et al.  Locomotor role of the corticoreticular-reticulospinal-spinal interneuronal system. , 2004, Progress in brain research.

[24]  A R Gibson,et al.  Construction of a reach-to-grasp. , 2007, Novartis Foundation symposium.

[25]  S. Rossignol,et al.  Phase-dependent responses evoked in limb muscles by stimulation of medullary reticular formation during locomotion in thalamic cats. , 1984, Journal of neurophysiology.

[26]  K Matsuyama,et al.  Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. I. Walking on a level surface. , 2000, Journal of neurophysiology.

[27]  T. Drew.  Functional organization within the medullary reticular formation of the intact unanesthetized cat. III. Microstimulation during locomotion. , 1991, Journal of neurophysiology.

[28]  Extrapyramidal Control of Primate Motoneurons , 1973 .

[29]  M. Ito,et al.  Interaction between the horizontal vestibulo-ocular reflex and optokinetic response in rabbits , 1979, Experimental Brain Research.

[30]  Elzbieta Jankowska,et al.  Neuronal Basis of Crossed Actions from the Reticular Formation on Feline Hindlimb Motoneurons , 2003, The Journal of Neuroscience.

[31]  P. Cheney,et al.  Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. , 1998, Journal of neurophysiology.

[32]  K. Pearson,et al.  Enhancement and Resetting of Locomotor Activity by Muscle Afferentsa , 1998, Annals of the New York Academy of Sciences.

[33]  S. Sasaki,et al.  Input-output organization of reticulospinal neurones, with special reference to connexions with dorsal neck motoneurones in the cat , 2004, Experimental Brain Research.

[34]  S. Rossignol,et al.  Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. , 1986, Journal of neurophysiology.

[35]  H. Magoun,et al.  Brain stem facilitation of cortical motor response. , 1946, Journal of neurophysiology.

[36]  H. Freund,et al.  Lesions of premotor cortex in man. , 1985, Brain : a journal of neurology.

[37]  J. Desmedt.  Human reflexes; pathophysiology of motor systems; methodology of human reflexes , 1973 .

[38]  Douglas M. Bowden,et al.  BrainInfo: An Online Interactive Brain Atlas and Nomenclature , 2003 .

[39]  S. Mori,et al.  Morphology of single pontine reticulospinal axons in the lumbar enlargement of the cat: A study using the anterograde tracer PHA‐L , 1999, The Journal of comparative neurology.

[40]  W. Chambers,et al.  Control of posture by reticular formation and cerebellum in the intract, anesthetized and unanesthetized and in the decerebrated cat. , 1953, The American journal of physiology.

[41]  D. Robinson,et al.  Subcortical contributions to head movements in macaques. I. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus. , 1994, Journal of neurophysiology.

[42]  H. Magoun,et al.  An inhibitory mechanism in the bulbar reticular formation. , 1946, Journal of neurophysiology.

[43]  S. Mori,et al.  Medullary reticulospinal tract mediating the generalized motor inhibition in cats: Parallel inhibitory mechanisms acting on motoneurons and on interneuronal transmission in reflex pathways , 2001, Neuroscience.

[44]  P. Cheney.  Response of rubromotoneuronal cells identified by spike-triggered averaging of EMG activity in awake monkeys , 1980, Neuroscience Letters.

[45]  Paul D Cheney,et al.  Chronic recording of EMG activity from large numbers of forelimb muscles in awake macaque monkeys , 2000, Journal of Neuroscience Methods.

[46]  S. Sasaki.  Direct connection of the nucleus reticularis gigantocellularis neurons with neck motoneurons in cats , 1999, Experimental Brain Research.

[47]  H. Forssberg.  Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. , 1979, Journal of neurophysiology.

[48]  F. Plum.  Handbook of Physiology. , 1960 .

[49]  W. Cowan,et al.  A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[50]  H. Kuypers,et al.  Brainstem projections to spinal motoneurons: An update , 1987, Neuroscience.

[51]  B. Betts,et al.  Telemetered EMG of fast and slow muscles in cats , 1976, Brain Research.

[52]  B. Alstermark,et al.  Monosynaptic raphespinal and reticulospinal projection to forelimb motoneurones in cats , 1987, Neuroscience Letters.

[53]  B. W. Peterson,et al.  Patterns of projection and branching of reticulospinal neurons , 1975, Experimental Brain Research.

[54]  H. Kuypers,et al.  Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in monkey (Macaca fascicularis) , 2004, Experimental Brain Research.

[55]  Sabine Dannenberg,et al.  Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching , 1997, Experimental Brain Research.

[56]  A. I. Shapovalov.  Extrapyramidal monosynaptic and disynaptic control of mammalian alpha-motoneurons. , 1972, Brain research.

[57]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[58]  K Matsuyama,et al.  Vestibulospinal and reticulospinal neuronal activity during locomotion in the intact cat. II. Walking on an inclined plane. , 2000, Journal of neurophysiology.

[59]  Effects on wrist and digit muscle activity from microstimuli applied at the sites of rubromotoneuronal cells in primates. , 1991, Journal of neurophysiology.

[60]  S. Rossignol,et al.  Functional organization within the medullary reticular formation of intact unanesthetized cat. I. Movements evoked by microstimulation. , 1990, Journal of neurophysiology.

[61]  J M SPRAGUE,et al.  Regulation of posture in intact and decerebrate cat. I. Cerebellum, reticular formation, vestibular nuclei. , 1953, Journal of neurophysiology.