Evidence for reticulospinal contributions to coordinated finger movements in humans.

The reticulospinal tract was recently shown to have synaptic connections to the intrinsic muscles of the fingers in nonhuman primates, indicating it may contribute to hand function long thought to be controlled exclusively through corticospinal pathways. Our objective was to obtain evidence supporting the hypothesis that these same anatomical connections exist in humans. startReact, an involuntary release of a planned movement via the startle reflex, provides a noninvasive means to examine the reticulospinal tract in humans. We found that startReact was triggered during coordinated grasp but not individuated finger movements. This result suggests that the reticulospinal tract does have connections to the intrinsic muscles of the fingers in humans but its functional role is limited to coordinated movement of the whole hand. These results do not diminish the well-established role of corticospinal pathways in the control of hand movement. Indeed, they cement the significance of corticospinal pathways in individuated finger movement control. Still, these results point to an updated and expanded view of distal hand control where reticulospinal and corticospinal pathways work in parallel to generate a large repertoire of diverse, coordinated movement in the hand. Finally, the presence of reticulospinal pathways to the muscles of the hand makes this pathway an attractive therapeutic target for clinical populations where the corticospinal tract is absent or injured.

[1]  J. Brobeck The Integrative Action of the Nervous System , 1948, The Yale Journal of Biology and Medicine.

[2]  P. Nathan,et al.  Long descending tracts in man. I. Review of present knowledge. , 1955, Brain : a journal of neurology.

[3]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. , 1968, Brain : a journal of neurology.

[4]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathways. , 1968, Brain : a journal of neurology.

[5]  D L Kohfeld,et al.  Effects of the intensity of auditory and visual ready signals on simple reaction time. , 1969, Journal of experimental psychology.

[6]  D L Kohfeld,et al.  Simple reaction time as a function of stimulus intensity in decibels of light and sound. , 1971, Journal of experimental psychology.

[7]  G. Hammond Lesions of pontine and medullary reticular formation and prestimulus inhibition of the acoustic startle reaction in rats. , 1973, Physiology & behavior.

[8]  P. Groves,et al.  Brain stem pathways, cortical modulation, and habituation of the acoustic startle response. , 1974, Behavioral biology.

[9]  M. Davis,et al.  Plasticity of the acoustic startle response in the acutely decerebrate rat. , 1977, Journal of comparative and physiological psychology.

[10]  H. Kuypers,et al.  Anatomy of descending pathways to the spinal cord , 1982 .

[11]  M. Davis,et al.  A primary acoustic startle circuit: lesion and stimulation studies , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  P. Nathan,et al.  The rubrospinal and central tegmental tracts in man. , 1982, Brain : a journal of neurology.

[13]  S. Mori Integration of posture and locomotion in acute decerebrate cats and in awake, freely moving cats , 1987, Progress in Neurobiology.

[14]  Y. Ohta,et al.  Site-specific postural and locomotor changes evoked in awake, freely moving intact cats by stimulating the brainstem , 1989, Brain Research.

[15]  J C Rothwell,et al.  New observations on the normal auditory startle reflex in man. , 1991, Brain : a journal of neurology.

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

[17]  Lemon Rn,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993 .

[18]  R N Lemon,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993, Experimental physiology.

[19]  J. Valls-Solé,et al.  Reaction time and acoustic startle in normal human subjects , 1995, Neuroscience Letters.

[20]  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.

[21]  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.

[22]  J. Rothwell,et al.  Patterned ballistic movements triggered by a startle in healthy humans , 1999, The Journal of physiology.

[23]  Sabine Meunier,et al.  Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. , 2003, Brain : a journal of neurology.

[24]  M. Rushworth,et al.  The left parietal and premotor cortices: motor attention and selection , 2003, NeuroImage.

[25]  T. Drew,et al.  Cortical and brainstem control of locomotion. , 2004, Progress in brain research.

[26]  S. Sasaki,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

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

[28]  Adam G. Davidson,et al.  Movement-related and preparatory activity in the reticulospinal system of the monkey , 2004, Experimental Brain Research.

[29]  J. Colebatch,et al.  The acoustic startle reflex in ischemic stroke , 2004, Neurology.

[30]  S. Sasaki,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[31]  Ian M Franks,et al.  Prepared Movements Are Elicited Early by Startle , 2004, Journal of motor behavior.

[32]  Marc H Schieber,et al.  Motor Control: Basic Units of Cortical Output? , 2004, Current Biology.

[33]  Anthony N. Carlsen,et al.  Can prepared responses be stored subcortically? , 2004, Experimental Brain Research.

[34]  E. Sybirska,et al.  Integration in descending motor pathways controlling the forelimb in the cat , 2004, Experimental Brain Research.

[35]  John W Krakauer,et al.  Arm function after stroke: from physiology to recovery. , 2005, Seminars in neurology.

[36]  Marc H Schieber,et al.  Bilateral Spike-Triggered Average Effects in Arm and Shoulder Muscles from the Monkey Pontomedullary Reticular Formation , 2007, The Journal of Neuroscience.

[37]  J. Valls-Solé,et al.  Interaction between startle and voluntary reactions in humans , 2008, Experimental Brain Research.

[38]  T. Drew,et al.  Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. , 2008, Journal of neurophysiology.

[39]  R. Lemon Descending pathways in motor control. , 2008, Annual review of neuroscience.

[40]  G. Orlovsky,et al.  Postural performance in decerebrated rabbit , 2008, Behavioural Brain Research.

[41]  T. G. Deliagina,et al.  Spinal and supraspinal postural networks , 2008, Brain Research Reviews.

[42]  T. Drew,et al.  The pontomedullary reticular formation contributes to the compensatory postural responses observed following removal of the support surface in the standing cat. , 2009, Journal of neurophysiology.

[43]  Stuart N. Baker,et al.  Direct and Indirect Connections with Upper Limb Motoneurons from the Primate Reticulospinal Tract , 2009, The Journal of Neuroscience.

[44]  Claire F. Honeycutt,et al.  Electromyographic responses from the hindlimb muscles of the decerebrate cat to horizontal support surface perturbations. , 2009, Journal of neurophysiology.

[45]  W. Byblow,et al.  Repetitive stimulation of premotor cortex affects primary motor cortex excitability and movement preparation , 2009, Brain Stimulation.

[46]  P. Langhorne,et al.  Motor recovery after stroke: a systematic review , 2009, The Lancet Neurology.

[47]  Anthony N. Carlsen,et al.  Differential effects of startle on reaction time for finger and arm movements. , 2009, Journal of neurophysiology.

[48]  S. T. Sakai,et al.  Reticulospinal neurons in the pontomedullary reticular formation of the monkey (Macaca fascicularis) , 2009, Neuroscience.

[49]  A. Handley,et al.  Movement disorders after stroke. , 2008, Age and ageing.

[50]  Stuart N. Baker,et al.  Convergence of Pyramidal and Medial Brain Stem Descending Pathways Onto Macaque Cervical Spinal Interneurons , 2010, Journal of neurophysiology.

[51]  T. Nichols,et al.  The decerebrate cat generates the essential features of the force constraint strategy. , 2010, Journal of neurophysiology.

[52]  Colum D. MacKinnon,et al.  Motor preparation is modulated by the resolution of the response timing information , 2010, Brain Research.

[53]  Stuart N Baker,et al.  The primate reticulospinal tract, hand function and functional recovery , 2011, The Journal of physiology.

[54]  Dana Maslovat,et al.  Considerations for the use of a startling acoustic stimulus in studies of motor preparation in humans , 2011, Neuroscience & Biobehavioral Reviews.

[55]  M. Schieber,et al.  Dissociating motor cortex from the motor , 2011, The Journal of physiology.

[56]  S. Baker,et al.  Reticular formation responses to magnetic brain stimulation of primary motor cortex , 2012, The Journal of physiology.

[57]  Stuart N Baker,et al.  Cells in the monkey ponto-medullary reticular formation modulate their activity with slow finger movements , 2012, The Journal of physiology.

[58]  I. Franks,et al.  The effects of prepulse inhibition timing on the startle reflex and reaction time , 2012, Neuroscience Letters.

[59]  C. MacKinnon,et al.  The early release of planned movement by acoustic startle can be delayed by transcranial magnetic stimulation over the motor cortex , 2012, The Journal of physiology.

[60]  Claire F. Honeycutt,et al.  Planning of Ballistic Movement following Stroke: Insights from the Startle Reflex , 2012, PloS one.

[61]  R. Lemon,et al.  Lawrence and Kuypers (1968a, b) revisited: copies of the original filmed material from their classic papers in Brain. , 2012, Brain : a journal of neurology.

[62]  Stuart N. Baker,et al.  Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey , 2012, Brain : a journal of neurology.

[63]  Ann A. O'Connell,et al.  Longitudinal Data Analysis , 2013 .

[64]  D. G. Lawrence . The effects of bilateral pyramidal lesions . II . The effects of lesions of the descending brainstem pathways , 2022 .