The role of inhibition in the hierarchical gating of executed and imagined movements.

A theory is presented concerning the neuronal mechanisms which may underlie the organisation of imagined versus executed movements. A review is first presented of previous theoretical and experimental evidence suggesting that the brain can use the same mechanisms for the imagination and the execution of movement. In particular the fact that adaptation of the vestibulo-ocular reflex can be obtained by pure mental effort and not solely by conflicting visual and vestibular cues has been suggestive of the fact that the brain could internally simulate conflicts and use the same adaptive mechanisms used when actual sensory cues were in conflict. The saccadic system is taken as a good model for the study of this question because the mechanisms which underlie saccade generation are now partially understood at different levels from the brain stem to the cortex. The central idea of the theory is based upon the fact that, in parallel with the excitatory mechanisms underlying saccade generation, several inhibitory mechanisms in cascade allow the selective modulation and blockage of saccades. Synaptic inhibition is therefore supposed to play a major role in a hierarchical selective gating of saccade execution not at one but at several levels allowing a variety of different types of "imagined movements' some involving only the higher levels some in which the execution is only blocked at the very immediate premotor level. But in all cases the theory proposes that imagination and execution have many mechanisms in common. PET data showing that indeed the same structures are activated in both types of movements support this idea although the final answer will have to be brought by neuronal data.

[1]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[2]  Lance M. Optican,et al.  Superior colliculus cell types and models of saccade generation , 1994, Current Opinion in Neurobiology.

[3]  M. Raichle,et al.  The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. , 1985, Journal of neurophysiology.

[4]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons , 1986, The Journal of comparative neurology.

[5]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  G. Somjen Integration in the nervous system , 1981 .

[7]  Richard S. J. Frackowiak,et al.  Cortical control of saccades and fixation in man. A PET study. , 1994, Brain : a journal of neurology.

[8]  J. Houk MODEL OF THE CEREBELLUM AS AN ARRAY OF ADJUSTABLE PATTERN GENERATORS. , 1987 .

[9]  Masao Ito The Cerebellum And Neural Control , 1984 .

[10]  A. Fuchs,et al.  Brainstem control of saccadic eye movements. , 1985, Annual review of neuroscience.

[11]  Ian S. Curthoys,et al.  Direct projection of pause neurons to nystagmus-related excitatory burst neurons in the cat pontine reticular formation , 1984, Experimental Neurology.

[12]  M. Kawato,et al.  Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum , 1993, Nature.

[13]  A Berthoz,et al.  The role of gaze in compensation of vestibular disfunction: the gaze substitution hypothesis. , 1988, Progress in brain research.

[14]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[15]  A Berthoz,et al.  Functional Neuroanatomy of the Human Visual Fixation System , 1995, The European journal of neuroscience.

[16]  M. Segraves Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. , 1992, Journal of neurophysiology.

[17]  David H. Hubel,et al.  Vision and the Brain , 1978 .

[18]  M. Wallace,et al.  Converging influences from visual, auditory, and somatosensory cortices onto output neurons of the superior colliculus. , 1993, Journal of neurophysiology.

[19]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. , 1993, Journal of neurophysiology.

[20]  M. Ito Cerebellar control of the vestibulo-ocular reflex--around the flocculus hypothesis. , 1982, Annual review of neuroscience.

[21]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. , 1983, Journal of neurophysiology.

[22]  Carlo Umiltà,et al.  Programming shifts of spatial attention , 1994 .

[23]  R. B. Hamilton,et al.  Neural coding of gustatory information in the thalamus of Macaca mulatta. , 1989, Journal of neurophysiology.

[24]  J. Jaffe,et al.  Ibogaine fails to reduce naloxone-precipitated withdrawal in the morphine-dependent rat. , 1990, Neuroreport.

[25]  C. Scudder,et al.  Structure of the primate oculomotor burst generator. II. Medium-lead burst neurons with downward on-directions. , 1991, Journal of neurophysiology.

[26]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  A K Moschovakis,et al.  Neural network simulations of the primate oculomotor system. I. The vertical saccadic burst generator. , 1994, Biological cybernetics.

[28]  David L. Sparks,et al.  Movement selection in advance of action in the superior colliculus , 1992, Nature.

[29]  Ma Gresty,et al.  Vestibular and Visual Control on Posture and Locomotor Equilibrium , 1986 .

[30]  A K Moschovakis,et al.  Structure of the primate oculomotor burst generator. I. Medium-lead burst neurons with upward on-directions. , 1991, Journal of neurophysiology.

[31]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[32]  A. Berthoz Multisensory control of movement , 1993 .

[33]  O Hikosaka,et al.  Functional properties of monkey caudate neurons. II. Visual and auditory responses. , 1989, Journal of neurophysiology.

[34]  A Berthoz,et al.  Adaptive mechanisms in eye-head coordination. , 1985, Reviews of oculomotor research.

[35]  P. Goldman-Rakic,et al.  Cerebral cortical mechanisms in schizophrenia , 1994 .

[36]  A. L. I︠A︡rbus Eye Movements and Vision , 1967 .

[37]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[38]  A. Berthoz,et al.  Neuronal mechanisms underlying eye-head coordination. , 1986, Progress in brain research.

[39]  J. Montgomery,et al.  Dogfish horizontal canal system: Responses of primary afferent, vestibular and cerebellar neurons to rotational stimulation , 1980, Neuroscience.

[40]  A. Fuchs,et al.  Role of cat pontine burst neurons in generation of saccadic eye movements. , 1981, Journal of neurophysiology.

[41]  J. Decety,et al.  Comparative analysis of actual and mental movement times in two graphic tasks , 1989, Brain and Cognition.

[42]  A K Moschovakis,et al.  Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. , 1988, Journal of neurophysiology.

[43]  A Berthoz,et al.  A positron emission tomography study of oculomotor imagery. , 1994, Neuroreport.

[44]  A. Berthoz,et al.  PET study of voluntary saccadic eye movements in humans: basal ganglia-thalamocortical system and cingulate cortex involvement. , 1993, Journal of neurophysiology.

[45]  Y Agid,et al.  Cortical control of reflexive visually-guided saccades. , 1991, Brain : a journal of neurology.

[46]  J. Paillard Brain and space , 1991 .

[47]  V. Henn,et al.  Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey , 1977, Brain Research.

[48]  A. Berthoz,et al.  Neural correlates of horizontal vestibulo‐ocular reflex cancellation during rapid eye movements in the cat. , 1989, The Journal of physiology.

[49]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

[50]  Jones Gm Adaptive modulation of VOR parameters by vision. , 1985 .

[51]  F. A. Miles,et al.  Plasticity in the vestibulo-ocular reflex: a new hypothesis. , 1981, Annual review of neuroscience.

[52]  F. Richmond,et al.  Control of head movement , 1988 .

[53]  S. Wray Adaptive mechanisms in gaze control. , 1986, Reviews of oculomotor research.

[54]  R. Baker,et al.  Comparison of the morphology of physiologically identified abducens motor and internuclear neurons in the cat: A light microscopic study employing the intracellular injection of horseradish peroxidase , 1982, The Journal of comparative neurology.

[55]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[56]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

[57]  Sohee Park,et al.  Schizophrenics show spatial working memory deficits. , 1992, Archives of general psychiatry.

[58]  S. Stone-Elander,et al.  Motor learning in man: a positron emission tomographic study. , 1990, Neuroreport.

[59]  S. Rivaud,et al.  Role of the left and right supplementary motor areas in memory‐guided saccade sequences , 1993, Annals of neurology.

[60]  A Berthoz,et al.  Mental control of the adaptive process. , 1985, Reviews of oculomotor research.

[61]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[62]  J. Droulez,et al.  Use and Limits of Visual Vestibular Interaction in the Control of Posture , 1985 .

[63]  A. Nambu,et al.  Activity of the Prefrontal Cortex on No-Go Decision and Motor Suppression , 1994 .

[64]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[65]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. , 1986, The Journal of comparative neurology.

[66]  C. Bruce,et al.  Physiological correlate of fixation disengagement in the primate's frontal eye field. , 1994, Journal of neurophysiology.

[67]  J. Allum,et al.  Vestibulospinal control of posture and locomotion. , 1988, Progress in brain research.

[68]  P. Goldman-Rakic,et al.  Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task , 1993, Nature.

[69]  C. Scudder A new local feedback model of the saccadic burst generator. , 1988, Journal of neurophysiology.

[70]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[71]  A. Berthoz,et al.  Is the prepositus hypoglossi nucleus the source of another vestibulo-ocular pathway? , 1975, Brain Research.

[72]  A. Thierry,et al.  Motor and Cognitive Functions of the Prefrontal Cortex , 1994, Research and Perspectives in Neurosciences.

[73]  S. Rivaud,et al.  Impairment of sequences of memory‐guided saccades after supplementary motor area lesions , 1990, Annals of neurology.

[74]  M. Goldberg,et al.  Functional properties of corticotectal neurons in the monkey's frontal eye field. , 1987, Journal of neurophysiology.

[75]  J. Cronly-Dillon,et al.  Vision and visual dysfunction. , 1994, Journal of cognitive neuroscience.

[76]  L M Optican,et al.  Superior colliculus neurons mediate the dynamic characteristics of saccades. , 1991, Journal of neurophysiology.

[77]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions , 1990, Trends in Neurosciences.

[78]  R. Wurtz,et al.  The Neurobiology of Saccadic Eye Movements , 1989 .

[79]  A. Pellionisz,et al.  Tensorial approach to the geometry of brain function: Cerebellar coordination via a metric tensor , 1980, Neuroscience.

[80]  A Berthoz,et al.  Morphological and physiological characteristics of inhibitory burst neurons controlling horizontal rapid eye movements in the alert cat. , 1982, Journal of neurophysiology.

[81]  J. Tanji The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[82]  M. Schlag-Rey,et al.  Evidence for a supplementary eye field. , 1987, Journal of neurophysiology.

[83]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[84]  The role of the frontal eye field and its corticotectal projection in the generation of eye movements. , 1990, Research publications - Association for Research in Nervous and Mental Disease.

[85]  L E Mays,et al.  Signal transformations required for the generation of saccadic eye movements. , 1990, Annual review of neuroscience.

[86]  G. Rizzolatti,et al.  Space and selective attention , 1994 .

[87]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. , 1993, Journal of neurophysiology.

[88]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[89]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[90]  G. Jones,et al.  Extreme vestibulo‐ocular adaptation induced by prolonged optical reversal of vision , 1976, The Journal of physiology.

[91]  A K Moschovakis,et al.  Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. , 1988, Journal of neurophysiology.