What Roles Do Tonic Inhibition and Disinhibition Play in the Control of Motor Programs?

Animals show periods of quiescence interspersed with periods of motor activity. In a number of invertebrate and vertebrate systems, quiescence is achieved by active suppression of motor behavior is due to tonic inhibition induced by sensory input or changes in internal state. Removal of this inhibition (disinhibition) has the converse effect tending to increase the level of motor activity. We show that tonic inhibition and disinhibition can have a variety of roles. It can simply switch off specific unwanted motor behaviors, or modulate the occurrence of a motor response, a type of ‘threshold’ controlling function, or be involved in the selection of a particular motor program by inhibiting ‘competing’ motor mechanisms that would otherwise interfere with the carrying out of a desired movement. A suggested general function for tonic inhibition is to prevent unnecessary non-goal directed motor activity that would be energetically expensive. The reason why basic motor programs might be a particular target for tonic inhibition is that many of them involve central pattern generator circuits that are often spontaneously active and need to be actively suppressed for energy saving. Based on this hypothesis, tonic inhibition represents the default state for energy saving and motor programs are switched-on when required by removal of this inhibition.

[1]  U. Norrsell,et al.  Behavioural repertory of cats without cerebral cortex from infancy , 1976, Experimental Brain Research.

[2]  P. Redgrave,et al.  The Basal Ganglia viewed as an Action Selection Device , 1998 .

[3]  Kevin Staras,et al.  Loss of Self-Inhibition Is a Cellular Mechanism for Episodic Rhythmic Behavior , 2003, Current Biology.

[4]  K. Saitoh,et al.  Role of basal ganglia–brainstem pathways in the control of motor behaviors , 2004, Neuroscience Research.

[5]  F B Krasne,et al.  Response-dedicated trigger neurons as control points for behavioral actions: selective inhibition of lateral giant command neurons during feeding in crayfish , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  H. Evans The Study of Instinct , 1952 .

[7]  C. Gerfen The neostriatal mosaic: multiple levels of compartmental organization , 1992, Trends in Neurosciences.

[8]  T. Carew,et al.  Activity-dependent regulation of neural networks: the role of inhibitory synaptic plasticity in adaptive gain control in the siphon withdrawal reflex of Aplysia. , 1997, The Biological bulletin.

[9]  And J. B. Plant,et al.  Mechanisms and significance of reduced activity and responsiveness in resting frog tadpoles , 2004, Journal of Experimental Biology.

[10]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[11]  William Rowan,et al.  The Study of Instinct , 1953 .

[12]  F. Krasne,et al.  Altered Excitability of the Crayfish Lateral Giant Escape Reflex during Agonistic Encounters , 1997, The Journal of Neuroscience.

[13]  S. Grillner,et al.  Diencephalic locomotor region in the lamprey--afferents and efferent control. , 2008, Journal of neurophysiology.

[14]  F. Krasne,et al.  Vu, E. T. , Lee, S. C. & Krasne, F. B. The mechanism of tonic inhibition of crayfish escape behavior: Distal inhibition and its functional significance. J. Neurosci. 13, 4379-4393 , 1993 .

[15]  D. Perkel,et al.  Motor Pattern Production in Reciprocally Inhibitory Neurons Exhibiting Postinhibitory Rebound , 1974, Science.

[16]  Dylan F. Cooke,et al.  The Cortical Control of Movement Revisited , 2002, Neuron.

[17]  W. Kristan Neuronal Decision-Making Circuits , 2008, Current Biology.

[18]  W. J. Heitler,et al.  Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish , 1999, Trends in Neurosciences.

[19]  A. Roberts,et al.  Sensory Activation and Role of Inhibitory Reticulospinal Neurons that Stop Swimming in Hatchling Frog Tadpoles , 2002, The Journal of Neuroscience.

[20]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[21]  S. Grillner,et al.  Neuronal Control of Locomotion 'From Mollusc to Man ' , 1999 .

[22]  E.C.L. Vu,et al.  Crayfish tonic inhibition: prolonged modulation of behavioral excitability by classical GABAergic inhibition , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  D. Bieger,et al.  Role of solitarial GABAergic mechanisms in control of swallowing. , 1991, The American journal of physiology.

[24]  S. Grillner The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[25]  S. Soffe,et al.  Brainstem control of activity and responsiveness in resting frog tadpoles: tonic inhibition , 2004, Journal of Comparative Physiology A.

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

[27]  Kaoru Takakusaki,et al.  Forebrain control of locomotor behaviors , 2008, Brain Research Reviews.

[28]  A. Roberts,et al.  Roles for inhibition: studies on networks controlling swimming in young frog tadpoles , 2008, Journal of Comparative Physiology A.

[29]  F. Krasne,et al.  Extrinsic modulation of crayfish escape behaviour. , 1975, The Journal of experimental biology.

[30]  Jianfeng Feng,et al.  Dynamic control of a central pattern generator circuit: a computational model of the snail feeding network , 2007, The European journal of neuroscience.