Representation of multiple kinematic parameters of the cat hindlimb in spinocerebellar activity.

Dorsal spinocerebellar tract (DSCT) neurons have been shown to transmit signals related to hindlimb position and movement direction in the anesthetized cat. Because both parameters may be encoded by single neurons, we examined the extent to which their representations might occur sequentially or simultaneously by recording unit activity while the hindlimb was moved passively in the sagittal plane by a robot arm. A center-out/out-center paradigm moved the foot 2 cm from a given position radially to eight positions located 45 degrees apart, holding each position for 8 s. Another paradigm moved the foot along various paths to 20 positions distributed throughout most of the limb's workspace. With each paradigm, we could assess the activity related to foot position and the direction of movement to each position. Modulation of unit activity evoked by center-out/out-center movements was determined for each 1-s postmovement interval by use of a cosine tuning model that specified modulation amplitude and preferred direction. Of 125 units tested, 82.4% were significantly modulated (P < 0.05) according to this model. We assessed the relative contributions of position and movement by taking advantage of the fact that directional modulation following out-center movements to a common position could only be related to the movement, whereas that following the center-out movements related to both position and movement. The results suggested a simultaneous modulation by these two parameters. Each cell could be characterized by a similar preferred direction for position or movement modulation and the distribution of preferred directions across cells clustered significantly along an axis close to the limb axis. When the limb axis was rotated, the unit preferred directions rotated similarly, on average. Unexpectedly, we found the activity of more than half the cells to be modulated for > or = 8 s after out-center movements, implying a persistent movement-related activity well after a movement is completed. These findings were confirmed and extended with the second paradigm by using a multivariate regression model that included terms for position, movement, and their multiplicative interaction. The activity of 81.3% of the 97 neurons tested fit the model (R2 > 0.4, P < .0001); 31.6% were modulated exclusively by foot position, and 58.2% simultaneously by both position and movement, with significant interaction. We conclude from our results that DSCT neurons may be modulated simultaneously by limb position and movement, and their preferred directions tend to align with the limb axis. The modulation is interactive such that movement modulation amplitude depends on limb position, and many cells also retain a memory trace of recent movements. The results are discussed in terms of a possible role for the DSCT in encoding limb compliance.

[1]  R. Álvarez-Buylla,et al.  Local responses in Pacinian corpuscles. , 1952, The American journal of physiology.

[2]  O. Oscarsson,et al.  FUNCTIONAL ORGANIZATION OF THE SPINO- AND CUNEOCEREBELLAR TRACTS. , 1965, Physiological reviews.

[3]  P. Grigg,et al.  Response of primate joint afferent neurons to mechanical stimulation of knee joint. , 1977, Journal of neurophysiology.

[4]  M. Arendse Magnetic field detection is distinct from light detection in the invertebrates Tenebrio and Talitrus , 1978, Nature.

[5]  E. Batschelet Circular statistics in biology , 1981 .

[6]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[8]  E. Bizzi,et al.  Neural, mechanical, and geometric factors subserving arm posture in humans , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  E. Jankowska,et al.  Information processed by dorsal horn spinocerebellar tract neurones in the cat. , 1988, The Journal of physiology.

[10]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. III. Positional gradients and population coding of movement direction from various movement origins , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[12]  Components of responses of a population of DSCT neurons to muscle stretch and contraction. , 1989, Journal of neurophysiology.

[13]  F Lacquaniti,et al.  The control of limb geometry in cat posture. , 1990, The Journal of physiology.

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

[15]  J F Soechting,et al.  Moving in three-dimensional space: frames of reference, vectors, and coordinate systems. , 1992, Annual review of neuroscience.

[16]  Gary D. Cravens,et al.  A Backpropagation Programmed Neural Network That Simulates the Properties of a Subset of Nucleus Reticularis Tegmenti Pontis Neurons , 1992 .

[17]  U Proske,et al.  Muscle history dependence of responses to stretch of primary and secondary endings of cat soleus muscle spindles. , 1992, The Journal of physiology.

[18]  R E Poppele,et al.  Broad directional tuning in spinal projections to the cerebellum. , 1993, Journal of neurophysiology.

[19]  Richard A. Andersen,et al.  Coordinate transformations in the representation of spatial information , 1993, Current Opinion in Neurobiology.

[20]  R. Poppele,et al.  Sensory integration by the dorsal spinocerebellar tract circuitry , 1993, Neuroscience.

[21]  F. Lacquaniti,et al.  Coordinate transformations in the control of cat posture. , 1994, Journal of neurophysiology.

[22]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  J. Kalaska,et al.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. , 1994, Journal of neurophysiology.

[24]  A. Opstal,et al.  Influence of eye position on activity in monkey superior colliculus. , 1995, Journal of neurophysiology.

[25]  R. Andersen,et al.  Head position signals used by parietal neurons to encode locations of visual stimuli , 1995, Nature.

[26]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  G. Laurent,et al.  Hysteresis reduction in proprioception using presynaptic shunting inhibition. , 1995, Journal of neurophysiology.

[28]  R. Poppele,et al.  Kinematic analysis of cat hindlimb stepping. , 1995, Journal of neurophysiology.

[29]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[30]  R. Poppele,et al.  Representation of passive hindlimb postures in cat spinocerebellar activity. , 1996, Journal of neurophysiology.

[31]  R E Poppele,et al.  Temporal features of directional tuning by spinocerebellar neurons: relation to limb geometry. , 1996, Journal of neurophysiology.