Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation

One must be prudent when selecting potential saccadic targets because the eyes can only move to one location at a time, yet movements must occur quickly enough to permit interaction with a rapidly changing world. This process of efficiently acquiring relevant targets may be aided by advanced planning of a movement toward an upcoming target whose location is gathered via environmental cues or situational experience. We studied how saccadic reaction times (SRTs) and early pretarget neuronal activity covaried as a function of saccadic probability. Monkeys performed a saccadic task in which the probability of the required saccade being directed into the response field of a neuron varied systematically between blocks of trials. We recorded simultaneously the early pretarget activity of saccade-related neurons in the intermediate layers of the superior colliculus. We found that, as the likelihood of the saccade being generated into the response field of the neuron increased, the level of neuronal activity preceding target presentation also increased. Our data suggest that this early activity codes motor preparation because its activity was related to not only the metrics but also the timing of the saccade, with 94% (29/31) of the neurons tested having significant negative correlations between discharge rate and SRT. This view is supported by cases in which exceptionally high levels of pretarget activity were associated with anticipatory saccades into the response field of a neuron that occurred in advance of the target being presented. This study demonstrates how situational experience can expedite motor behavior via the advanced preparation of motor programs.

[1]  R. Hackman,et al.  An experimental study of variability in ocular latency. , 1940 .

[2]  W. E. Hick Quarterly Journal of Experimental Psychology , 1948, Nature.

[3]  Alexa Riehle,et al.  Preparation for Action: one of the Key Functions of Motor Cortex , 2004 .

[4]  A. Bartz,et al.  Eye-movement latency, duration, and response time as a function of angular displacement. , 1962, Journal of experimental psychology.

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

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

[7]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[8]  E. Megaw,et al.  Individual and simultaneous tracking of a step input by the horizontal saccadic eye movement and manual control systems. , 1973, Journal of experimental psychology.

[9]  R H Wurtz,et al.  Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. , 1976, Journal of neurophysiology.

[10]  C. R. Deboor,et al.  A practical guide to splines , 1978 .

[11]  D. Sparks Functional properties of neurons in the monkey superior colliculus: Coupling of neuronal activity and saccade onset , 1978, Brain Research.

[12]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[13]  D. Sparks,et al.  Dissociation of visual and saccade-related responses in superior colliculus neurons. , 1980, Journal of neurophysiology.

[14]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[15]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[16]  B. Fischer,et al.  Saccadic eye movements after extremely short reaction times in the monkey , 1983, Brain Research.

[17]  J. Requin,et al.  Changes in neuronal activity of the monkey precentral cortex during preparation for movement. , 1986, Journal of neurophysiology.

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

[19]  Hidehiko Komatsu,et al.  A grid system and a microsyringe for single cell recording , 1988, Journal of Neuroscience Methods.

[20]  D. Sparks,et al.  The deep layers of the superior colliculus. , 1989, Reviews of oculomotor research.

[21]  Eileen Kowler,et al.  The role of location probability in the programming of saccades: Implications for “center-of-gravity” tendencies , 1989, Vision Research.

[22]  D Guitton,et al.  Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. , 1991, Journal of neurophysiology.

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

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

[25]  B. Fischer,et al.  Express saccades and visual attention , 1993, Behavioral and Brain Sciences.

[26]  D L Sparks,et al.  Effects of low-frequency stimulation of the superior colliculus on spontaneous and visually guided saccades. , 1993, Journal of neurophysiology.

[27]  A. Riehle,et al.  The predictive value for performance speed of preparatory changes in neuronal activity of the monkey motor and premotor cortex , 1993, Behavioural Brain Research.

[28]  Henry Szechtman,et al.  Longlasting consequences of chronic treatment with the dopamine agonist quinpirole for the undrugged behavior of rats , 1993, Behavioural Brain Research.

[29]  R. Klein,et al.  Does Oculomotor Readiness Mediate Cognitive Control of Visual-Attention - Revisited , 1994 .

[30]  D. Munoz,et al.  A neural correlate for the gap effect on saccadic reaction times in monkey. , 1995, Journal of neurophysiology.

[31]  R. H. S. Carpenter,et al.  Neural computation of log likelihood in control of saccadic eye movements , 1995, Nature.

[32]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[33]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.

[34]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[35]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[36]  D. Robinson,et al.  Shared neural control of attentional shifts and eye movements , 1996, Nature.

[37]  D P Munoz,et al.  Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. , 1996, Journal of neurophysiology.

[38]  Michele A. Basso,et al.  Modulation of neuronal activity by target uncertainty , 1997, Nature.

[39]  N. J. Gandhi,et al.  Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. , 1997, Journal of neurophysiology.

[40]  D. Munoz,et al.  Neuronal Activity in Monkey Superior Colliculus Related to the Initiation of Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[41]  D. Munoz,et al.  Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. , 1998, Journal of neurophysiology.