Correlation of primate caudate neural activity and saccade parameters in reward-oriented behavior.

Changes in the reward context are associated with changes in neuronal activity in the basal ganglia as well as changes in motor outputs. A typical example is found in the caudate (CD) projection neurons and saccade parameters. It raised the possibility that the changes in CD neuronal activity contribute to the changes in saccade parameters. To examine this possibility, we calculated the correlation coefficients (CORs) of the firing rates of each neuron with saccade parameters (peak saccade velocity and latency) on a trial-by-trial basis. We then calculated the mean CORs separately for two CD populations: reward-enhanced type neurons (RENs) that showed enhanced activity and reward-depressed type neurons (RDNs) that showed depressed activity when reward was expected. The activity of RENs was positively correlated with the saccadic peak velocity and negatively correlated with the saccade latency. The activity of RDNs was not significantly correlated with the saccade parameters. We further analyzed the CORs for RENs, a major type of CD neurons. First, we examined the time courses of the CORs using a moving time window (duration: 200 ms). The positive correlation with the saccade velocity and the negative correlation with the saccade latency were present not only in the peri-saccadic period but also during the pre- and postcue periods. Second, we asked whether the CORs with the saccade parameters were direction-selective. A majority of RENs were more active before contralateral saccades (contralateral-preferring neurons) and their activity was correlated more strongly with contralateral saccades than with ipsilateral saccades. A minority of RENs, ipsilateral-preferring neurons, showed no such preference. These results are consistent with the hypothesis that CD neuronal activity exerts facilitatory effects on contralateral saccades and that the effects start well before saccade execution. Furthermore, a multiple regression analysis indicated that changes in activity of some, but not all, CD neurons could be explained by changes in saccade parameters; a major determinant was reward context (presence or absence of reward). These results suggest that, while a majority of CD neurons receive reward-related signals, only some of them can make a significant contribution to change saccadic outputs based on expected reward.

[1]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

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

[3]  M. Delong,et al.  Putamen: Activity of Single Units during Slow and Rapid Arm Movements , 1973, Science.

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

[5]  Hanna Damasio,et al.  Neglect following damage to frontal lobe or basal ganglia , 1980, Neuropsychologia.

[6]  M. D. Crutcher,et al.  Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. M. Beckstead Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes , 1983, Neuroscience.

[8]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. , 1983, Journal of neurophysiology.

[9]  M. Williams,et al.  The striatonigral projection and nigrotectal neurons in the rat. A correlated light and electron microscopic study demonstrating a monosynaptic striatal input to identified nigrotectal neurons using a combined degeneration and horseradish peroxidase procedure , 1985, Neuroscience.

[10]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons , 1985, Brain Research.

[11]  D L Sparks,et al.  Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. , 1986, Physiological reviews.

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

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

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

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

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

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

[18]  A. Parent Extrinsic connections of the basal ganglia , 1990, Trends in Neurosciences.

[19]  Okihide Hikosaka,et al.  Visual and oculomotor functions of monkey subthalamic nucleus. , 1992 .

[20]  A. Graybiel,et al.  Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  J. Schall,et al.  Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  W. Schultz The Primate Basal Ganglia Between the Intention and Outcome of Action , 1995 .

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

[24]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  P. Goldman-Rakic,et al.  Differential Activation of the Caudate Nucleus in Primates Performing Spatial and Nonspatial Working Memory Tasks , 1997, The Journal of Neuroscience.

[26]  D. R. Smith,et al.  Behavioural assessment of mice lacking D1A dopamine receptors , 1998, Neuroscience.

[27]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[28]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

[29]  Y. Smith,et al.  Microcircuitry of the direct and indirect pathways of the basal ganglia. , 1998, Neuroscience.

[30]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[31]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[32]  O. Hikosaka,et al.  Modulation of saccadic eye movements by predicted reward outcome , 2001, Experimental Brain Research.

[33]  佐藤 真琴,et al.  Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement , 2002 .

[34]  O. Hikosaka,et al.  Effects of caudate nucleus stimulation on substantia nigra cell activity in monkey , 2004, Experimental Brain Research.