Population vector analysis of primate prefrontal activity during spatial working memory.

Population vectors were used to examine information represented by a population of prefrontal activity and its temporal change during spatial working memory processes while monkeys performed ODR and R-ODR tasks. In the ODR task, monkeys made a saccade to the cue location after the delay, whereas in the R-ODR task, they made a saccade 90 degrees clockwise from the cue location. We first constructed population vectors using cue- and response-period activity. The directions of population vectors were similar to the cue directions and the saccade target directions, respectively, indicating that population vectors correctly represented information regarding directions of visual cues and saccade targets. We then calculated population vectors during a 250 ms time-window from the cue presentation to the end of the response period. In the ODR task, all population vectors were directed toward the cue direction. However, in the R-ODR task, the population vector gradually rotated during the delay period from the cue direction to the saccade direction. These results indicate that spatial information represented by a population of prefrontal activity can be shown as the direction of the population vector and that its temporal change during spatial working memory tasks can be depicted as the temporal change of the vector's direction.

[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]  J. Fuster.  Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[3]  Kanti V. Mardia,et al.  Statistics of Directional Data , 1972 .

[4]  H. Niki.  Differential activity of prefrontal units during right and left delayed response trials. , 1974, Brain research.

[5]  Masataka Watanabe,et al.  Prefrontal unit activity and delayed response: Relation to cue location versus direction of response , 1976, Brain Research.

[6]  J. Fuster.  Prefrontal Cortex , 2018 .

[7]  P. Goldman-Rakic,et al.  Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response , 1982, Brain Research.

[8]  John F. Kalaska,et al.  Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations , 1983 .

[9]  Shozo Kojima,et al.  Functional analysis of spatially discriminative neurons in prefrontal cortex of rhesus monkey , 1984, Brain Research.

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

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

[12]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[13]  E. G. Jones.  Cerebral Cortex , 1987, Cerebral Cortex.

[14]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Georgopoulos.  Neural integration of movement: role of motor cortex in reaching , 1988, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[16]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  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.

[18]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

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

[20]  C. Bruce,et al.  Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. , 1990, Journal of neurophysiology.

[21]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[22]  P. Goldman-Rakic,et al.  Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. , 1991, Journal of neurophysiology.

[23]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[24]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during sinusoid tracing. , 1993, Journal of neurophysiology.

[25]  A. Georgopoulos,et al.  Cognitive neurophysiology of the motor cortex. , 1993, Science.

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

[27]  G. S. Russo,et al.  Effect of eye position within the orbit on electrically elicited saccadic eye movements: a comparison of the macaque monkey's frontal and supplementary eye fields. , 1993, Journal of neurophysiology.

[28]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

[29]  S. Funahashi,et al.  Working memory and prefrontal cortex , 1994, Neuroscience Research.

[30]  P. Goldman-Rakic.  Cellular basis of working memory , 1995, Neuron.

[31]  A. Aertsen,et al.  Dynamics of neuronal interactions in monkey cortex in relation to behavioural events , 1995, Nature.

[32]  G. S. Russo,et al.  Neurons in the supplementary eye field of rhesus monkeys code visual targets and saccadic eye movements in an oculocentric coordinate system. , 1996, Journal of neurophysiology.

[33]  P. Goldman-Rakic.  The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[35]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[36]  A. Miyake,et al.  Models of Working Memory: Mechanisms of Active Maintenance and Executive Control , 1999 .

[37]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999, Journal of neurophysiology.

[38]  Representation of spatial information by the neuronal population of the prefrontal cortex , 2000 .

[39]  S. Funahashi,et al.  Neuronal interactions related to working memory processes in the primate prefrontal cortex revealed by cross-correlation analysis. , 2000, Cerebral cortex.

[40]  Shintaro Funahashi,et al.  Neuronal mechanisms of executive control by the prefrontal cortex , 2001, Neuroscience Research.

[41]  P. Goldman-Rakic,et al.  Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex , 2001, The Journal of Neuroscience.

[42]  Christos Constantinidis,et al.  The sensory nature of mnemonic representation in the primate prefrontal cortex , 2001, Nature Neuroscience.

[43]  Shintaro Funahashi,et al.  Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks. , 2002, Journal of neurophysiology.

[44]  Klaus-Peter Hoffmann,et al.  Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements. , 2002, Cerebral cortex.

[45]  T. Wen,et al.  Developmental Control of Foraging and Social Behavior by the Drosophila Neuropeptide Y-like System , 2003, Neuron.

[46]  A. P. Georgopoulos,et al.  Cognitive spatial-motor processes , 2004, Experimental Brain Research.

[47]  S. Funahashi.  Information Processing in the Primate Prefrontal Cortex , 2004 .

[48]  J. T. Massey,et al.  Cognitive spatial-motor processes , 2004, Experimental Brain Research.

[49]  Masato Taira,et al.  Motor cortical activity in a memorized delay task , 1992, Experimental Brain Research.

[50]  Masato Taira,et al.  Motor cortical activity preceding a memorized movement trajectory with an orthogonal bend , 1993, Experimental Brain Research.