Spatial processing in the monkey frontal eye field. II. Memory responses.

Monkeys and humans can easily make accurate saccades to stimuli that appear and disappear before an intervening saccade to a different location. We used the flashed-stimulus task to study the memory processes that enable this behavior, and we found two different kinds of memory responses under these conditions. In the short-term spatial memory response, the monkey fixated, a stimulus appeared for 50 ms outside the neuron's receptive field, and from 200 to 1,000 ms later the monkey made a saccade that brought the receptive field onto the spatial location of the vanished stimulus. Twenty-eight of 48 visuomovement cells and 21/32 visual cells responded significantly under these circumstances even though they did not discharge when the monkey made the same saccade without the stimulus present or when the stimulus appeared and the monkey did not make a saccade that brought its spatial location into the receptive field. Response latencies ranged from 48 ms before the beginning of the saccade (predictive responses) to 272 ms after the beginning of the saccade. After the monkey made a series of 16 saccades that brought a stimulus into the receptive field, 21 neurons demonstrated a longer term, intertrial memory response: they discharged even on trials in which no stimulus appeared at all. This intertrial memory response was usually much weaker than the within-trial memory response, and it often lasted for over 20 trials. We suggest that the frontal eye field maintains a spatially accurate representation of the visual world that is not dependent on constant or continuous visual stimulation, and can last for several minutes.

[1]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[2]  P. E. Hallett,et al.  Saccadic eye movements to flashed targets , 1976, Vision Research.

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

[4]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

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

[7]  L. Optican,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. , 1987, Journal of neurophysiology.

[8]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[9]  B. Cohen,et al.  Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and Its homologue in man , 1988, The Journal of comparative neurology.

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

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

[12]  M. Goldberg,et al.  Representation of visuomotor space in the parietal lobe of the monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[13]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. II. Spatial properties. , 1991, Journal of neurophysiology.

[14]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[15]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. , 1993, Journal of neurophysiology.

[16]  M. Segraves,et al.  Primate frontal eye field activity during natural scanning eye movements. , 1994, Journal of neurophysiology.

[17]  S Eifuku,et al.  Neuronal activity in the primate hippocampal formation during a conditional association task based on the subject's location , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  M. Goldberg,et al.  Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. , 1995, Journal of neurophysiology.

[19]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[20]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[21]  M. A. Basso,et al.  Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability , 1998, The Journal of Neuroscience.

[22]  Christian Quaia,et al.  The maintenance of spatial accuracy by the perisaccadic remapping of visual receptive fields , 1998, Neural Networks.

[23]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[24]  J. O’Keefe Do hippocampal pyramidal cells signal non‐spatial as well as spatial information? , 1999, Hippocampus.

[25]  Jacqueline Gottlieb,et al.  The lateral intraparietal area as a salience map: the representation of abrupt onset, stimulus motion, and task relevance , 2000, Vision Research.