Activity linked to externally cued saccades in single units recorded from hippocampal, parahippocampal, and inferotemporal areas of macaques.

We studied whether target-directed, externally commanded saccadic eye movements (saccades) induced activity in single units in inferotemporal cortex, the hippocampal formation, and parahippocampal gyrus. The monkeys first were required to fix their gaze on a small cross presented to the left or right of center on the monitor screen. The cross was extinguished, and a random 600-1,000 ms thereafter, a small dot was presented for 200 ms. The dot was located either 10 degrees above, below, right, or left of the position on which the fixation cross had been. The monkey made a saccadic eye movement to this dot (in darkness). The neuronal activity around this goal-directed saccade was analyzed. In addition, control conditions were imposed systematically in which similar dots were presented, but the monkey's task was to withhold the saccade. We recorded 290 units from two monkeys. From this group, 134 met two criteria, they did not show visual response in control trials and they had spike rates >2 Hz. These were analyzed further; 53% (71/134) showed modulation related to the target directed saccade, and 29% (39/134) showed saccadic modulation during spontaneous eye movements. These two groups were correlated only weakly. Of the units with significant saccadic modulation, 17% (12/71) showed significant directional selectivity, and 13% (9/71) showed significant position selectivity (P < 0.01). At a lower criterion (P < 0.05), almost one-half (33/71) showed one or the other spatial selectivity. Primates use saccades to acquire visual information. The appearance of strong saccadic modulation in brain structures previously characterized as mnemonic suggests the possibility that the mnemonic circuitry uses an extraretinal signal linked to saccades to control visual memory processes, e.g., synchronizing mnemonic processes to the pulsatile visual data inflow.

[1]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[3]  E. Rolls,et al.  Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate , 1991, Psychobiology.

[4]  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.

[5]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  J L Ringo,et al.  Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. , 1994, Journal of neurophysiology.

[7]  J. Ringo Stimulus specific adaptation in inferior temporal and medial temporal cortex of the monkey , 1996, Behavioural Brain Research.

[8]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[9]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[11]  W. R. Adey,et al.  A stereotaxic brain atlas for Macaca nemestrina , 1969 .

[12]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[14]  R. Wurtz,et al.  Visual responses of inferior temporal neurons in awake rhesus monkey. , 1983, Journal of neurophysiology.

[15]  Leslie G. Ungerleider,et al.  Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys , 1993, Visual Neuroscience.

[16]  M. W. Brown Neuronal responses and recognition memory , 1996 .