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1 Department of Neurobiology and Anatomy, University of Rochester Medical Center, Rochester, New York, 14642; and 2 Department of Neurophysiology, Nencki Institute of Experimental Biology, 02-093 Warsaw, Poland
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Sobotka, Stanislaw, Anna Nowicka, and James L. Ringo. Activity linked to externally cued saccades in single units recorded from hippocampal, parahippocampal, and inferotemporal areas of macaques. J. Neurophysiol. 78: 2156-2163, 1997. 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° 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.
Previous work from this laboratory (Ringo et al. 1994 Subjects
Two adult female macaque monkeys (Macaca nemestrina) were used in the experiments. They had limited access to water but received the necessary fluids as rewards in the behavioral task. Hydration levels were carefully monitored, and free water access was allowed at least once each week.
Surgery
Each monkey was prepared for single-unit recording. Nine stainless steel guide tubes (1.5 mm OD) were implanted stereotactically and directed to inferotemporal cortex, hippocampal formation, and posterior parahippocampal gyrus of one hemisphere. These guide tubes penetrated ~6 mm into the dorsal surface of the brain and were fixed in an acrylic layer, which, in turn, was secured to the skull via stainless steel (0.86 mm) and titanium (0.5 mm) screws. During each experimental session, a recording electrode was inserted through one of these guide tubes. At the conclusion of each session, the guide tube was filled with a stainless steel obturator and covered with a screw-top cap. The use of permanently implanted guide tubes made the anatomic localization of our recordings relatively certain.
Unit recording
Single-unit recordings were made with parylene coated electrodes (Microprobe), etched from 75 µm tungsten wire with an impedance of ~1 M Experimental procedure
The monkey was seated in a primate chair. Its head was held by a padded face mask mounted over the snout and by a plate behind the head, preventing withdrawal. Recordings were done in darkness. The display screen, a computer monitor, was positioned 32 cm in front of the monkey's eyes. Each session consisted of 450 trials.
Spontaneous and cued saccades
Before each trial, spontaneous saccadic eye movements were recorded. There was no illumination, from the display or otherwise, in that period. Changes in gaze position >4° within a 20-ms period (200°/s) were treated as saccades. In all cases, the beginning of a saccade was defined by the first time point in which the speed of the eye movement was >15°/s.
Response to the dot in the control condition (without eye movements)
Because the cued saccades always followed a dot presentation, it was necessary to separate responses to the cued saccade from responses to the dot per se (e.g., a visual response). This was done by use of control trials (33% of all trials) in which the monkey was presented with dot patterns designed to be as good or better at eliciting visual responses as the saccade-cuing dots, while at the same time, the monkey was required to refrain from making a saccade. In these control trials, the monkey was required to maintain gaze on the position defined by the placement of the initial fixation cross. Only trials in which the monkey's gaze remained within the 3° window were rewarded.
Localization of recorded areas
At the end of the experiment, one monkey had electrolytic lesions made through each of the guide tubes and was killed with an overdose of barbiturate, then perfused transcardially with saline followed by 10% formalin. The brain was blocked in situ, extracted, embedded in wax, sectioned, and stained. The regions from which the recorded units were isolated were derived from histological data.
Statistical analysis
The existence of saccadic modulation in each unit was tested statistically. However, a simple spike count was not used because that method is poor at detecting biphasic activity, (i.e., discharge patterns after a trigger event that show an increased rate following or followed by a decreased one) and because such biphasic activity patterns are common in ventral temporal lobe units following saccades (Ringo et al. 1994 The monkeys performed the task well, making crisp saccades to the location of the dot on experimental trials while gaze remained fixed on control trials. Figure 3 shows a typical set of eye position records. The unit was selected for its good unit spike activity but was not selected for good saccades. All the eye position records for movements in the different directions and alternate records for control trials (i.e., a comparable number) are shown.
The experiment described in this paper has revealed a strong saccadic modulation widely spread in the ventral temporal lobe. Roughly half of the units recorded in the hippocampal region, the parahippocampal gyrus, and the inferotemporal cortex showed significant modulation of their activity linked to target-directed saccades.
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
) found that approximately one-quarter of the units recorded in the inferotemporal cortex, the parahippocampal gyrus, and the hippocampal formation showed significantly altered activity with spontaneous saccadic eye movements. This was termed saccadic modulation. The activity occurred in the dark as well as in the light. The activity in the light could be measured in a time period before the slip of an image on the retina due to the eye movement could have affected unit activity. Thus its origin is extraretinal.
). This effect is a reduction in response to the representation of specific images, without any general fatigue in the neuron's responsiveness, which we have called a stimulus-specific adaptation (for review, see Brown 1996; Ringo 1996).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). During the experiment, the monkey was situated within two independent, oscillating magnetic fields, and the eye position was monitored by the method of Robinson (1963). The animals were trained to fix gaze on a series of calibration crosses, and a short calibration session was run every day before the experimental session. The eye position signal was sampled every 4 ms and stored together with information about spikes and behavioral events.
(measured at 1 kHz). During insertion, the electrodes were protected by a 0.3-mm stainless steel guard tube and lowered to within 10 mm of the recording site. A unit then was sought while advancing the electrode with a hydraulic microdrive. In each session, one, or sometimes two simultaneous, units were recorded using commercial recording and spike separation software (Datawave, Longmont, CO). Unit activity was separated from noise and the activity of other cells, off-line, on the basis of the shape and amplitude of spikes. Up to eight parameters such as latency and amplitude of different spike components, fit to template, and first and second principal components were used.
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FIG. 1.
Diagram of the positions (top) and timing (bottom) of events during experimental and control trials. In the experimental trial, a cross was presented for 750 ms, 7.5° to the left or to the right of the center of a screen located in front of the monkey. In this figure, only crosses positioned to the left of center are shown. Half the trials, interleaved, were performed with all stimuli at the symmetric position to the right of center. The monkey was initially required to fixate gaze inside a 3° window around the cross. This window is shown in the figure as a dotted circle. That dotted circle and the dotted line showing the axis did not appear on the display. After a 600- to 1,000-ms delay, a dot was presented, for 200 ms, 7.5° to the left, right, above, or below the position of the cross. The monkey then was required to make a saccade to the dot and keep a steady gaze within a 3° window for 
500 ms. Sequence of events in the control trial was similar to that in the experimental trial. Difference was that peripheral presentation of 1 dot was replaced with 4 dots in the periphery, for monkey M1 (as shown) or 1 central dot, for monkey M2, (not shown). To get its reward, the monkey had to withhold a saccade and keep a steady gaze (during 500 ms within a 3° window) on the position where the cross was presented previously. During recording sessions, 300 experimental and 150 control trials were run.
500 ms (within a circular window, 3° radius). A correct response was rewarded with a squirt of fruit juice.
.
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FIG. 2.
Regions where units were recorded are shown on standard brain drawings. Distance in millimeters, anterior to the external auditory meatus, is indicated. About 70% of the total number of units were recorded from monkey M1 (left hemisphere was used). In monkey M2 (still participating in other experiments), recordings were made from the right hemisphere. The fixed guide tube, inserted stereotactically, together with the rigid guard tube that protected the electrode, restricted accessible regions of recording to the marked areas.
). Instead, we used an analysis that examined how repeatable the shape of the unit response was after the cued saccade in different trials. We measured whether the spike distribution in a single trial could be predicted from the averaged spike distribution from all other trials (excluding the trial in question). The ability of this template to predict the spike pattern at a level greater than chance was used as the indication of a significant response. This method had the additional advantage, compared with a spike count in a fixed time bin, that it adjusts to the time course of the response of each unit.
where
(1)
n
is the number of saccades in the data set for the unit
Mi
is the inner product measure for a particular, i, saccade,
yij
is the amplitude of the response for a particular saccade, i, and an individual 20 ms bin, j. The amplitude is measured with respect to a presaccade baseline (defined from the 300-ms period just before saccade onset).
ykj
same as yij, index k substituting for index i.
), if the percentage of saccades for which the inner product measure, Mi, had positive values was significantly >50%. Fifty percent is the value expected by chance if there is no consistent response, and hence no predictive power from calculating the average response to all other saccades. A value significantly >50% indicates predictive power, hence a consistent response.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 3.
Cumulative spike histograms from an example unit showing results separated for control and the 4 directions. Below each histogram are the eye position records from the trials making up the histograms. Only correct trials are shown, and only such trials entered the main analysis. All the eye position records are displayed for the 4 histograms with saccades. For up and down directions, the vertical eye position is shown; for left and right directions, the horizontal eye position is shown. In the middle are data from control trials. To improve clarity, only alternate, horizontal eye position records are shown in that case. Other horizontal eye position records and the vertical ones show similar lack of movement. Zero in the histograms from trials with saccades is the onset of the saccade. Zero in the control trials is the onset of the 4 dots.
2 Hz. Only these more active units were analyzed to limit the number of trials with zero spikes in the period of interest. The numbers of units recorded from different regions are presented in Table 1. The anterior/posterior distinction used here was with reference to a coronal level at the posterior end of the anterior medial temporal sulcus and the anterior end of the occipital temporal sulcus. This divides area TE (Seltzer and Pandya 1978; Von Bonin and Bailey 1947) into approximately anterior and posterior halves, labeled aIT and pIT in the Table. The dorsal/ventral distinction (dorsal including TEa and TEm; ventral including TE1, TE2 and TE3) follows Seltzer and Pandya (1978).
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TABLE 1.
Results of statistical testing of saccadic modulation in units recorded from different brain regions
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FIG. 4.
Four examples (A-D) of units showing activity linked to externally cued saccades. Responses of the units to saccades in experimental trials are presented (top). Vertical line denotes the beginning of a saccade (defined as the first time point in which the speed of the eye was >15°/s). Corresponding response of the units in control trials also are presented (bottom). Vertical line denotes the onset of the control dot(s), which instructed the monkey to withhold eye movements. Only trials without any eye movements >1° for a 800-ms period beginning with the onset of the dot(s) were included in the analysis. A-C were recorded from monkey M1 (4-dot control). D was recorded from monkey M2 (1-dot control presented in the same position as the cross).
). However, there was no such difference in units with saccadic modulation linked to externally cued saccades (54 and 50%, respectively).
). Results are presented in Table 2. There were 12 units (17%) that showed direction sensitivity at a P < 0.01 level (probability after Bonferroni adjustment). Using a lower criterion (P < 0.05, Bonferroni corrected), 22 units (31%) showed directional sensitivity. Two clear examples of cells showing different target directed saccadic modulation for different directions are presented in Fig. 5.
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TABLE 2.
Number of units with saccadic modulation that showed significant directional and positional specificity of postsaccadic activity
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FIG. 5.
Directional sensitivity. Two examples (A and B) of units that show differential saccadic modulation for different directions of eye movement. A: greatest response was to saccades directed downward. B: saccades to the left produced an inhibition of the unit activity, whereas saccades to the right produced an increase in the unit activity. In neither unit was there any statistically significant response to dots in control trials. Both units were recorded from monkey M1.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Nowicka et al. 1996). The current study has the advantage that it clearly could separate influences of gaze position from the saccades that preceded those fixation episodes. If one equates the place viewed by the monkey with the place occupied by the rat, these units may, in some ways, be reminiscent of head-direction cells recorded in the rat subiculum, and elsewhere (Taube et al. 1990), or hippocampal place cells (Muller and Kubie 1987; O'Keefe and Speakman 1987). However, our experiments do not provide conditions to separate the direction the eye is pointed with respect to the head and/or the rest of the body from the direction of the eye in spatial coordinates independent of the body.
), we found robust saccadic modulation related to spontaneous eye movements. The current work shows that saccades directed by an external command also produce extensive saccadic modulation in the same areas. This makes it clear that the modulation was not peculiar to saccades in a monkey unoccupied by any task. The current work also suggests that the saccadic modulation is not due to some internal state change, which itself is not directly related to saccades but which simply correlates with saccades. From previous work, it was possible to suppose that both spike activity in the temporal lobe recordings and spontaneous saccades stemmed from a shared preceding event but were not themselves causally linked. For example, one might suppose that the neural circuitry had reached a "decision" or a break point in some internal state, perhaps related to attention, that would lead to both activity in units in the temporal lobe recording regions and to an increased tendency to make a saccade but that the temporal lobe unit activity and the saccade were not directly related. The current work, showing robust and short-latency activity with externally commanded saccades, indicates that these are liable to be related more directly.
; Büttner and Büttner-Ennever 1988).
; Riches et al. 1991; Richmond et al. 1983; Rolls 1987; Sobotka and Ringo 1993). In agreement with such a possibility, we have found recently that saccades approximately doubled the stimulus specific adaptation seen widely in inferior temporal cortex (Nowicka et al. 1995). Indeed, such effects may be part of the mechanism of the cognitive role saccades have long been thought to play (see, for example, the still cogent arguments for a role of eye movements in perceptual learning made in Chapter 2 of Hebb 1949).
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ACKNOWLEDGEMENTS |
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We thank S. O'Neill and M. Diltz for expert technical assistance and J. DiGiorgianni for valuable discussion.
This work was supported by National Institute of Neurological Disorders and Stroke Grant NS-26526.
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FOOTNOTES |
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Address for reprint requests: J. L. Ringo, Box 603, Dept. of Neurobiology and Anatomy, University of Rochester, Rochester, NY 14642.
Received 13 December 1996; accepted in final form 18 June 1997.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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