1 Institute of Neuroscience, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, 320 Yue-Yang Road, Shanghai, 200031, China, 2 Graduate School of the Chinese Academy of Sciences
Address correspondence to Chao-Yi Li, Institute of Neuroscience, Chinese Academy of Sciences, 320 Yue-Yang Road, Shanghai, 200031, China. Email: cyli{at}sibs.ac.cn.
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Abstract |
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Key Words: classical receptive field contextual modulation extra-receptive field monkey striate cortex suppression
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Introduction |
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In the present study, we used an iso-orientation paradigm to stimulate the CRF and ERF of V1 neurons in alert monkeys. By varying the relative spatial phase (RSP) between the central (CRF) and the surround (ERF) gratings, we investigated whether neurons in primate V1 are sensitive to the RSP. In a similar experiment, DeAngelis et al. (1994) found that most cells in V1 of anesthetized cat were not sensitive to the RSP between the CRF and ERF. In the present study, however, we have found significant neuronal sensitivity to RSP in V1 of the alert monkey. We further examined the dependence of the RSP sensitivity on the ERF property and on the spatial configuration of the center and surround stimuli.
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Materials and Methods |
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Experiments were performed on two female Macaca mulatta weighing 4.55.5 kg during the experimental period. All experimental procedures were performed in accordance with the National Institutes of Health guidelines. The monkey sat in a restraining chair that allowed movement of the head. Juice was given as a reward for performing the task. The animal was trained to fixate at a small spot (0.3° in diameter) located at the center of a monitor placed at a distance of 57 cm from the eyes. When the monkey pressed a lever, a trial began with the fixation point appearing as a white spot. After a variable delay of 0.55 s, the spot changed color to light yellow and the lever had to be released within 500 ms for a successful trial. Then, the fixation spot was extinguished until the next trial began. During this interval, the monkey received a drop of juice if the trial was successful. Once the monkey learned the task, a head-restraining implant, as well as a stainless steel recording chamber overlaying areas V1 and V2, were surgically attached to the skull. Surgery was conducted under aseptic conditions while the monkey was under deep pentobarbital anesthesia. A remote, infrared eye tracker (ASL Model 504, resolution 0.25° visual angle, system accuracy 0.5° visual angle) monitored the fixation and eye movements during post-operative training and throughout the experiments.
Recordings
Activity from single neurons or clusters of neurons was recorded extracellularly with glass-coated tungsten electrodes prepared according to the method of Li et al. (1995). The electrode was inserted through the intact dura by means of a hydraulic micro-drive mounted on the chamber. Responses were recorded from neurons in the striate cortex whose CRFs were at eccentricities in the range of 36°. Nerve impulses, after being converted to standard pulses by a window discriminator, were fed into a computer, along with eye position data for real-time monitoring and analysis. Both the behavioral and physiological data were processed using software written in our laboratory. During fixation trials, eye position was continuously sampled at 60 Hz. A fixation window (1°) was set and centered on the fixation position, so that deviations of the eye position from the fixation point resulted in cancellation of the trial. To confirm that the recording sites were in V1, the CRF positions of the neurons in each penetration were traced according to the topographic mapping of V1, and the recording depth was determined with reference to the reading on the electrode manipulator and the response properties characteristic of layer 4 cells (little or no orientation selectivity, synchronized with light on and off). When more than one neuron was recorded simultaneously, the spikes from different neurons were differentiated on the basis of both amplitude and slope of the spike waveform.
Visual Stimuli
A computer (Pentium III, 800) with a graphics card (Gforce GTS) was used to generate visual stimuli and the fixation point on the monitor (frame rate, 85 Hz). The screen was 40 x 30 cm. This visual stimulator could generate multiple patches of sinusoidal or line-grating stimuli of various sizes, spatial frequencies, orientations, velocities and contrasts. The stimulus patterns consisted of two gratings with a mean luminance of 10 cd/m2 and a contrast of 0.95. The small rectangle grating was set to have the same size and location as the CRF of the recorded neuron and the large rectangle grating in the ERF covered both the inhibitory end and side regions. Various RSP (0330°) was introduced between the CRF and ERF grating stimuli. To test the spatial phase tuning of the end and side regions separately, elongated gratings extending along either the length or the width of the CRF were used. The center grating stimulated the CRF, while the bilaterally elongated grating stimulated either the end or the side regions.
Data Analysis
Data collection was synchronized with the stimulus presentation, which began at the on-set of the stimulus and ended at the termination of the stimulus. To quantify the neuronal responses, we computed the mean firing rate over the entire period of the stimulus presentation (23 cycles of drifting gratings, 5001000 ms), but the results were similar if the period immediately following stimulus onset (50100 ms) was excluded. For each stimulus configuration, the responses to 520 repeats were averaged.
Determination of the CRF and ERF
The procedures were identical to those described in a previous paper (Li and Li, 1994). Briefly, to locate the center of CRF, a small rectangular gating patch (typically 0.1 x 1°) was moved at successive positions along axes perpendicular or parallel to the optimal orientation of the cell as the monkey fixated. The peak in the response profile along the length and width axes was defined as the center of the CRF, and the length and width of the CRF were determined by the distance between the bases of the rising and falling sections of the curves. The ERF properties of the neuron were assessed with reference to the spatial summation properties. To determine a neuron's length-summation curve, patch width was held constant (equivalent to the CRF's width) and the grating length was varied systematically. A similar method was used to determine a neuron's width summation curve. In V1 of the alert monkey, the majority of cells show suppression at both the end and side regions. Consequently, both the length and width summation curves decline when the stimulus length or width extends into the end or side regions. The length (or width) at which the response decreases to the spontaneous level reflects the dimensions of the end (or side) regions.
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Results |
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Relative Spatial Phase Tuning of V1 Cells
We presented the centersurround sinusoidal grating stimuli at the optimal orientation and spatial frequency drifting in the optimal direction, with the central grating confined to the CRF and the surround grating to the ERF. The two gratings drifted at the same speed, but their RSP varied randomly from trial to trial with an interval of 30° phase shift. Within each trial, the RSP between the CRF and ERF gratings was held constant, and the responses were recorded for 23 cycles of the drifting grating; for each RSP the data from 520 trials were averaged (Fig. 1). Since no substantial difference was found between the simple and complex cells in their RSP tuning properties, we grouped them together in subsequent analyses.
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We further analyzed the relationship between spatial phase sensitivity and the strength of ERF suppression. The neuronal RSP sensitivity was quantified by the index of spatial phase sensitivity (SPS), which was defined as:
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We analyzed the relationship between SPS and the suppression index for a total of 86 cells from two monkeys (55 in monkey A and 31 in monkey B). Figure 4a shows the relationship when both the end and the side regions of the ERF were stimulated. A significant correlation was found (r2 = 0.54, P < 0.01, regression slope = 0.87). Figure 4b and 4c depict the relationship between SPS and the suppression index for end-suppression (r2 = 0.78, P < 0.01, regression slope = 0.87) and side-suppression (r2 = 0.46, P < 0.01, regression slope = 0.69), respectively. Thus, SPS is strongly correlated with the strength of ERF suppression, suggesting a causal relationship between them.
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In the experiments described thus far, SPS was measured when the center grating was confined to the CRF and the RSP was placed at the boundary between the CRF and the ERF. To explore the spatial extent of the modulation, we systematically changed the location of the RSP within the ERF. Figure 5a shows the result from a cell with a 0.5° CRF and a 3° ERF with extremely strong surround suppression (suppression index = 0.97). The RSPresponse curves of the cell were measured at various sizes of the center grating (0.5, 1.0, 1.5, 2.0 and 2.5°). We found that RSP modulation occurred across the entire ERF, although the amplitude decreased with the size of the center grating. As shown in Figure 5b, SPS was highest at the CRF border (0.5 x 0.5°) and at 0.25° away from the border (1.0 x 1.0°) and diminished with increasing distance, disappearing at the border of the ERF (2.5 x 2.5°). The data presented in Figure 5c were obtained from another cell with a 0.6° CRF and 2.3° suppressive end region (suppression index = 0.42). The SPS also exhibited a gradual decay from the CRF border to the ERF border. Thus, although SPS is strongest at or near the CRF/ERF boundary, the entire ERF contributes to the modulatory effect.
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A prerequisite for V1 cells to detect spatial phase difference between the CRF and ERF stimuli is that the terminations of constituent lines at the boundary must be conjunctive. To demonstrate this, we conducted an experiment in which narrow gray gaps were introduced at the boundary between the center and the surround gratings. The RSPresponse curves measured with the gap were compared with those without the gap. An example is shown in Figure 6 for a cell with a 1.5° CRF and a 4° suppressive ERF. Without the gap, we observed a normal RSP modulation, with complete suppression at 0° RSP and a maximum response at 240° RSP (SPS = 0.75) (Fig. 6a). When small (0.2°) gray gaps were introduced, the SPS decreased substantially, although it was still detectable (Fig. 6b). As the gap size increased to 0.5°, the SPS was completely abolished (Fig. 6c). This effect indicates that the spatial conjunction of displaced gratings at the interface between CRF and ERF is crucial for the SPS of V1 cells.
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For most cells, a small RSP at the interfaces can produce a substantial release of end-suppression. This implies that V1 cells are capable of detecting small displacements in straight lines at the interfaces. In order to obtain a more precise measurement of this capacity of V1 cells, we determined the minimum RSP that caused 50% reduction of ERF suppression (half-height release) at various spatial frequencies. The visual angle corresponding to the RSP was calculated as
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Figure 7ac shows the RSPresponse curve of an example cell tested at three spatial frequencies. At 0.5 c/deg, Dmin was 30° RSP (Fig. 7a). When the spatial frequency increased to 0.8 c/deg (Fig. 7b), Dmin shifted to 45°. Further increasing the spatial frequency to 1.5 c/deg caused a shift of Dmin to 75° RSP (Fig. 7c). At these spatial frequencies, SR was found to be 0.167, 0.156 and 0.139°, respectively, which was approximately constant. Such spatial-frequency invariance allows assessment of the spatial resolution at which the cortical cell can detect the displacement of edges or line segments at the CRF/ERF border. For the cell shown in Figure 7ac, the mean SR was 0.154 ± 0.015°, corresponding to the displacement of line segments shown in Figure 7d, which was 6% of the CRF size. For a population of 42 cells analyzed, the mean SR was 0.14 ± 0.07°, which was 6.9 ± 5.4% of the CRF size (Fig. 7e). Such a high spatial resolution of the striate cortical cells in detecting line displacement at the interface between CRF and ERF may serve useful perceptual functions.
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Discussion |
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We found significant SPS over the entire ERF, but the effect is strongest at the CRF/ERF border, declining monotonically from the CRF border to the ERF border (see Fig. 5b,c). This result is consistent with the findings of Rossi et al. (2001), in which the magnitude of the response to an orientation-defined figure was dependent on the distance between the boundary of the figure and the border of the CRF, with a maximum at, or in close proximity to, the CRF border. Rossi et al. suggested that this effect is due to the response of the neuron to the orientation-defined boundary within the RFs. Here we propose an alternative interpretation. Our data showed that for most neurons with small CRFs (
1° in diameter) and strongly suppressive ERFs (suppression index > 0.9), the suppressive zone is often confined to a narrow space (typically 4° in diameter or smaller). When we expanded the grating stimulus from CRF into ERF, the response of the neuron decreased gradually and reached 70% reduction when the stimulus was 3° in diameter. Under such a condition, the surrounding grating (with 0° RSP) will exert little suppressive effect even at 0° RSP, thus changing the RSP does not significantly affect the neuronal response. This is why many neurons show obvious sensitivity to RSP at small central grating sizes (2° or less in diameter), but little or no RSP sensitivity when the central gratings reach 3° or more in diameter.
As shown in Figures 6 and 7, the suppression at 0° RSP can be largely eliminated by a small shift of the surround grating in either the horizontal (thus leaving a small gap between the center and surround gratings, Fig. 6) or vertical (thus creating a small RSP, Fig. 7) direction. The spatial resolution at which the cells can detect the shifts corresponds to a small fraction of the CRF size. The effect of the gap between the center and surround gratings has been studied previously in anaesthetized cat (Akasaki et al., 2002), which was found to be spatially co-extensive with the suppressive effect of the surround (i.e. the suppression is abolished only when the gap covers the entire suppressive surround). This is different from our finding that the suppression at 0° RSP was greatly reduced by including a small gap with a width of 0.5° (a small fraction of the width of the suppressive surround), leaving a small component of the suppression that is not phase sensitive. It is possible that this phase-insensitive component is analogous to the suppressive effect found in the cat, which is spatially co-extensive with the surround (Akasaki et al., 2002
), where as the phase-sensitive component that can be abolished by the small gap represents an additional effect in the awake primate. As discussed above, this difference may be due to the difference in the animal preparation.
Another important difference between the studies in anesthetized and awake, behaving animals is the presence of eye movement. In the present study, we used a 1° fixation window to determine whether a trial is included for analysis. Due to the variability of eye position in different fixation trials within this window, the boundary between the center and the surround stimuli may fall in different locations relative to the neuronal RF, leading to inaccuracy in the measurement of the SPS extent (Fig. 5). In addition, if the boundary falls within the CRF in some trials, the edge created by RSP may contribute to the response through the CRF. Note, however, that the variability in fixation position similarly affects our measurement of the CRF border, causing an overestimate of the size of the CRF. The mean CRF size among our cells was 1.27 ± 0.6° (n = 26) in monkey A and 1.17 ± 0.34° (n = 31) in monkey B, larger than that reported by others at similar eccentricities (0.52° in Lamme et al., 1999; 0.69° in Ito and Gilbert, 1999
). Thus, the boundary between the center and surround stimuli that we set at the estimated CRF border is likely to be outside of the real CRF, which should reduce the probability that the stimulus boundary falls within the CRF.
In conclusion, the RSP modulation we have found in awake monkeys was different from that observed in anesthetized cats. The exquisite sensitivity of V1 neurons to the center/surround stimulus configuration may serve important perceptual functions.
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Acknowledgments |
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References |
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Allman J, Miezin F, McGuinness E (1985) Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for localglobal comparisons in visual neurons. Annu Rev Neurosci 8:407430.[CrossRef][ISI][Medline]
Bishop PO, Coombs JS, Henry GH (1973) Receptive fields of simple cells in the car striate cortex. J Physiol 231:3160.[ISI][Medline]
Blakemore C, Tobin EA (1972) Lateral inhibition between orientation detectors in the cat's visual cortex. Exp Brain Res 15:439440.[ISI][Medline]
DeAngelis GC, Freeman RD, Ohzawa I (1994) Length and width tuning of neurons in the cat's primary visual cortex. J Neurophysiol 71:347374.
De Valois RL, Thorell LG, Albrecht DG (1985) Periodicity of striate-cortex-cell receptive fields. J Opt soc Am A 2:11151123.[ISI][Medline]
Gilbert CD, Wiesel TN (1990) The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Res 30:16891701.[CrossRef][ISI][Medline]
Hubel DH, Wiesel TN (1965) Receptive fields and functional architecture in two nonstriate visual areas (18 and, 19) of the cat. J Neurophysiol 28:229289.
Ito M, Gilbert CD (1999) Attention modulates contextual influences in the primary visual cortex of alert monkeys. Neuron 22:593604.[CrossRef][ISI][Medline]
Jones HE, Andolina IM, Oakely NM, Murphy PC, Sillito AM (2000) Spatial summation in lateral geniculate nucleus and visual cortex. Exp Brain Res 135:279284.[CrossRef][ISI][Medline]
Jones HE, Grieve KL, Wang W, Sillito AM (2001) Surround suppression in primate V1. J Neurophysiol 86:20112028.
Knierim JJ, van Essen DC (1992) Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J Neurophysiol 67:961980.
Lamme VA, Super H, Spekreijse H (1998a) Feedforward, horizontal, and feedback processing in the visual cortex. Curr Opin Neurobiol 8:529535.[CrossRef][ISI][Medline]
Lamme VA, Zipser K, Spekreijse H (1998b) Figure-ground activity in primary visual cortex is suppressed by anesthesia. Proc Natl Acad Sci USA 95:32633268.
Lamme VA, Rodriguez-Rodriguez V, Spekreijse H (1999) Separate processing dynamics for texture elements, boundaries and surfaces in primary visual cortex of the macaque monkey. Cereb Cortex 9:406413.
Levitt JB, Lund JS (1997) Contrast dependence of contextual effects in primate visual cortex. Nature 387:7376.[CrossRef][ISI][Medline]
Li CY, Li W (1994) Extensive integration field beyond the classical receptive field of cat's striate cortical neurons classification and tuning properties. Vision Res 34:23372355.[CrossRef][ISI][Medline]
Li CY, Xu XZ, Tigwell D (1995) A simple and comprehensive method for the construction, repair and recycling of single and double tungsten microelectrodes. J Neurosci Methods 57:217220.[CrossRef][ISI][Medline]
Li CY, Lei JJ, Yao HS (1999) Shift in speed selectivity of visual cortical neurons: a neural basis of perceived motion contrast. Proc Natl Acad Sci USA 96:40524056.
Maffei L, Fiorentini A (1976) The unresponsive regions of visual cortical receptive fields. Vision Res 16:11311139.[CrossRef][ISI][Medline]
Nelson JI, Frost BJ (1978) Orientation-selective inhibition from beyond the classic visual receptive field. Brain Res 139:359365.[CrossRef][ISI][Medline]
Nothdurft HC, Gallant JL, Van Essen DC (1999) Response modulation by texture surround in primate area V1: correlates of popout under anesthesia. Vis Neurosci 16:1534.[CrossRef][ISI][Medline]
Orban GA, Kato H, Bishop PO (1979) End-zone region in receptive fields of hypercomplex and other striate neurons in the cat. J Neurophysiol 42:818832.
Rose D (1977) Responses of single units in cat visual cortex to moving bars of light as a function of bar length. J Physiol 271:123.[ISI][Medline]
Rossi AF, Desimone R, Ungerleider LG (2001) Contextual modulation in primary visual cortex of macaques. J Neurosci 21:16981709.
Sillito AM, Grieve KL, Jones HE, Cudeiro J, Davis J (1995) Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378:492496.[CrossRef][ISI][Medline]
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