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1 Graduate School of Biosphere Sciences, Hiroshima University, Hiroshima 739-8521, Japan 2 Department of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, Aichi 484-8506, Japan 3 Precursory Research for Embryonic Science and Technology, Japan Science and Technology Corporation, Kawaguchi 332-0012, Japan
Submitted 5 December 2002; accepted in final form 23 April 2003
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ABSTRACT |
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INTRODUCTION |
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;
Van Hoesen 1982). However,
there are differences in anatomical connections between the PH and PR
cortices. The PR cortex receives cortical inputs principally from area TE, the
higher-order visual area related to object vision
(Martin-Elkins and Horel 1992;
Suzuki and Amaral 1994;
Webster et al. 1991). Neurons
in area TE are known to have large, nontopographically organized visual
receptive fields (RFs), which almost always include the center of gaze
(Desimone and Gross 1979;
Gross et al. 1972;
Tanaka et al. 1991). On the
other hand, the PH cortex receives inputs from various cortical areas such as
the inferior temporal, posterior parietal, prefrontal, and cingulate cortices
(Barnes and Pandya 1992;
Cavada and Goldman-Rakic 1989;
Distler et al. 1993;
Goldman-Rakic et al. 1984;
Jones and Powell 1970;
Martin-Elkins and Horel 1992;
Seltzer and Pandya 1976,
1984,
1991;
Suzuki and Amaral 1994). The
PH cortex receives inputs only from the peripheral visual field representation
of areas V2 and TEO (Distler et al.
1993; Gattass et al.
1997). These anatomical characteristics suggest that the PH cortex
receives information from the peripheral as well as central visual fields,
whereas the PR cortex principally receives information from the central visual
field related to object vision.
So far the effect of the lesion of the PH cortex is not unclear, but
neuropsychological studies suggest some functional differences between the PH
and PR cortices. A lesion in the PR cortex induces deficits in various visual
recognition memory tasks, such as delayed nonmatching-to-sample tasks (e.g.,
Buckley et al. 1997;
Meunier et al. 1993), whereas
that in the PH cortex does not (Ramus et
al. 1994). A few studies suggest that combined lesions of the PH
and the other area induce some impairment. Lesions in both the PH and PR
cortices produce deficits in a tactual memory task
(Suzuki et al. 1993) and those
in both the PH cortex and hippocampus produce deficits in spatial memory tasks
(Angeli et al. 1993;
Parkinson et al. 1988).
Neuronal responsiveness in the PR cortex has been relatively well
investigated in the context of visual memory tasks (e.g.,
Miller et al. 1993;
Nakamura et al. 1994;
Riches et al. 1991). Those
studies found that neurons in the PR cortex responded selectively to complex
visual stimuli such as images. In contrast, response properties of PH neurons
are poorly understood. Riches et al.
(1991) examined visual
response properties of various areas in the medial temporal lobe using simple
geometrical shapes and reported that the stimulus selectivity in the PR cortex
and area TE was higher than that in the PH cortex and hippocampus. Boussaoud
et al. (1991) examined an RF
property of neurons in the posterior portion of the inferior temporal cortex
and reported that neurons in the posterior portion of the PH cortex (area VTF)
had a relatively small, contralateral RF and tended to have a visuotopographic
organization. Nakamura et al.
(1994) examined neuronal
responses to images of various natural objects in the anterior medial temporal
areas and reported that neurons in the PH and PR cortices selectively
responded to complex visual stimuli. However, these studies did not focus on
the function of PH neurons. Creutzfeldt and colleagues attempted to elucidate
the functions of the hippocampus and PH cortex and reported that PH neurons
responded to some obscure events (e.g., opening or closing of a door of a
shielded room; Salzmann et al.
1993; Vidyasagar et al.
1991). Thus response properties of PH neurons are still
unclear.
In the present study we examined visual response properties of PH neurons,
such as an RF property, a direction selectivity, and selectivities for images,
shapes, and colors to elucidate the role of the PH cortex in visual
processing. For some aspects we further compared visual response properties of
PH neurons with those of PR neurons. Based on the previous studies described
above, it is expected that neurons in the PH cortex convey more information
concerning spatial processing, whereas those in the PR cortex do more
information concerning object processing
(Nakamura and Kubota
1996).
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METHODS |
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Three male rhesus monkeys (Macaca mulatta, 4.5–6.2 kg, 3- to 5-yr-old) were used as subjects. Each monkey was housed in an individual cage. Water was withheld before each daily session and juice was given as reward in an experimental room. Supplemental water and fruit were given after the session, when needed. Food (monkey chow) was available ad libitum. All experiments were performed in accordance with the guidelines outlined in the "Guide for the Care and Use of Laboratory Animals" of the National Research Council (1996) and the "Guide for Care and Use of Laboratory Primates" published by Primate Research Institute, Kyoto University (1986, 2002).
Behavioral procedure
All experiments were performed in a dark soundproof room. Each monkey was seated in a primate chair with its head fixed by a head-restraining device during the experimental session. All of the monkeys had been habituated to the experimental room and the primate chair with the head restraint. A 20-in. CRT monitor was placed 28 cm from the monkeys' eyes. During the experiment, the monkeys' behavior was monitored by an infrared camera, and was observed through a TV monitor. The monkeys were trained to perform visual reaction time and delayed nonmatching-to-sample tasks by pressing and releasing a lever attached to the primate chair (Fig. 1).
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VISUAL REACTION TIME TASK. Each trial started by the monkey pressing the lever. After the monkey pressed the lever and kept it pressed for 1.5 s, a circular fixation spot (0.6 deg in diameter) was presented at the center of the monitor display. The monkey was required to fixate the spot within 3 deg for 3.5–5.0 s and to release the lever when the spot was replaced by a cross. If the monkey correctly released the lever within 0.8 s of the presentation of the cross, a drop of juice (approximately 0.4 ml) was administered as a reward. If the monkey broke fixation or released the lever during the trial, the trial was aborted without any rewards. After the monkey started to fixate the spot for 1.0 s, a visual stimulus was presented for 0.5 s.
DELAYED NONMATCHING-TO-SAMPLE TASK. The monkey had to press the lever and keep it pressed throughout a trial in the delayed nonmatching-to-sample task. After a waiting period of 1.5 s, a fixation spot (0.6 deg in diameter) was presented at the center of the monitor. After the monkey fixated the spot within 5 deg for 0.5 or 1.0 s (usually 1.0 s), a sample stimulus was presented for 0.5 s. After the sample stimulus was presented repeatedly one to three times (at random) with a delay period of 1.5 s, a different (nonmatching) stimulus was presented. The monkey was required to remember the sample stimulus during the delay period, to maintain its fixation on the spot throughout a trial, and to release the lever within 0.8 s of the presentation of the nonmatching stimulus. If the monkey correctly released the lever, a drop of juice was given as a reward. If the monkey released the lever before the nonmatching stimulus presentation or broke fixation at any time during the trial, the trial was aborted without providing any rewards.
First the monkey was trained to perform both tasks without eye control. After a surgery to implant a head-restraining device, the monkey was retrained in the tasks with eye control.
Visual stimuli
We prepared 3 types of visual stimuli: bars, geographical shapes, and images. The bar and shape stimuli were generated by a personal computer to present equiluminantly in 5 colors (blue, green, yellow, red, and white). The bar was a rectangle subtending the visual angle of 0.6 x 8 deg. A set of the shape stimuli consisted of 8 simple geometrical patterns (see Figs. 7B and 8B). The images were full-colored images of a human face, a monkey face, a fruit, and a tool. These image stimuli were presented on the monitor by a personal computer via a video board (Canopus, Kobe, Japan). Each image was presented with a gray square (14 x 14 deg) as the background. The images of a human or monkey face were whole-faced calm facial images. A set of the image stimuli consisted of 2 images of each category (8 images in total). Two sets of image stimuli were prepared (see Figs. 7A and 8A).
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Surgery
After the monkey had learned visual reaction time and delayed nonmatching-to-sample tasks, a head-holding device was implanted. After the monkey performed both tasks with eye control at a level of >90% correct responses, a recording cylinder was implanted. The surgery was carried out under pentobarbital sodium anesthesia (20–25 mg/kg, intravenous). Antibiotics were administered postoperatively for >1 wk to protect against infection. After a recovery period of >10 days, retraining was started.
Recording procedure
During recording, the monkey's head was tightly fixed to a chair frame. The
activity of single neurons was recorded extracellularly with a
polyurethane-coated tungsten or cobalt-nickel alloy including iron (Elgiloy)
microelectrode (1.5–3.0 M
, 0.3 mm in diameter). We inserted a
stainless steel guide tube (50 mm in length, 1.1 mm in diameter) to
10–20 mm below the surface of the dura to penetrate an electrode without
distortion and to allow accurate placement of the electrode into the deepest
brain site. For parallel penetration of the guide tube and electrodes, we used
a grid system (Crist et al.
1988). The electrode was advanced using a hydraulic microdrive
(Narishige, Tokyo, Japan).
Neuronal activity was amplified and converted into pulses using a window discriminator (BAK Electronics, Germantown, MD). The timings of each pulse and task events were stored on disks with a resolution of 0.5 ms using a personal computer. The neuronal activity was transmitted to another computer to generate on-line peristimulus time histograms.
When a single neuron was isolated, we tested response properties of this neuron according to the following procedure (Fig. 2). First, we manually determined the optimal stimulus position using basic stimuli of 4 shapes (Fig. 2) with 4 colors (red, green, blue, and white) using a computer mouse. If we could not determine the optimal stimulus position manually, we presented visual stimuli at the center of gaze to perform the following tests. We examined the orientation selectivity of the neuron using 4 oriented bar stimuli presented at the manually determined optimal position (Fig. 2). Using the optimally oriented bar stimulus, we next examined the color selectivity of the neuron using 5 colors [blue, 0.143 (X), 0.119 (Y); green, 0.289, 0.670; yellow, 0.432, 0.535; red, 0.584, 0.372; white, 0.273, 0.303]. Using the optimally oriented and colored stimulus presented at 3 x 3 grid positions (including the optimal stimulus position but excluding the center), we next examined systematically each neuron's RF property and determined the position where the stimulus induced the maximal response of the neuron. We also investigated the direction selectivity of the neuron using a bar stimulus moving in 8 directions in steps of 45 deg (Fig. 2). The moving distance and speed were 14 deg and 28 deg/s, respectively.
After the orientation, color, position, and direction tests or if the bar stimuli did not induce responses in the neuron, we examined whether the neuron responded to the shape and image stimuli presented at the center of gaze. If the bar stimuli could not induce the responses but the shape or image stimuli induced the responses, we examined the RF property using the shape or image stimuli (7/25 neurons in the PR cortex). All of the tests using the bar stimuli were carried out during the visual reaction time task. Parts of the data in the shape and image tests were obtained using stimuli presented during the delayed nonmatching-to-sample task (29/40 neurons in the PH cortex and 11/88 neurons in the PR cortex).
Eye position measurement
To determine the monkey's eye position, a measurement system equipped with
a charge-coupled device (CCD) camera and an infrared ray irradiation device
was used. From an eye image, the center of an approximated oval fitted to the
pupil was obtained. The monkey's eye position was computed by transforming the
coordinates of the center in the eye image into the vector of the eye
direction (Matsuda 1996;
Sato and Nakamura 2001). The
eye position data were obtained with a resolution of 0.7 deg at a sampling
rate of 30 Hz. At the beginning of each daily session, the eye measuring
system was calibrated during the visual reaction time task using 9 locations
of a fixation spot arranged in a 3 x 3 grid, 20 deg apart from each
other.
Data analysis
Neuronal data stored in disks were analyzed off-line. A period of 0.5 s before the stimulus presentation was used as the control period. We regarded a neuron as responsive to a visual stimulus if the number of spikes during visual stimulation was significantly different from that during the control period (Wilcoxon ranked sum test, P < 0.05). With regard to the data obtained in the delayed nonmatching-to-sample task, the number of spikes during the first sample stimulus presentation was compared with that during the control period. For the data in the direction test, the number of spikes from 250 to 750 ms after the stimulus onset was analyzed.
We calculated the response latency of each visually responsive neuron from the maximal response of the neuron. We measured the time of the first of consecutive bins differing from the discharge rate during the control period by >2SDs.
If a neuron showed differential responses to different stimuli in a
stimulus set (Kruskal–Wallis test, P < 0.05), the neuronal
response was considered to be stimulus selective. To evaluate the strength of
stimulus selectivity, we used Kruskal–Wallis's H value as the index for
the selectivity. This index approaches zero if the responses to different
stimuli are not different and increases as the difference becomes prominent.
Because the H value has an approximate chi-square distribution, it can be
regarded as an index for dispersion. To compare the present results with those
of pervious studies, we also calculated the selectivity index (SI) used by
Rainer and Miller (2000).
To evaluate the RF property of each neuron, we classified the types of RF into 5 categories. If a neuron has an RF extending more than 10 deg from the vertical meridian to the contralateral, ipsilateral, or bilateral visual field, we regarded the neuron as having a contralateral, ipsilateral, or bilateral RF. If a neuron has an RF extending no more than 10 deg from the vertical meridian and extending more than 10 deg from the horizontal meridian, we regarded the neuron as having a vertical RF. If a neuron has an RF extending no more than 10 deg from both the horizontal and vertical meridians, we regarded the neuron as having a central RF.
Histology
Microlesions were made at 2 or 3 sites of representative recording tracks
by passing an anodal current (3–4 µA, 600 µC) through Elgiloy
microelectrodes. After all of the recording sessions, the monkeys were deeply
anesthetized with pentobarbital sodium (30–35 mg/kg, intravenous), and
perfused with saline and 10% buffered formalin. Ferrocyanide (2%) was mixed
with the formalin solution and the mixture was used to stain iron deposits
from the Elgiloy electrodes by the Prussian blue reaction. The brains were
frozen and sectioned coronally at 50- or 100-µm intervals, and stained with
cresyl violet. The locations of neurons were determined using the sites of the
microlesions as reference points. Area boundaries were determined based on the
previous studies (Bonin and Bailey
1947; Goldman-Rakic et al.
1984; Insausti et al.
1987; Suzuki and Amaral
1994; Tranel et al.
1988; Yukie
2000).
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RESULTS |
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We also examined the activity of 189 neurons in the PR cortex. Of these
neurons, 81 neurons (43%) were regarded as visually responsive. The proportion
of visually responsive neurons was significantly higher in the PR cortex than
that in the PH cortex (
2 = 10.68, df = 1, n = 548,
P < 0.005). Of these visually responsive neurons, 93% (75/81)
showed excitatory responses. The control rate of these neurons ranged from 0.0
to 17.4 spikes/s (2.2 ± 4.0 spikes/s) and were significantly lower than
those of PH neurons [t(176) = 3.70, P < 0.001]. The
discharge frequencies of the maximal excitatory responses ranged from 1.0 to
87.2 spikes/s (16.4 ± 13.6 spikes/s) and were significantly higher than
those of PH neurons [t(153) = 3.14, P < 0.005]. The mean
onset latencies were 170 ± 83 ms and were not significantly different
from those of PH neurons.
During recording sessions, the monkeys made few errors in behavioral tasks, except for error in fixation, averting its gaze outside of the electronic window. The proportions of correct responses for the 3 monkeys were more than 98%. Including the fixation errors, the proportions of correct responses were 83.1 ± 14.7, 76.4 ± 12.1, and 77.2 ± 10.2% (means ± SD). The reaction times for the 3 monkeys were 264 ± 47, 362 ± 57, and 414 ± 51 ms, respectively.
Spatial information
RECEPTIVE FIELD PROPERTY. We systematically examined the RF
property of 36 PH neurons (Fig.
3A). Of these neurons, 22 (61%) had bilateral, 3 (8%) had
contralateral, 0 (0%) had ipsilateral, 2 (6%) had vertical, and 9 (25%) had
central RFs. For 8 of the 36 PH neurons (22%), the RF did not include the
center of gaze (e.g., Fig.
3Ab). We examined the optimal stimulus position where a
stimulus induced the maximal response of the neurons
(Fig. 4). About one-half of the
PH neurons (47%, 17/36) had the optimal stimulus position within 10 deg of the
center of gaze, whereas the remaining neurons (53%) had that with an
eccentricity of more than 10 deg (Fig.
4A). We also examined 25 visually responsive neurons in
the PR cortex. The RF of the PR neurons always included the center of gaze and
most neurons (80%, 20/25) had the optimal stimulus position around the center
of gaze (Fig. 4B). The
proportion of neurons having the "central" optimal stimulus
position was significantly higher in the PR cortex than in the PH cortex
(2 = 6.64, df = 1, n = 61, P < 0.01).
These data indicate that PH neurons receive more information from the
peripheral visual field than PR neurons.
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Differences in neuronal responses as to the stimulus positions may be attributed to differences in the monkey's eye position and eye movement. For example, a PH neuron in Fig. 3Ba showed stronger responses to the stimulus presented in the lower ipsilateral quadrant of the visual field (b) than that presented in the more distant, contralateral visual field (c–e). During the stimulus presentation, there were no apparent differences in eye position. As shown, horizontal eye position (x in Fig. 3, Bb, Bc, Bd, and Be) was within 1 deg. Vertical eye position (y) was more variable than the horizontal one, but was within 2 deg. In addition, there were no large saccadic eye movements defined by more than 1-deg shift of visual angle within 20 ms (Fig. 3, Bb, Bc, Bd, and Be). Similarly, no large saccadic eye movements were observed during recordings of the other 8 neurons. For the remaining neurons investigated, only a few saccadic eye movements were recorded. On average, 0.07 times saccadic eye movements per trial were observed in the investigated 11 neurons. There was no correlation between the number of the saccadic eye movements and that of spikes. Therefore it is unlikely that the differential responses to stimuli presented at different positions were a consequence of the monkey's eye position and movement.
DIRECTION SELECTIVITY. Eighty-five PH neurons were tested for direction selectivity systematically using a bar stimulus. About half of the neurons (46%, 39/85) were responsive and 11 neurons (13%) showed direction-selective responses. However, because we used a bar stimulus in the direction test, the direction-selective responses may be explained by their selective responses to the orientation of the bar. To examine this possibility, we compared the responses to a moving bar with those to a static bar. Consequently, we classified neurons into 3 types as follows (Fig. 5A). Neurons that responded more strongly to the bar moving in the optimal direction than to the static bar of the same orientation as the moving bar were classified as M-type neurons (Fig. 5Aa). Neurons that responded less strongly to the moving bar than to the static bar were classified as S-type neurons (Fig. 5Ab). The remaining neurons were classified as MS-type neurons (Fig. 5Ac). Forty-four PH neurons were examined using both orientation and direction stimuli. Of these, 10 (23%) were M-type, 2 (5%) were S-type, and 32 (73%) were MS-type neurons. Of the 10 M-type neurons, 5 showed direction- but not orientation-selective responses (Fig. 5B; DSON neurons). The direction selectivity of these neurons was probably a consequence of the direction of movement, not of the orientation of the bar. In addition, some PH neurons showed unidirectional response patterns (4 of 11 direction-selective neurons; Fig. 5C) in which the maximal response was significantly stronger than that in the other directions except for the two neighboring directions. These neuronal responses also could not be explained by the orientation selectivity of those neurons.
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EYE-POSITION–SENSITIVE NEURONS. We investigated the effect of the monkey's eye position on activity of 67 PH neurons by changing the position of the fixation spot in the visual reaction time task. During the test, no visual stimulus except for the fixation spot was presented. Of the 67 neurons, 27 (40%) showed changes in their activity depending on the monkey's eye position (Fig. 6).
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Object information
SELECTIVITY TO COMPLEX STIMULI. Using 16 full-colored images, we
tested selectivity for image stimuli in 175 PH and 151 PR neurons. Of these
neurons, 15 PH neurons (9%) and 59 PR neurons (39%) were responsive. Six PH
neurons (3%) showed image-selective responses, whereas 49 PR neurons (32%) did
(Figs. 7A and
8A). The proportions
of the visually responsive (2 = 42.98, df = 1, n =
326, P < 0.0001) and image-selective neurons (2 =
48.68, df = 1, n = 326, P < 0.0001) were significantly
higher in the PR cortex than in the PH cortex.
To evaluate the image selectivity, we used Kruskal–Wallis's H value
as the index of selectivity. This index approaches zero if the responses to
all stimuli are similar in magnitude and increases as the difference in
response magnitude becomes prominent. The mean H values of the responsive
neurons in the PH and PR cortices were 7.6 ± 4.1 (mean ± SD) and
30.0 ± 15.1, respectively (Fig.
9Aa). The mean H value of these neurons was significantly
larger in the PR cortex than in the PH cortex [t(66) = 5.02,
P < 0.0001]. The selectivity index (SI) used by Rainer and Miller
(2000) was also calculated.
The mean SI values in the PH and PR cortices were 0.38 ± 0.24 and 0.55
± 0.21, respectively (Fig.
9Ba). The SI values of PR neurons was significantly
larger than those of PH cortex [t(58) = 2.09, P < 0.05].
These data suggest that PR neurons can convey more information about complex
images than PH neurons.
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SELECTIVITY TO SIMPLE STIMULI. Responsiveness to 8 geometrical
shapes was studied in 173 PH and 44 PR neurons. Of these neurons, 13 PH (8%)
and 17 PR (39%) neurons were responsive to simple shapes, and 7 PH (4%) and 8
PR (18%) neurons showed shape-selective responses (Figs.
7B and
8B). The proportions
of the responsive (2 = 28.52, df = 1, n = 217,
P < 0.0001) and selective neurons (2 = 11.96, df =
1, n = 227, P < 0.001) for the shape stimuli were
significantly higher in the PR cortex than in the PH cortex. We also tested
selectivity for the orientation of a bar stimulus in 131 PH and 58 PR neurons.
Of these neurons, 46 PH (35%) and 20 PR (34%) neurons were responsive, and 10
PH (8%) and 6 PR (10%) neurons showed orientation-selective responses
(Fig. 7C). Both of the
proportions of the responsive (2 = 0.01, df = 1, n =
189, P > 0.1) and orientation-selective neurons (2
= 0.38, df = 1, n = 189, P > 0.1) for the orientation of
the bar stimuli were not significantly different between the two areas.
The H values for the responses to the simple stimuli were compared between the PH and PR cortices. The H values of the neurons responsive to the shape stimuli were 11.4 ± 7.6 (mean ± SD) in the PH cortex and 14.3 ± 11.6 in the PR cortex (Fig. 9Ab), and those of the neurons responsive to the bar stimuli were 5.2 ± 4.3 in the PH cortex and 7.5 ± 5.7 in the PR cortex (Fig. 9Ac). There were no significant differences in the H values of both types of neurons between the two areas [shape, t(30) = 0.79, P > 0.1; orientation, t(64) = 1.76, P > 0.05]. The SI values for shape were 0.46 ± 0.21 in the PH cortex and 0.33 ± 0.12 in the PR cortex (Fig. 9Bb) and those for orientation were 0.26 ± 0.16 in the PH cortex and 0.25 ± 0.13 in the PR cortex (Fig. 9Bc). Again, there were no significant differences [shape, t(23) = 0.76, P > 0.05; orientation, t(57) = 0.24, P > 0.1]. These data suggest that the ability of PH neurons to discriminate simple stimuli is similar to that of PR neurons.
COLOR SELECTIVITY. Of 72 PH neurons systematically tested for color selectivity, 42 (58%) neurons were responsive and 17 (24%) neurons showed color-selective responses (Fig. 7D). The mean H values were 13.9 ± 9.3 (mean ± SD).
Locations of responsive neurons
Viewed on the basis of the RF property, we examined the distribution of the visually responsive neurons. The neurons that had the optimal stimulus position in the central (filled circles) and peripheral visual fields (open circles) were inter-mingled both in the PH and PR cortices (Fig. 10). We could not find any relationship between the eccentricity of the optimal stimulus position and the location of the neurons.
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Viewed on the basis of stimulus selective property, the distribution of the visually responsive neurons was examined. In the PH cortex, the neurons that responded only to images and not to simple shapes and bars (filled squares) seemed to be observed more frequently at its anterior portion. This was confirmed in one of two monkeys by a statistical test (Mann–Whitney's U = 68.00, P < 0.01; the statistical test was not carried out in the other monkey because most neurons were sampled within a few millimeters of the anterior–posterior axis. See Fig. 11B).
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We also examined the distribution of the eye-position–sensitive neurons. The eye-position–sensitive neurons (filled triangles) did not seem to be clustered at some specific locations but were scattered over the PH cortex, although they tended to be observed at specific recording tracks (Fig. 10).
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DISCUSSION |
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First of all, PR neurons rarely responded to the bar stimuli that were used
in our RF search and direction test. This is a prominent characteristic of PR
neurons. Therefore our comparison between responses of PH and PR neurons with
respect to spatial processing is not enough at present. Even though the number
of PR neurons examined was limited, our present results demonstrate that the
PH cortex is more involved than the PR cortex in processing visual information
in the periphery. Some PH neurons did not include the center of gaze in their
RFs, whereas the RFs of the PR neurons always included the center of gaze.
About half of PH neurons had the peripheral optimal stimulus position, whereas
most of PR neurons had the central one. The representation of the peripheral
visual field in the PH cortex is suggested by previous anatomical studies,
which showed that afferents from area TEO and V2 to area TF were only from the
peripheral representation region of the areas
(Distler et al. 1993;
Gattass et al. 1997).
Boussaoud et al. (1991)
investigated visual responsiveness of PH neurons. They found visually
responsive neurons at the most posterior portion of the PH cortex, area VTF
according to their terminology, and failed to find responsive neurons at its
anterior portion. They reported that neurons in area VTF had relatively small,
contralateral RFs, and tended to have a visuotopographic organization. In
contrast, we found many visually responsive neurons in the anterior portion of
the PH cortex. About half of them had relatively large, bilateral RFs. These
discrepancies may be attributed to the difference in the condition of the
subjects. They recorded and investigated the activity of PH neurons of
anesthetized monkeys, whereas we examined that of behaving monkeys. Some PH
neurons, particularly those in the anterior PH cortex, may respond to visual
stimuli only under the awake condition, or change their responsiveness
depending on the conditions of the subjects. Previous studies also reported
visual responsive neurons in the anterior PH cortex of behaving monkeys
(Nakamura et al. 1994;
Riches et al. 1991;
Salzmann et al. 1993;
Vidyasagar et al. 1991). There
may be subareas in the PH cortex. Neurons in the posterior portion have small
and topographically RFs, whereas those in the anterior portion have relatively
large, bilateral RFs and are difficult to be activated under anesthesia.
The present results of direction selectivity suggest that some PH neurons
convey information about the direction of a moving object. The PH cortex
receives inputs from visual areas in the dorsal pathway
(Cavada and Goldman-Rakic 1989;
Jones and Powell 1970;
Martin-Elkins and Horel 1992;
Seltzer and Pandya 1976,
1984,
1991;
Suzuki and Amaral 1994) and
has connections with area MST, area FST, and the superior temporal polysensory
area (Barnes and Pandya 1992;
Boussaoud et al. 1990; Seltzer
and Pandya 1976,
1991;
Suzuki and Amaral 1994). These
areas are considered to be involved in higher-order motion processing
(Desimone and Ungerleider
1986; Oram and Perrett
1996; Perrett et al.
1985; Sakata et al.
1985
1994;
Tanaka et al. 1986). These
data support our present results that some PH neurons process motion
information.
There were neurons in the PH cortex that were sensitive to the monkey's eye
positions. These neurons have been observed in areas in the dorsal pathway,
such as V6A, area 7a, and area LIP
(Andersen et al. 1990;
Galletti et al. 1995;
Nakamura et al. 1999;
Sakata et al. 1980). The PH
cortex receives afferents from these areas
(Andersen et al. 1990;
Barnes and Pandya 1992;
Cavada and Goldman-Rakic 1989;
Jones and Powell 1970;
Martin-Elkins and Horel 1992;
Seltzer and Pandya 1976,
1984,
1991;
Suzuki and Amaral 1994). In
addition, PH neurons showed responses related to saccadic eye movement
(Ringo et al. 1994;
Sobotka et al. 1997).
In summary, our present results together with those of the previous studies indicate that the PH cortex is involved in spatial processing.
Object processing
Consistent with our previous results
(Nakamura et al. 1994), we
found neurons in the PH cortex as well as in the PR cortex showing selective
responses to complex visual images. The PH cortex receives inputs from
higher-order visual areas, such as areas TE and TEO
(Distler et al. 1993;
Seltzer and Pandya 1976;
Suzuki and Amaral 1994).
Felleman and Van Essen (1991)
regarded the PH cortex as a visual area higher than area TE in the hierarchy
of visual processing. Together with these anatomical data, the selective
responses of the PH neurons to complex visual stimuli suggest that visual
information related to object processing reaches the PH cortex as well as the
PR cortex. However, it is unlikely that the PH cortex plays a central role in
visual object recognition or identification. Lesions of the PH cortex did not
affect the performance of delayed nonmatching-to-sample task
(Ramus et al. 1994) and object
discrimination task (Murray et al.
1998), whereas lesions in the PR cortex induce deficits in various
visual recognition memory tasks (Buckley et
al. 1997; Meunier et al.
1993). Consistent with these data, our present data suggest that
the PR cortex is more involved than the PH cortex in processing of complex
images. The function of the PH neurons selectively responding to complex
stimuli is as yet unclear. Previous studies have suggested that neurons in the
PH cortex are correlated with the tone signaling the start of a trial
(Ringo and O'Neill 1993) and
with a complex behavioral context
(Salzmann et al. 1993;
Vidyasagar et al. 1991). It is
possible that the selective responses of PH neurons could be explained by
other factors such as behavioral significance, as observed in the amygdala
(Nakamura et al. 1992;
Nishijo et al. 1988).
Function of PH cortex
The human PH cortex has been implicated in visual processing related to
recognition of local environments. Damage to the PH cortex causes a syndrome
known as "topographical disorientation"
(Aguirre and D'Esposito 1999;
Habib and Sirigu 1987;
Landis et al. 1986). Patients
with this syndrome are unable to navigate from one place to another in
familiar and/or novel environments. The involvement of the PH cortex in
navigation has also been shown by functional neuroimaging studies (Maguire et
al. 1997,
1998a,b;
Owen et al. 1996). Recognition
of a current location from a scene is required for navigation
(Aguirre and D'Esposito 1999)
and actually functional neuroimaging studies have revealed that the PH cortex
is involved in perception and/or recognition of a scene of a local environment
(Aguirre and D'Esposito 1997;
Epstein and Kanwisher 1998;
Epstein et al. 1999;
Nakamura et al. 2000;
Sato et al. 1999). Van Diepen
and colleagues (van Diepen and Wampers
1998; van Diepen et al.
1994) investigated effects of deprivation of central or peripheral
information on scene processing and demonstrated that it was possible to
recognize a scene even if the central part of the stimulus was missing,
suggesting the importance of peripheral information for scene recognition. PH
neurons reported in the present study, which have relatively large and
peripherally emphasized RFs and often show responsiveness to complex images,
seem to be convenient for such scene processing. Our PH neurons responsive to
complex images may respond to objects associated with certain locations in
their daily life. Further studies are needed to clarify this issue.
The PH cortex is regarded as a polymodal area, receiving information from
higher-order unimodal visual, auditory, and somatosensory cortical regions as
well as from other polymodal areas (Jones
and Powell 1970; Suzuki and
Amaral 1994; Van Hoesen
1982). Lesion of the PH and PR cortices impaired tactual as well
as visual recognition memories (Suzuki et
al. 1993). In the present study, visually responsive neurons are
fewer in the PH cortex than in the PR cortex. These results might reflect the
involvement of the PH cortex in modalities other than visual.
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DISCLOSURES |
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ACKNOWLEDGMENTS |
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Present address of N. Sato: Division of Applied System Neuroscience, Nihon University, School of Medicine, Tokyo 173-8610, Japan.
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FOOTNOTES |
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Address for reprint requests: K. Nakamura, Department of Behavioral Brain Sciences, Primate Research Institute, Kyoto University, Kanrin, Inuyama, Aichi 484-8506, Japan (E-mail: knakamur{at}pri.kyoto-u.ac.jp).
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ABSTRACT
INTRODUCTION
