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HIPPOCAMPUS, VOL. 2, NO. 3, PAGES 307-322,JULY 1992
Spatial Responsiveness of Monkey Hippocampal Neurons to
Various Visual and Auditory Stimuli
Ryoi Tamura, Taketoshi Ono, Masaji Fukuda, and
Kiyomi Nakamura
Department of Physiology, Faculty of Medicine, T o y a m a Medical a n d
Pharmaceutical University, Toyama, Japan
ABSTRACT
To investigate involvement of the hippocampal formation in spatial information processing,
activity of neurons in the hippocampal formation of the conscious monkey was recorded during
presentation of various visual and auditory stimuli from several directions around the monkey.
Of 1,047 neurons recorded, 106 (10.1%) responded to some stimuli from one or more directions.
Of these 106 neurons with directionally differentiating responsiveness, 49 responded to visual
stimulation, 35 to auditory stimulation, and 22 to both. Among 81 neurons, each tested with
more than 10 different stimuli, one type responded independent of the nature of the stimulus
(nonselective, n = 39), and responses of the other type depended on the nature of the stimulus
(selective, n=42). To investigate effects of change in spatial relations between test stimuli and
background stimuli fixed on the monkey or fixed in the environment, 59 of 106 neurons were
tested while the experimental apparatus holding the stimulus was moved relative to the monkey.
Of these 59 neurons, 36 changed their responsiveness; 7 maintained the magnitude of their responses but changed the response direction with the movement of the apparatus, 5 changed
direction regardless of the movement, and 24 did not change direction, but decreased or extinguished responses from the preferred direction. Thirty-two of 106 neurons were also tested by
rotating the monkey. The directionally differentiating responsiveness of 1 1 neurons followed the
monkey (egocentric neurons), that of 9 remained in place in the environment (allocentric neurons), and responses of 12 were reversibly extinguished when the monkey was rotated. The
results suggest that these hippocampal neurons may be involved in identification of relations
among various kinds of stimuli in different spatial frameworks (egocentric or allocentric) and
this identification may be developed from multiple sensory modalities.
Key words: hippocampal formation, single unit recording, spatial memory, egocentric neurons, allocentric
neurons
It is now widely accepted that the hippocampal formation
(HF) is involved in spatial memory as well as nonspatial memory. Humans with damage in the medial temporal lobe, including the HF, exhibit spatial memory deficits (Smith and
Milner, 1981; 1984; 1989; Cave and Squire, 1991). In the monkey, bilateral lesions in the H F system impair performance
in several kinds of spatial tasks (Zola-Morgan and Squire,
1986; Rupniak and Gaffan, 1987; Parkinson et al., 1988). In
the rat, bilateral lesions in the H F system also impair performance in spatial tasks (Olton et al., 1978; Moms et al.,
1982). Unit-recording studies of the rat H F suggest the existence of “place units” in the H F that respond preferentially
to particular locations of the animal in the field (O’Keefe and
Correspondence and reprint requests to Professor Taketoshi Ono,
Department of Physiology, Faculty of Medicine, Toyama Medical and
Pharmaceutical University, Sugitani, Toyama 930-01, Japan.
Dostrovsky, 1971; O’Keefe and Nadel, 1978; Muller et al.,
1987; Breese et al., 1989; Foster et al., 1989). Unit-recording
reports indicate that some primate H F neurons respond in
spatial tasks (Watanabe and Niki, 1985; Cahusac et al., 1989;
Miyashita et al., 1989; Rolls et al., 1989; Feigenbaum and
Rolls, 1991). These unit-recording studies in the monkey H F
suggest that some neurons in the H F may be involved in spatial learning or memory developed from vision. As suggested
in a previous study of the rat hippocampus (O’Keefe and Conway, 1978), place-specific activity change in place units can
depend not only on vision but also on other sensory modalities, such as audition. However, relations between neuronal
responses of the monkey H F to spatial factors and properties
of stimuli (such as sensory modalities or a kind of stimulation
have not been ascertainedin one sensory
The H F has reciprocal connections with both the posterior
region of the inferior parietal cortex and the prefrontal as-
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HZPPOCAMPUS VOL. 2, NO. 3, JULY 1992
sociation cortex, which are involved in spatial information
processing (Teuber, 1964; Pohl, 1973; Petrides and Iversen,
1979; Andersen and Mountcastle, 1983; Passingham, 1985;
Andersen, 1987; Goldman-Rakic, 19871, mainly via the parahippocampal cortices (PH) (Jones and Powell, 1970; Van
Hoesen, 1982; Amaral, 1987; Tranel et al., 1988). Recent results indicate that the HF, and the system to which it belongs,
are essential for acquisition, relation, combination, and conjunction among stimuli (Eichenbaum et al., 1988; Squire et
al., 1989; Sutherland and Rudy, 1989; Wiener et al., 1989)
and such functions are important for allocentric spatial mapping. A computational theory suggests the possibility that
egocentric representation of information is converted to allocentric form in the hippocampus (O’Keefe, 1990). Assuming that there are neurons in the monkey H F that respond to
stimuli presented in a particular local context (or configuration of background stimuli), responsiveness of such neurons
may also depend on some reference stimuli as well. Furthermore, if reference stimuli are fixed to the animal or things
that move with the animal, responses of neurons may have
“egocentric” properties, and if reference stimuli are fixed in
the environment, responses of neurons may have “allocentric” properties. It was thus thought to be useful and important to investigate whether there are neurons in the monkey H F that respond to some spatial aspects of stimuli
presented, and if there are such neurons, which relations between stimuli are represented in their responses.
In this study, we analyzed the responses of single neurons
in the monkey H F to the presentation of various test stimuli,
visual or auditory or both, from various directions relative to
the monkey. To investigate relations between test stimuli and
reference stimuli further, the same tests were performed
either while keeping the monkey fixed and changing part of
the environment, or while moving the monkey relative to a
fixed environment. A preliminary report of this work has appeared elsewhere (Tamura et al., 1990), and some supporting
evidence has recently been reported (Feigenbaum and Rolls.
1991).
MATERIALS AND METHODS
Except for differences in some parts of the experimental
design and the stimulus presentation paradigm, the experimental methods were essentially the same as those used in
the accompanying paper (Tamura et al.). Therefore, the Materials and Methods section has been minimized: the reader
is referred to the accompanying paper (pp. 287-306) and our
previous papers (Ono et al., 1980; 1981; 1989; Fukuda et al.,
1986; Nishijo et al., 1988a; 1988b; Yamatani et al., 1990).
Experimental design and stimulus presentation
The monkeys normally sat in a chair facing an apparatus
(Fig. 1). The apparatus had a front panel and two wings of
aluminum plate that could be easily detached. The panel had
a window (Wm, about 10 cm x 20 cm) covered by a oneway-mirror shutter. Each wing also had a window (W1 or Wr,
about 15 cm x 15 cm). Behind each window was a stage for
setting objects. The normal arrangement of the experimental
room is shown in Figure 1A. The apparatus was in front of
the monkey (M). The experimenter(s) (H) usually sat in front
of the monkey to its right and was hidden by a wing of the
apparatus. In this situation, various visual and auditory stimuli were presented to the monkey from several directions.
Many different objects chosen from a pool of about 1,000,
as well as some parts of the human body, were used as visual
stimuli. Sometimes food (raisin, a piece of apple, cookie, etc.)
was given to the monkey to retain its attention to the presented objects. Since, in the experimental situation reported
here, the monkey’s limb movements (e.g., reaching his hands
to foods) were restricted by attaching an acrylic plate in front,
the foods were placed directly in the monkey’s mouth by the
experimenter. The range that the monkey could see was restricted to about 280” from the center by attaching opaque
acrylic plates at the sides of its face. Usually each object was
presented by the experimenter putting it on the stage behind
the window for about 2.0 seconds. The distance between the
monkey’s face and the object was usually about 40 cm. Sometimes the same object was also presented by the experimenter’s hand, which approached closer to the monkey. When
large objects, such as the human body, were presented, the
wings were detached or the experimental apparatus in front
of the monkey was completely removed. When the apparatus
was removed and the room light was on, the monkey could
see the white walls of the room in front and to the left anterior,
and the recording setup to the right anterior (Fig. 1A). In this
situation, the experimenter could walk around the monkey,
stop at various places, and display various actions, such as
sitting, standing, or presenting an object by hand that had
been shown in the experimental apparatus.
Many different kinds of sounds were used for auditory
stimulation, including meaningful or complex sounds (step
sound, clap, human voice, crash, etc.) and computer-synthesized sounds (harmonic rich sounds or pure tones) using
a sound board (PC-9801-26K, NEC). Meaningful or complex
sounds were usually presented by some act of the experimenter (stepping, clapping, vocalizing, crashing metal materials, etc). Computer-synthesized sounds were presented
through speakers arranged around the monkey. Each sound
source (experimenter’s act or speaker) was usually located
about 80 cm from the monkey’s head except for sound from
fixed sources, such as the sound of opening or closing the
entrance door. The intensity of computer-synthesized sounds
was usually controlled to about 80 dB. Intensities of complex
sounds made by the experimentcr were estimated to range
between 70 and 90 dB. Most auditory stimuli were presented
from various directions around the monkey by moving the
source of the sound. If a stimulus was considered to contain
both visual and auditory components, we attempted to separate the modalities by attenuating the intensity of the sound
or by masking it with white noise, or by reducing illumination
to a minimum to restrict the monkey’s vision.
When activity of a single neuron in the H F or PH was
detected, a few kinds of objects or human actions were presented as visual stimuli at the left anterior (about 45” from
the anterior-posterior plane), anterior, and right anterior positions (Fig. 1B). Each visual stimulus was presented five or
more times at each position before the next object was presented. A few kinds of sounds were similarly presented five
or more times each from the left anterior, anterior, right anterior, right posterior, posterior, and left posterior directions.
MONKEY HIPPOCAMPAL RESPONSES TO SPACE / Tarnura et al.
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Fig. 1. Schema of experimental situation. (A) Arrangement of 4 m x 6 m experimental room. Monkey sat in a chair facing
a front panel. Monkey's limb movements were restricted by plate attached in front of its body. Two wings (left wing and
right wing) were at left and right sides of the front panel. There was a window in the front panel (Wm) and one in each wing
(Wl, Wr). Experimenter(s) were usually at right anterior of the monkey to observe behavior of the monkey and direct on
line analysis of unit activity. Various kinds of objects (0)were presented to monkey from left anterior (WI), anterior (Wm),
or right anterior (Wr) directions as visual stimuli. Various kinds of sounds were presented to monkey from one of eight
speakers (S) set around monkey as auditory stimuli. Entrance door to room was behind monkey. (B) Directions of visual
and auditory stimulation sources. Various kinds of visual and/or auditory stimuli were presented from several directions
around the monkey. Solid lines, visual stimulation; broken lines, auditory stimulation. M, monkey; H, experimenter(s); 0,
objects presented; S, speakers used for computer-generated auditory stimuli; AC, air conditioner.
If neuronal activity changed when the relative direction of
the origin of a stimulus was changed, then more detailed relations between the directionally differentiating responsiveness and the kind of stimulation were examined using various
kinds of visual and auditory stimuli. We use the term directionally differentiating since the neurons responded differently when stimuli were presented from different positions
(or directions) around the monkey. This phrase is then used
to describe responses of these neurons as they are subjected
to corresponding procedures. Stimulus presentations were
separated by intervals of at least 30 seconds.
After these tests were concluded, and if the neuron being
recorded was thought to have directionally differentiating responsiveness, we tested its responses in the following two
procedures.
Procedure 1
The experimental apparatus in front of the monkey was
moved to several places in the experimental room. Since the
experimental apparatus was usually located in front of the
monkey and covered a large part of its visual field, this apparatus was considered to have many visual stimuli that could
be dominant landmarks (references) for locational information of test stimuli. If the neuron did not change responses
31 0
HPPOCAMPL~S VOL. 2, NO. 3, JULY 1992
in this procedure, it was deemed to be responding to relations
between a test stimulus and background stimuli other than
those on the experimental apparatus. If the responses of the
neuron followed movement of the apparatus, the neuron
could have been responding to relations between test stimuli
and stimuli on the experimental apparatus. Background stimuli is a general term meaning stimuli that could provide spatial
reference for the test stimulus. Therefore, background stimuli
include all stimuli fixed in the environment (experimental
room), on the monkey, and all visible parts of the restraining
device.
Procedure 2
The monkey chair was rotated 45” to the left and then 45”
to the right of the experimental apparatus, and the test stimuli
remained in their initial positions. If the responses follow this
rotation, as in Figure 9A, the neuron was considered to respond to some spatial relation between the test stimulus and
some stimuli that rotated with the monkey. If the responses
remained constant relative to the environment, as in Figure
9B, the neuron was considered to respond to some spatial
relation between the test stimulus and some stimuli that were
fixed in the environment.
Recording and data analysis
Most of the recording technique and data analysis were the
same as those described in the accompanying paper (pp. 287306). Briefly, single-unit activity was recorded from the HF
and PH. Neuronal activity was processed in a window discriminator and displayed as peristimulus time histograms
using minicomputers on-line and off-line.
During auditory stimulation, the stimuli themselves triggered data collection by converting sounds to electrical start
signals through a microphone near the monkey’s head. For
visual stimulation, the experimenter pressed a foot switch to
trigger collection of data when stimuli were presented. Neuronal responses for the first 1.0 seconds after presentation
were averaged for each of several stimulus presentations. Responses to the presented stimuli were compared by one-way
analysis of variance (ANOVA) with significance at Pc.05.
Latency of each response to the stimulus was measured
mainly for auditory stimulation off-line since timing of auditory stimulation could be precisely determined from
recorded sound data, whereas timing of visual stimulation,
especially of human actions, could not be precisely determined.
During recording sessions, eye movement of the monkey
was monitored through a monochrome television camera or
electrooculograms (EOG) or both, as well as directly by the
experimenter. During recording sessions, behavior of the
monkey was also monitored through a color television camera
or electromyograms (EMG) or both, as well as directly by
the experimenter.
RESULTS
Animal behavior
All monkeys usually turned their attention to a visual stimulus when it was presented. Since the head was restrained,
only the eyes of the monkeys could move in the direction of
a visual stimulus. When food was presented, the monkeys
would usually fix their eyes on it until they got it or it was
withdrawn. No other consistent overt behavior was noticed
when visual stimuli were presented. When auditory stimuli
were presented, they did not usually exhibit any consistently
overt behavior or eye movement, except when a loud or
frightening sound was made.
General properties of HF neurons with
directionally differentiating responsiveness
Of 1,047 neurons tested in the HF and PH, 106 (10.1%)
responded (all by excitation) preferentially to the presentation of visual andlor auditory stimuli from a particular direction(s) around the monkey. Many of the neurons responded
phasically , but a few responded tonically during stimulus presentation. Judging from EOGs, television monitoring, and inspection of experimenter, there was no clear correlation between visual responses of most neurons and initial eye
position or eye movement. Responses of these neurons did
not correlate to particular movements of the monkey, such
as arm or leg movements. The spike activity of some of these
neurons was complex, that is, a decrementing series of spikes
at short intervals (2.0-5.0 ms) with 0.4-0.6 ms spike durations
and low spontaneous firing rates (<2.0 spikesls). However,
many of the neurons with directionally differentiating responsiveness did not show typical complex spike activity, but
showed irregular bursting with shorter spike duration of
spikes (0.2-0.5 ms) and slightly higher spontaneous firing
rates (0.5-18.1 spikeds). Neurons that showed regular firing
activity with short spike duration (0.2-0.3 ms) and high frequency of spontaneous firing (> 10.0 spikesh) usually did not
have directionally differentiating responsiveness. There was
no overlap between the neurons with directionally differentiating responsiveness described in this paper and neurons
that responded to the sight of objects during performance of
the object discrimination task described in the accompanying
paper (Tamura et al., 1992).
Relations among sensory modalities, kinds of
stimuli, responsiveness, and direction
Of these 106 neurons with directionally differentiating responsiveness, 49 responded to visual stimulation, 35 responded to auditory stimulation, and 22 responded to both
visual and auditory stimulation. The relations among sensory
modalities, neuronal responses, and orientation are shown in
Figure 2. The number of neurons in each category that also
responded in the other modality are shown in parentheses.
The vision-responsive neurons tended to respond to stimulation presented from the right anterior direction, and the
sound-responsiveness neurons tended to respond more to
stimulation presented from the posterior. Of the 22 visual plus
auditory neurons with directionally differentiating responsiveness, the visual and auditory responses of 11 overlapped
(4,left anterior; 2, anterior; 5, right anterior) and responses
of 11 did not overlap direction.
Of the 106 neurons, 81 could be tested with more than 10
kinds of stimuli, and these 81 neurons were divided into two
groups. In one group, responsiveness was independent of the
nature (or kind) of the stimulus in one sensory modality (non-
MONKEY HIPPOCAMPAL RESPONSES TO SPACE / Tarnura et al.
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Fig. 2. Relations among sensory modalities, neuronal responses, and stimulus orientation. Ordinates, numbers of
neurons with directionally differentiating responsiveness that
respond in each position. Hatched areas (V), neurons with
visual responses; solid areas (A), neurons with auditory responses. Number in parentheses below each column indicate
number of neurons in that column that are bimodal. Totals
may exceed those in text because of overlap.
selective group, n = 39). In the other group, responsiveness
depended on the nature of the stimulus, and these neurons
tended to respond more to some stimuli than to others (selective group, n = 42).
Of 49 visual neurons, 34 were tested with more than 10
kinds of stimuli and 21 of 34 were classified into a nonselective group. Responses of a visual nonselective neuron are
shown in Figure 3. This neuron, located in the CAI area of
the HF, was tested with 1 1 kinds of visual stimuli (not all
shown) and 4 kinds of auditory stimuli. It responded phasically to visual stimuli presented from the right anterior direction (Ac, B), and did not respond to the same visual stimuli
presented from any other direction (Aa, Ab). This neuron did
not respond to any of four kinds of auditory stimuli presented
from any direction (Aa-f, pure tone; B, human voice, step,
clap, pure tone). Thus the responses of this neuron were nonselective to the kind of visual stimuli tested, but they were
selective to the direction of stimulation (right anterior) and
to sensory modality (vision). As shown in Figure 4, there
seemed to be no clear relation between the response of this
neuron and eye movement. For example, there was no significant eye movement in the second presentation of apple
(A2) and second presentation of stick (C2) since the monkey
had already directed its eyes toward right anterior, and there
was significant movement to the right in the other presentations. However, the responses of the neuron were almost
the same in all of these situations.
The other 13 of 34 visual neurons were classified into a
selective group (1 1 responded strongly to particular human
movements and 2 responded to the sight of rewarding objects). Responses of a typical, visual selective neuron are
shown in Figure 5. This neuron, located in the CAl area of
31 1
the HF, was tested with 15 kinds of visual stimuli and 8 kinds
of auditory stimuli (not all shown). It responded selectively
to human action (standing up or sitting down) in the right
anterior position (A,B), but not to any of 14 other kinds of
visual stimuli or 8 kinds of auditory stimuli (B). This neuron
did not respond to any other test stimuli presented from any
direction (A). When room illumination was reduced to a minimum or the monkey was prevented from seeing human action
by an opaque plate, responses to human action at right anterior were completely extinguished (B, human action in
dark). The response magnitude of this neuron to the presentation of visual stimuli did not depend on the length of the
period that the monkey fixed his eyes on the visual stimulus,
since the monkey almost always fixed his eyes longer on rewarding objects, such as a piece of apple, raisin, or cookie,
than on human action. However, responses to human action
were much stronger than the responses to these rewarding
objects.
Of 35 auditory neurons, 32 were tested with more than 10
kinds of stimuli, and 14 of 32 could be classified as nonselective. Responses of an auditory nonselective neuron are
shown in Figure 6. This neuron, located in the CA3 area of
the HF, was tested with six kinds of visual stimuli and seven
kinds of auditory stimuli. It responded strongly to auditory
stimuli presented from the left posterior direction (A). It also
responded weakly to auditory stimuli from the posterior direction, but not if they were presented from any other direction. This neuron did not respond to any of six kinds of
visual stimuli presented from anterior directions. Magnitudes
of responses were almost the same for all kinds of different
auditory stimuli presented from the left posterior direction
(B) (ANOVA, P > . 1). Other auditory neurons (18 of 32) were
classified as selective. All of these neurons exhibited strongly
selective responses to complex sounds made by the experimenter: seven responded to a step, four to the sound of a
chair moving, two to the sound of a door opening, two to a
data recorder being switched, two to board tapping, one to
the sound of paper crumpling. Responses of an auditory selective neuron are shown in Figure 7. This neuron, located
in the dentate gyrus, was tested with 8 kinds of visual stimuli
(not shown) and 10 kinds of auditory stimuli. The neuron
responded strongly to sounds related to human movement
presented from posterior directions (A, B); the strongest response was to the door being opened in the posterior direction
(B). When the directionally differentiating responsiveness of
this neuron was further tested by using a human voice, a clap,
or a pure tone, responses to the human voice and clap diminished as the source of the stimulus approached the anterior direction. There were no responses to a pure tone from
any direction nor to any auditory stimulation from anterior
directions within the monkey's vision ( k80" from the center)
(A). Judging from EOGs and television monitoring, there was
no correlation between eye movement and responses of these
auditory neurons.
Of 22 neurons that responded to both visual and auditory
stimuli, 15 were tested with more than 10 kinds of stimuli.
Of these 15 neurons, 4 were classified as nonselective and 11
as selective (all 1 1 responded strongly to human action such
as walking and to complex sounds made by the experimenter).
31 2
HZPPOCAMPUS VOL. 2, NO. 3, JULY 1992
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Fig. 3 . Responses of visual nonselective neuron. (A) Directionally differentiating responsiveness to visual and auditory stimuli
shown as raster displays. Visual stimuli (e.g., apple, syringe, and stick) were presented from left anterior (a), anterior (b),
and right anterior (c) directions. Auditory stimuli (e.g., pure tone) were presented from six directions (a-0. Note phasic
responses to visual stimuli presented from right anterior direction (c). Abscissa, time (sec); vertical line in each plot indicates
time 0 when each stimulus was presented; horizontal line above abscissa, period of stimulus presentation (2 seconds). P,
front panel. Other descriptions as for Figure 1 . (B) Comparison of visual nonselective responses to various kinds of visual
or auditory stimuli presented from right anterior direction. This neuron responded to all visual stimuli tested with almost
the same response magnitude when presented from right anterior, but not from other directions, and did not respond to
auditory stimuli. Each histogram, mean and SEM of response size of five presentations of each stimulus. (Response size
defined as difference between 1 .O second measurement of firing number before stimulus presentation and 1.O second measurement of firing number during stimulus presentation.)
MONKEY HIPPOCAMPAL RESPONSES TO SPACE / Tamura et al.
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perimental apparatus was fixed. Changing the location of the
experimental apparatus modified the responses of 36 of 59
neurons. For 12 of these neurons, the direction of maximum
response changed (7 neurons changed the direction according
to the movement of the apparatus and 5 changed the direction
independent of the movement). For the other 24, the preferred direction did not change, but responses in the preferred
direction were very weakened, or the directionally differentiating responses were reversibly extinguished. The responsiveness of a neuron whose responsiveness was completely extinguished by moving the apparatus is shown in
Figure 8. This is the same neuron shown in Figure 5. The
strong responses to human action presented from the right
anterior direction (Aa) were completely extinguished when
the experimental apparatus, which was considered to be a
part of the environment, was removed to a place where the
monkey could not see it (Ab). The response magnitude also
depended on the precise location of the apparatus when the
monkey could see it. When the apparatus was moved about
5 cm to either the left or the right, responses in the preferred
direction were steeply diminished irrespective of the relations
between the test stimulus and the experimental apparatus
(Fig. 8Ac, B), and when the apparatus was moved more than
10 cm to the left or 15 cm to the right, responses were completely extinguished (Fig. SAb, B) although the visibility of
the human action was not changed.
When the monkey was rotated, the directionally differentiating responsiveness of 11 neurons followed the monkey.
We designate these neurons as “egocentric,” because the
directions of their responses followed the rotation of the monkey, and these responses were considered to represent relations between the test stimulus and background stimuli on
the monkey or on the restraining device that rotated with the
monkey. An example of responsiveness of an egocentric neuron is shown in Figure 9A. This neuron responded strongly
to both visual and auditory stimuli related to human movement, such as walking, presented from the right anterior position. The responses to walking at the right anterior were
weakened but not extinguished when all of the lights in the
experimental room were turned off or when the monkey was
prevented by a screen from seeing the human walking (not
shown). Thus, the directionally differentiating responsiveness of this neuron may include both vision and audition. The
responsiveness to a human walking at the right anterior (Aa)
followed the monkey when it was rotated 45” to the left (Ab)
or to the right (Ac). Electroculograms and television monitoring of eye movement did not show correlation between
responses of these egocentric neurons and eye movement.
The directionally differentiating responsiveness of nine
neurons remained in place in the environment and did not
follow the monkey. We designated these neurons as “allocentric,” because the directions of their responses did not
follow the rotation of the monkey but remained constant relative to the environment, and these responses were considered
to represent relations between test stimulus and background
stimuli fixed in the environment. An example of the responses
of an allocentric neuron is shown in Figure 9B. This neuron
also responded to visual or auditory stimulation caused by
human actions (walking) presented from right anterior (Ba).
Responses to human action presented from the right anterior
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Fig. 4. Relation between neuronal responses to visual stimulation (upper rastergrams) and electrooculograms (EOGs,
lower traces). These neuronal responses are those to the visual stimulation from the right anterior direction in Figure 3
but shown relative to EOGs. There were no clear correlations
between eye movement and directionally differentiating neuronal responses even if the visual stimulus was the sight of
a rewarding (A, apple), an aversive (B, syringe), or a neutral
(C, stick) object. EOG, upward deflection, movement to left
(L); downward deflection, movement to right (R). Abscissa,
time (sec); time 0, each stimulus was presented; horizontal
line above abscissa, period of stimulus presentation (2 seconds).
Spontaneous firing rates and response latencies of each
type of neuron are summarized in Table I .
Dependence of responsiveness on relations
between test stimulus and background stimuli
Fifty-nine of 106 neurons were tested by changing the location of experimental apparatus in front of the monkey while
the monkey’s position was fixed in the environment. Thirtytwo of 106 neurons were also tested by rotating the chair in
which the monkey was seated while the location of the ex-
314
HZPPOCAMPUS VOL. 2, NO. 3, JULY 1992
A
20-
-
.
15-
N
m
I
m
r
.-
0
0
0
0 10-
Y
Q
n
Q
c
1
m
IT
0
.L
.-
-n
5 -
O
n
a
L
:0 I
C
.-C
.Y)
m
.-O
L
O
Y
o
E
O
P
.
LT
0
v)
0
UJ
.-C
L
%
v)
Y
V
c
.-
v)
T
Stimuli P r e s e n t e d
-5-
Fig. 5. Responses of visual selective neuron. (A) Comparison of responses to human movement (from left anterior and right
anterior directions) and pure tone from six directions. This neuron responded strongly when human sat down or stood up
at right anterior. There were no responses to human movements from left side directions or to auditory stimulation from
any direction. (B) Comparison of responses to various visual or auditory stimuli presented from right anterior direction. This
neuron responded selectively to human movement (sitting down or standing up). l h e r e were no responses to presentation
of other stimuli, nor were there responses when all room lights were turned off and illumination was minimized (human
movement in dark). Each histogram, mean and SEM of response size of six presentations of each stimulus. Hatched area
in A and B, responses to human movement: filled area in A and B, responses to pure tone. Other descriptions as for Figures
1 and 3.
A
--+P
B
ia
A
Q
m
‘m8
Q
Y
.-
Q
u)
- 6
Q
6
a
cn4
E
..-IL
L
r 2
2
(D
a2
z
0
0
Q
c
u)
II
*
0
c
*I
Q
Q
v)
6
6
L
0
L
Stimuli Presented
Fig. 6. Responses of auditory nonselective neuron. (A) Comparison of responses to stimuli presented around monkey. Visual
stimuli (e.g., apple) were presented from left anterior, anterior, and right anterior directions. Auditory stimuli (e.g., pure
tone) were presented from six directions. This neuron responded to auditory stimuli presented from left posterior direction.
(B) Comparison of responses to several auditory stimuli presented from left posterior direction. This neuron responded to
all auditory stimuli tested from the left posterior direction with almost the same response magnitude. Each histogram, mean
and SEM of response size of six presentations of each stimulus. Dotted area in A, responses to sight of apple; filled area
in A and B, responses to pure tone. Calibration at right side of bottom histogram (responses to auditory stimuli from posterior
direction) in A, firing rate. Other descriptions as for Figures 1 and 3.
A
l-
T
B
c
a,
U
Q
.-rn
0
Q)
N
L
0
0
15
c
0
v)
\
UJ
xn
10
a
l-
.-
P,
C
Q
.-a
3
(d
E
T
Q)
0
0
Y
0
0
r
v)
v
2
T
N
I
0
Q)
>
Q)
P,
n
r
+0
CI)
c
0.
I-
P
-Q
0
P
v)
Q)
Q
cn
0
c
L
7
n
5
En
.-C
L
iio
C
(d
Stimuli P r e s e n t e d
Q)
2
-5
Fig. 7. Responses of auditory selective neuron. (A) Comparison of responses to human voice (hatched area), clap (dotted
area), and 1,000 Hz pure tone (filled area) from various directions. This neuron responded to several kinds of auditory stimuli
when presented from posterior directions, but not to visual stimuli (not shown) from anterior directions. (B) Comparison of
responses to various auditory stimuli presented from posterior direction. This neuron responded strongly to sound of door
being opened behind monkey, moderately to human voice, tapping, and clap, and weakly to step and crash. There were no
responses to computer-synthesized complex sounds nor to pure tone. Other descriptions as for Figures 1 and 3.
31 6 HIPPOCAMPUS VOL. 2, NO. 3, JULY 1992
Table 1. Spontaneous Firing Rates and Response Latencies of Each Type of Neuron
Visual
No. of neurons
Visual and Auditory
Auditory
NS
S
NS
S
NS
S
Spontaneous firing rate
Range (spikesis)
Mean f SEM (spikesis)
21
13
14
18
4
11
0.0-18.3
3.6 k 0.8
0.0-5.1
1.4 f 0.5
0.0-5.5
2.2 k 0.6
0.0-4.8
2.1 f 0.3
0.4-1 1.4
4.4 -c 1.3
0.0-2.8
1.2 f 0.4
Response latency
Range (ms)
Mean i SEM (ms)
No. of neurons
150-190
173 f 10
3
240
240
1
80-240
134 k 19
11
140-460
264 -+ 30
140-240
190 i 15
3
160k280
225 i 24
4
13
NS, nonselective neurons; S , selective neurons.
Recording sites
were weakened but not extinguished when all of the lights in
the experimental room were turned off or when the monkey
was prevented by a screen from seeing the human movement
(not shown). The responsiveness to walking at the right anterior direction (Ba) remained fixed in the environment and
did not follow the monkey when the monkey was rotated 45"
to the left (Bb) or to the right (Bc). Response magnitude was
decreased to about half of the original when the monkey was
rotated 45" to the left and could not see the human because
of the restriction of monkey's vision to ?So". These responses to walking at the right are considered to be responses
to the auditory component of the stimulus (step). The directionally differentiating responsiveness of 12 other neurons
was reversibly extinguished when the monkey was rotated.
Recording sites of all neurons sampled are depicted in Figure 10. None of the three monkeys was significantly different
from the other two, nor was any of the six hemispheres significantly different from any of the other five (chi-square test,
P > . l ) . Therefore, recording sites from both hemispheres of
three monkeys are plotted on representative sections of the
left hemisphere. The recording sites of each type of neuron
are depicted in Figure 1 1 and summarized in Table 2. These
neurons were located throughout the rostrocaudal extent of
the HF, but tended to be located caudally (chi-square test,
fY.01). There were no clear relations between the subfields
in the H F and sensory modalities nor between the subfields
0 5
.-.-
L
LL
C
I
: 0
5
C
cm
*I
-p
I
:-
-5
I
15
Left
1
10
5
0
5
10
15
cm
Right
U
Fig. 8. Effects of change of environment on responsiveness of the neuron shown in Figure 5. (A) Effects of change of front
panel location. Strong responses to human movement (hatched area) at right anterior position (a) extinguished when front
panel was moved from sight (b) or attenuated when it was moved about 5 cm to left (c). There were no responses to pure
tone (filled area). (B) Analysis of effect of small location change of front panel on directionally differentiating responsiveness.
Responsiveness of this neuron was strongest when panel was in its usual position (0 cm), attenuated as panel was moved
from usual position, and extinguished when panel was moved more than 10 cm left or more than 15 cm right. Each point,
mean and SEM of response size of six presentations of each stimulus. Abscissa, distance (cm) from usual position.
MONKEY HIPPOCAMPAL RESPONSES TO SPACE / Tarnura et al.
A
a
Usual Situation
-
b
45"Rotation t o L e f t
-
4 5 " R o t a t i o n to Right
c
45"Rotation to Righ!
T
B a Usual Situation
c
31 7
b
1
\
45"Rotation to L e f t
Fig. 9. Effects of monkey rotation on responsiveness of neurons. (A) Egocentric neuron. (Aa) Strong responses to human
walking at monkey's right anterior while the monkey was in its usual position. (Ab) Directionally differentiating responsiveness to human movement after monkey was rotated 45" left from its initial position. (Ac) Directionally differentiating
responsiveness to human movement after monkey was rotated 45" right from its initial position. Note that responsiveness
to human movement at right anterior (a) followed monkey (b and c). (B) Allocentric neuron. (Ba) Directionally differentiating
responsiveness to human walking; there were strong responses at right anterior. (Bb) Directionally differentiating responsiveness to human walking (step sound) remained fixed in environment after monkey was rotated 45"left from initial position.
(Bc) Directionally differentiating responsiveness remained fixed in environment after monkey was rotated 45" right from
initial position. Each histogram in A and €3, mean and SEM of response size of five and three (A and B, respectively)
presentations of each stimulus. Hatched areas, responses to human movement. Filled circles in B, no responses to stimuli
presented (spontaneous firing rate of this neuron was almost 0). Other descriptions as for previous figures.
and nonselective or selective nature of the neurons. In the
subicular complex, the number of neurons that changed their
directionally differentiating responsiveness when the location
of the experimental apparatus was changed exceeded the
number of stable neurons that did not change (8 of 10
changed, 2 of 10 stable), but there were no clear differences
between the numbers of these neurons in other areas (dentate
gyrus: 7 of 13 changed, 6 of 13 stable; CA3: 8 of 16 changed,
8 of 16 stable; CAI: 10 of 17 changed, 7 of 17 stable; EC: 2
of 2 changed; PH: 1 of 1 changed). The 11 egocentric neurons
were located in the dentate gyrus (n = 4) and in the CA3 (n = 2)
and CAI (n = 5) subfields. The nine allocentric neurons were
located in the dentate gyrus (n = 3), the CAI subfield (n = 4),
and the subicular complex (n=2). The 12 neurons that reversibly extinguished their directionally differentiating responsiveness with rotation of the monkey were located in the
dentate g y m (n = 2), CA3 (n = 3), CAI (n = 6), and subicular
complex (n = 1).
DISCUSSION
Relations between directionally differentiating
responsiveness and sensory modalities
The neurons with directionally differentiating responsiveness tended to respond to visual stimuli presented from the
right anterior direction and to auditory stimuli presented from
the posterior. This tendency was observed in all three monkeys. The reasons for this discrimination are not entirely
clear, but it seems reasonable that vision should depend on
stimuli presented within the visual field, and audition might
be more valuable to the monkey when stimuli cannot be seen.
Also, since the experimenters were usually positioned at the
right front of the monkey during most experiments (training
sessions and recording sessions for operant tasks), this location may have achieved special importance to the monkey.
It is also probable that the monkey has spent more time with
its attention directed to its right anterior than in any other
318 HIPPOCAMPUS VOL. 2, NO. 3, JULY 1992
Fig. 10. Recording sites of sampled neurons. Solid circles, neurons with directionally differentiating responsiveness; dots,
neurons without directionally differentiating responsiveness. DG, dentate gyms; CA1 and CA3, hippocampal subfields; SUB,
subicular complex; EC, entorhinal cortex; PH, parahippocampal cortices. Number below each section: distance (mm) anterior
from interaural line.
direction in the experimental room. If learning or memory
should be related to neuronal activity, it might be possible
that the increased time of attention to that area caused the
difference seen in the number of neurons, that is, more neurons represent relations to various combinations of stimuli
that were seen in the right anterior.
The tendency of neurons to respond to visual stimuli presented from the anterior direction cannot be explained by leftright difference of hemispheres since there was no significant
difference in the incidence of recording rate in the left and
right hemispheres. It is also difficult to believe that H F neurons have this tendency by nature or that this tendency was
observed in all three monkeys by chance. Rather it seems
reasonable that this tendency may be formed in the experimental condition of training and recording sessions.
Existence of neurons that respond to visual or auditory
stimuli or both is not surprising, since the HF receives input
mainly from multimodal or so-called supramodal cortical
areas (Swanson, 1983; Amaral, 1987). This means that, consistent with a previous study of the rat hippocampus (O'Keefe
and Conway, 1978), some neurons in the HF of the monkey
may be involved in the representation of relations between
stimuli through both vision and audition.
Nonselective and selective neurons
Nonselective neurons responded to different kinds of stimulus presentation in one or both sensory modalities with almost the same response magnitude. The responses of these
stimulus nonselective neurons might partly reflect attention.
However, even if a visual stimulus was not presented, the
monkey often glanced toward the space where we believed
it expected the next stimulus to be put, thus directing its attention to that space. Visual nonselective neurons never responded consistently in this situation. Therefore, these neurons did not respond even if the monkey did direct its
attention to that space and perceive only background stimuli.
MONKEY HIPPOCAMPAL RESPONSES TO SPACE / Tamura et al.
319
I
I
L
A 19
I
L
PH'--
A 17
--
A 15
A 13
Nonselective
A Visual Selective
0 Auditory Nonselective
= Auditory Selective
0 Visual and Auditory Nonselective
Visual and Auditory Selective
* Visual
A 11
A 9
Fig. 1 1 . Recording sites of different types of neurons with directionally differentiating responsiveness. Sensory modality of
neurons: visual, triangles; auditory, squares; visual and auditory, circles. Selectivity of neurons: nonselective, open; selective,
solid. Other description as for Figure 10.
Table 2. Recording Sites of Each Neuron Type
Recording
Sites
Visual
(NS, S)
Auditory
(NS, S)
Visual and Auditory
(NS, S)
Total Directional Neurons
(NS, S)
Total Neurons
Sampled
20 (10, 10)
22 (10, 12)
25 (12, 13)
11 (6, 5 )
2 (1, 1)
1 (0,1)
220
205
369
81 (39, 42)
1047
114
51
88
NS, nonselective neurons; S, selective neurons: DG, dentate gyrus; CA3 and CAI, subfields of hippocampus proper; SUB, subicular
complex; EC, entorhinal cortex; PH, parahippocampal cortices.
320
HIPPOCAMPUS VOL. 2, NO. 3, JULY 1992
However, these neurons required that visual stimulation, ment of the apparatus might represent relations between test
stimuli, background stimuli fixed on the apparatus, and other
such as an object, be presented from a particular location.
Selective neurons responded more to some stimuli than to background stimuli. However, other factors might have inothers in at least one sensory modality. Hippocampal neurons fluenced the responsiveness, such as suppression by particwith selective (or differential) responses have been previ- ular stimuli that could not be seen in the usual position.
Responsiveness of egocentric neurons is considered to repously reported (Wible et al., 1986; Rolls et al., 1989; Wiener
et al., 1989; Creutzfeldt, 1990; Vidyasagar et al., 1991; Ta- resent relations between the test stimulus and background
mura et al., 1992). Furthermore, there were some reports stimuli fixed to the monkey or the restraining device, whereas
(Creutzfeldt, 1990; Vidyasagar et al., 1991) of hippocampal responsiveness of allocentric neurons is considered to inneurons that were activated by presentation of particular volve representation of relations between the test stimulus
human actions during what they called the “raisin show.” and background stimuli fixed in the room. Responsiveness of
This report is very similar to the present results in that se- neurons that is extinguished by rotation of the monkey may
be involved in representation of relations between the test
lective neurons tended to respond to human action.
Two visual information-processing pathways have been re- stimulus, background stimuli apparent after rotation of the
ported (Mishkin, 1972). One is the dorsal pathway, which is monkey, and stimuli fixed in the room, though it is also posinvolved in analysis of the location of objects, and the other sible that some other factors might influence the responsiveis the ventral pathway, which is involved in analysis of the ness.
To represent a visible object in an egocentric (head-cenphysical properties of objects. For detecting a particular location in which a particular object is located, interaction be- tered) framework, it is necessary to combine and compute
tween these two pathways is necessary. The H F and PH the information about location of the image of the object on
would be positions in which such interaction could occur, a visual field, eye position, neck position, and so on. Some
since anatomical studies (Jones and Powell, 1970; Van Hoe- neurons in the neocortical areas have been reported to resen, 1982; Amaral, 1987; Tranel et al., 1988) show inputs to spond to retinotopic space, eye position, or combinations of
the H F via the PH from the visual and auditory association these two factors (for review, see Andersen, 1987). However,
cortices after processing perception of physical properties there is still no evidence to suggest neurons in the neocortical
(Rolls et al., 1977; Gross et al., 1979; Sato et al., 1980; Fuster areas that represent aspects of spatial factors in the egocentric
and Jervey, 1982; Ungerleider and Mishkin, 1982; Desimone framework or allocentric framework. Present results suggest
et al., 1984; Miyashita, 1988; Miyashita and Chang, 1988), that neurons in the monkey H F or PH may relate stimuli in
and from the posterior parietal and prefrontal cortices, after an egocentric framework or an ailocentric framework. Thereanalysis of spatial information (Teuber, 1964; Pohl, 1973; Pe- fore, some computation or conversion of information from
trides and Iversen, 1979; Andersen and Mountcastle, 1983; the primary step of spatial representation (such as retinotopic
Passingham, 1985; Andersen, 1987; Goldman-Rakic, 1987). space) to a more complicated spatial representation (such as
Responsiveness of the visual selective neurons might reflect egocentric or allocentric space) may be made between the
results of such interaction. It has been reported that bilateral sensory association cortices and the H F and PH, or within
lesions of the H F impaired performance in a spatial memory the H F and PH. Further studies are necessary to investigate
task (Parkinson et al., 1988) that required object-place as- such computation or conversion.
sociation, so we can imagine that association between a stimACKNOWLEDGMENTS
ulus and its location in space, as reflected in responses of the
selective group, would be formed in the HF.
The authors wish to thank Dr. A. Simpson, Showa University,
for help in preparing the manuscript, and Mrs. M.
Dependence of responsiveness on relations
Yamazaki and Mrs. A. Tabuchi for typing.
between test stimulus and background cues
Supported in part by the Japanese Ministry of Education,
Responsiveness of neurons that was not modulated by
Science and Culture, Grants-in-Aid for Scientific Research
changing the location of experimental apparatus may repre02404023 and 02255106, by a Bioscience Grant for Internasent relations between the test stimulus and background stimtional Joint Research Project from the NEDO, Japan, and by
uli, other than those fixed on the apparatus. Responsiveness
Brain Science Foundation, Japan.
of the neurons that was changed by movement of the apparatus may represent relations between the test stimulus and References
background stimuli fixed on the apparatus, and these might
correspond to neurons with responses in the frame-of-ref- Amaral, D. G. (1987) Memory: Anatomical organization of candidate
brain regions. In Handbook of Physiology, The Nervous System,
erence of allocentric coordinates reported by Feigenbaum
V.B. Mountcastle, ed., vol. V, pp. 211-294, American Physiology
and Rolls (1991). It is difficult to interpret responsiveness of
Society, Bethesda, MD.
neurons that change irrespective of movement of the apparatus. It is possible that newly appearing directionally dif- Andersen, R. A. (1987) lnferior parietal lobule function in spatial
perception and visuomotor integration. In Handbook of Physiolferentiating responsiveness reflects representation of other
o g y , The Nervous System, V.B. Mountcastle, ed., vol. V, pp. 483relations between the test stimulus and background stimuli,
518, American Physiology Society, Bethesda, MD.
and this phenomenon might correspond to the firing of H F Andersen, R. A,, and V. B. Mountcastle (1983) The influence of the
“place cells” in the rat that can be changed by adding, or
angle of gaze upon the excitability of the light-sensitive neurons of
removing, intramaze or extramaze cues (Muller et al., 1987).
the posterior parietal cortex. J. Neurosci. 3532-548.
Responsiveness of neurons that was extinguished by move- Breese, C. R., R. E. Hampson, and S. A. Deadwyler (1989) Hip-
MONKEY HIPPOCAMPAL RESPONSES TO SPACE / Tamura et al.
pocampal place cells: Stereotypy and plasticity. J. Neurosci.
9: 1097-11 12.
Cahusac, P. M. B . , Y . Miyashita, and E . T. Rolls (1989) Responses
of hippocampal formation neurons in the monkey related to delayed
spatial response and object-place memory tasks. Behav. Brain Res.
33:229-240.
Cave, C. B., and L. R. Squire (1991) Equivalent impairment of spatial
and nonspatial memory following damage to the human hippocampus. Hippocampus 1:329-340.
Creutzfeldt, 0. D. (1990) Neuronal responses in human and monkey
temporal lobe during memory tasks: Compartmentalization of
memory functions. In Vision, Memory and the Temporal Lobe, E.
Iwai and M. Mishkin, eds., pp. 187-204, Elsevier, New York.
Desimone, R., T. D. Albright, C. G . Gross, and C. Bruce (1984)
Stimulus-selective properties of inferior temporal neurons in the
macaque. J. Neurosci. 4:2051-2062.
Eichenbaum. H., A. Fagan, P. Mathews, and N. Cohen (1988) Hippocampal system dysfunction and odor discrimination learning in
rats: Impairment or facilitation depending on representational demands. Behav. Neurosci. 102:331-339.
Feigenbaum, J. D., and E. T. Rolls (1991) Allocentric and egocentric
spatial information processing in the hippocampal formation of the
behaving primate. Psychobiology 19:21-40.
Foster, T. C., C. A. Castro, and B. L. McNaughton (1989) Spatial
selectivity of rat hippocampal neurons: Dependence on preparedness for movement. Science 244: 1580-1582.
Fukuda, M., T. Ono, H. Nishino, and K. Sasaki (1986) Visual responses related to food discrimination in monkey lateral hypothalamus during operant feeding behavior. Brain Res. 374:249-259.
Fuster, J. M., and J. P. Jervey (1982) Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. J. Neurosci. 2:361-375.
Goldman-Rakic, P. S. (1987) Circuitry of primate prefrontal cortex
and regulation of behavior by representational memory. In Hundbook of Physiology, The Nervous System, vol. V, V. B. Mountcastle, ed., pp. 373-417, American Physiology Society, Bethesda,
MD.
Gross, C. G., D. B. Bender, and G. L. Gerstein (1979) Activity of
inferior temporal neurons in behaving monkeys. Neuropsychologia
17:215-229.
Jones, E. G., and T. P. S. Powell (1970) An anatomical study of
converging sensory pathways within the cerebral cortex of the
monkey. Brain 93:793-820.
Mishkin, M. (1972) Cortical visual areas and their interactions. In
Brain and Human Behavior, A. G. Karczmar and J. C. Eccles,
eds., pp. 187-208, Springer-Verlag, Berlin.
Miyashita, Y. (1988) Neuronal correlate of visual associative longterm memory in the primate temporal cortex. Nature 335317-820.
Miyashita, Y., and H. S. Chang (1988) Neuronal correlate of pictorial
short-term memory in the primate temporal cortex. Nature 331:6870.
Miyashita, Y., E. T. Rolls, P. M. B. Cahusac, H. Niki, and J. D.
Feigenbaum (1989) Activity of hippocampal formation neurons in
the monkey related to a conditional spatial response task. J. Neurophysiol. 61 :669-678.
Morris, R. G . M., P. Garrud, J. N. P. Rawlins, and J. O’Keefe (1982)
Place navigation impaired in rats with hippocampal lesions. Nature
297168 1-683.
Muller, R. U., J . L. Kubie, and J. B. Ranck Jr. (1987) Spatial firing
patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7:1935-1950.
Nishijo, H., T. Ono, and H. Nishino (1988a) Topographic distribution
of modality-specific amygdalar neurons in alert monkey. J. Neurosci. 8:3556-3569.
Nishijo, H., T. Ono, and H. Nishino (1988b) Single neuron responses
321
in amygdala of alert monkey during complex sensory stimulation
with affective significance. J. Neurosci. 8:3570-3583.
O’Keefe, J. (1990) A computational theory of the hippocampal cognitive map. Prog. Brain Res. 83:301-312.
O’Keefe, J., and J. Dostrovsky (1971) The hippocampus as a spatial
map: Preliminary evidence from unit activity in freely-moving rat.
Brain Res. 34:171-175.
O’Keefe, J., and Conway, D. H. (1978) Hippocampal place units in
the freely moving rat: Why they fire where they fire. Exp. Brain
Res. 3 1:573-590.
O’Keefe, J., and L. Nadel (1978) The Hippocampus as a Cognitive
Map, Oxford, Clarendon, UK.
Olton, D. S . , J. A. Walker, and F. H. Gage (1978) Hippocampal
connections and spatial discrimination. Brain Res. 139:295-308.
Ono, T., H. Nishino, K. Sasaki, M. Fukuda, and M. Muramoto (1980)
Role of the lateral hypothalamus and the amygdala in feeding behavior. Brain Res. Bull. 5 (Suppl. 4):143-149.
Ono, T., H. Nishino, K. Sasaki, M. Fukuda, and M. Muramoto(l981)
Monkey lateral hypothalamic neuron responses to sight of food,
and during bar press and ingestion. Neurosci. Lett. 219-104.
Ono, T., R. Tamura, H. Nishijo, K. Nakamura, and E. Tabuchi(l989)
Contribution of amygdalar and lateral hypothalamic neurons to visual information processing of food and nonfood in monkey. Physiol. Behav. 45:411-421.
Ono, T., K. Nakamura, M. Fukuda, and R. Tamura (1991) Place
recognition responses of neurons in monkey hippocampus. Neurosci. Lett. 121:194-198.
Parkinson, J. K., E. A. Murray, and M. Mishkin (1988) A selective
mnemonic role for the hippocampus in monkeys: Memory for the
location of objects. J. Neurosci. 8:4159-4167.
Passingham, R. E. (1985) Memory of monkeys (Macaca mulatta) with
lesions in prefrontal cortex. Behav. Neurosci. 99:3-21.
Petrides, M . , and S. D. Iversen (1979) Restricted posterior parietal
lesions in the rhesus monkey and performance on visuospatial
tasks. Brain Res. 161:64-77.
Pohl, W. (1973) Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. J. Comp. Physiol. Psychol. 82:227-239.
Rolls, E. T., S . J. Judge, and M. K. Sanghera (1977) Activity of
neurons in the inferotemporal cortex of the alert monkey. Brain
Res. 130:229-238.
Rolls, E. T., Y. Miyashita, P. M. B. Cahusac, R. P. Kesner, H. Niki,
J . D. Feigenbaum, and L. Bach (1989) Hippocampal neurons in the
monkey with activity related to the place in which a stimulus is
shown. J. Neurosci. 9:1835-1845.
Rupniak, N. M. J., and D. Gaffan (1987) Monkey hippocampus and
learning about spatially directed movements. J. Neurosci. 7:23312337.
Sato, T., T. Kawamura, and E . Iwai (1980) Responsiveness of inferotemporal single units to visual pattern stimuli in monkeys performing discrimination. Exp. Brain Res. 38:313-319.
Smith, M. L., and B. Milner (1981) The role of the right hippocampus
in the recall of spatial location. Neuropsychologia 19:781-793.
Smith, M. L., and B. Milner (1984) Differential effects of frontal-lobe
lesions on cognitive estimation and spatial memory. Neuropsychologia 22:697-705.
Smith, M. L., and B. Milner (1989) Right hippocampal impairment
in the recall of spatial location: Encoding deficit or rapid forgetting?
Neuropsychologia 27:71-81.
Squire, L. R., A. P. Shimamura, and D. G. Amaral(l989) Memory
and hippocampus. In Neural Models of Plasticiry, H. Byrne and
W. Berry, eds., pp. 208-239, Academic Press, New York.
Sutherland, R. J., and J. W. Rudy (1989) Configural association theory: The role of the hippocampal formation in learning, memory
and amnesia. Psychobiology 17:129-144.
Swanson, L. W. (1983) The hippocampus and the concept of the
322
HIPPOCAMPUS VOL. 2, NO. 3, JULY 1992
limbic system. In Neurobiology of ihe Hippocampus, W. Seifert,
ed., pp. 3-19, Academic Press, New York.
Tamura, R., T. Ono, M. Fukuda, and K. Nakamura (1990) Recognition of egocentric and allocentric visual and auditory space by
neurons in the hippocampus of monkeys. Neurosci. Lett. 109:293298.
Tamura, R., T. Ono, M. Fukuda, and H. Nishijo (1992) Monkey hippocampal neuron responses to complex sensory stimulation during
object discrimination. Hippocampus 2:287-306
Teuber, H.-L. (1964) The riddle of frontal lobe function in man. In
The Frontal Granular Cortex and Behavior, J. M. Warren and K .
Akert, eds., pp. 410-444, McGraw-Hill, New York.
Tranel, D., D. R. Brady, G. W. Van Hoesen, and A. R. Damasio
(1988) Parahippocampal projections to posterior auditory association cortex (area Tpt) in Old-World monkeys. Exp. Brain Res.
70~406-416.
Ungerleider, W., and M. Mishkin (1982) Two cortical visual systems.
In The Analysis of Visual Behavior, D. J. Ingle, M. A . Goodale,
and R. J. W. Mansfield, eds., pp. 549-586, MIT Press, Cambridge,
MA.
Van Hoesen, G. W. (1982) The parahippocampal gyms: New obser-
vations regarding its cortical connections in the monkey. Trends
Neurosci. 5:345-350.
Vidyasagar, T. R., E. Salzmann, and 0. D. Creutzfeldt (1991) Unit
activity in the hippocampus and the parahippocampal temporobasal
association cortex related to memory and complex behaviour in
the awake monkey. Brain Res. 544:269-278.
Watanabe, T., and H. Niki (1985) Hippocampal unit activity and delayed response in the monkey. Brain Res. 325:241-254.
Wible, C. G., R. L. Findling, M. Shapiro, E. J. Lang, S. Crane, and
D. S. Olton (1986) Mnemonic correlates of unit activity in the hippocampus. Brain Res. 39997-110.
Wiener, S. I., C. A. Paul, and H. Eichenbaum (1989) Spatial and
behavioral correlates of hippocampal neuronal activity. J. Neurosci. 9:2737-2763.
Yamatani, K., T. Ono, H. Nishijo, and A. Takaku (1990) Activity
and distribution of learning-related neurons in monkey (Macaca
fuscaia) prefrontal cortex. Behav. Neurosci. 104503-53 I .
Zola-Morgan, S., and L. R. Squire (1986) Memory impairment in
monkeys following lesions limited to the hippocampus. Behav.
Neurosci. 100:155-160.