1Division of Biology and 2Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125
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ABSTRACT |
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Linden, Jennifer F., Alexander Grunewald, and Richard A. Andersen. Responses to Auditory Stimuli in Macaque Lateral Intraparietal Area II. Behavioral Modulation. J. Neurophysiol. 82: 343-358, 1999. The lateral intraparietal area (LIP), a region of posterior parietal cortex, was once thought to be unresponsive to auditory stimulation. However, recent reports have indicated that neurons in area LIP respond to auditory stimuli during an auditory-saccade task. To what extent are auditory responses in area LIP dependent on the performance of an auditory-saccade task? To address this question, recordings were made from 160 LIP neurons in two monkeys while the animals performed auditory and visual memory-saccade and fixation tasks. Responses to auditory stimuli were significantly stronger during the memory-saccade task than during the fixation task, whereas responses to visual stimuli were not. Moreover, neurons responsive to auditory stimuli tended also to be visually responsive and to exhibit delay or saccade activity in the memory-saccade task. These results indicate that, in general, auditory responses in area LIP are modulated by behavioral context, are associated with visual responses, and are predictive of delay or saccade activity. Responses to auditory stimuli in area LIP may therefore be best interpreted as supramodal responses, and similar in nature to the delay activity, rather than as modality-specific sensory responses. The apparent link between auditory activity and oculomotor behavior suggests that the behavioral modulation of responses to auditory stimuli in area LIP reflects the selection of auditory stimuli as targets for eye movements.
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INTRODUCTION |
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The process of sensorimotor transformation (conversion of sensory input to motor output) for goal-directed movement presumably involves several steps. At the sensory end of the process, a stimulus is transduced and localized; at the motor end, movement is generated through coordinated muscle activation. Between these two extremes, several other events occur: for example, attention is directed toward the stimulus, the stimulus is recognized as a potential target for movement, a decision to move is made, and the location of the target is transformed from sensory to motor coordinates.
The lateral intraparietal area (LIP), a region of posterior parietal
cortex (Andersen et al. 1985), participates in these intermediate stages of sensorimotor transformation. Anatomically, area
LIP appears to be involved in conversion of visual input to oculomotor
output (Andersen 1987
; Colby et al. 1996
;
Gnadt and Andersen 1988
). Located in the middle of the
dorsal visual stream, the "where" pathway in vision
(Ungerleider and Mishkin 1982
), area LIP receives strong
visual inputs from multiple extrastriate visual areas and is
interconnected with oculomotor centers in the frontal cortex
(Andersen et al. 1985
, 1990a
;
Blatt et al. 1990
; Stanton et al. 1995
),
the superior colliculus (Lynch et al. 1985
), and the
cerebellum (via the pontine nuclei) (May and Andersen 1986
).
Like the anatomy, the physiology of LIP suggests that this area links
visual processing with oculomotor planning. Neurons in area LIP are
activated during visual stimulation (Blatt et al. 1990),
during visual attention (Colby et al. 1996
;
Gottlieb et al. 1998
), during eye movement planning
(Bracewell et al. 1996
; Gnadt and Andersen
1988
; Mazzoni et al. 1996b
; Platt and
Glimcher 1997
; Shadlen and Newsome 1996
), and
during eye movements (Barash et al. 1991a
;
Hyvärinen 1982
; Lynch et al. 1977
;
Mountcastle et al. 1975
). Visual responses in area LIP
are spatially tuned in an oculocentric coordinate frame (Barash
et al. 1991b
; Colby et al. 1995
; Gnadt
and Andersen 1988
) and additionally are modulated by eye
position (Andersen et al. 1990b
). Neurons in area LIP
respond more strongly when the visual stimulus in the receptive field is a saccadic target than when the same stimulus is a visual
distractor, even when the offset of the visual distractor is made
relevant to the behavioral task (Platt and Glimcher
1997
). Moreover, activity in area LIP seems to follow the eye
movement plan (Bracewell et al. 1996
; Mazzoni et
al. 1996b
), and LIP neurons respond more strongly to visual
stimuli that are targets for eye movements than to visual stimuli that
are targets for arm movements (Snyder et al. 1997
,
1998
). These findings indicate that area LIP plays a
special role in directing eye movements to visual stimuli.
Because auditory as well as visual stimuli can serve as targets for eye
movements, area LIP could conceivably be involved in
auditory-to-oculomotor as well as visual-to-oculomotor transformations. Although the known auditory inputs to LIP are sparse compared with the
visual inputs, at least one auditory association area, area 22 and
temporoparietal cortex (area Tpt), is linked to the posterior parietal
region (Divac et al. 1977; Hyvärinen
1982
; Pandya and Kuypers 1969
). Polysensory
areas in the superior temporal sulcus also project directly to the
intraparietal sulcus (Baizer et al. 1991
; Blatt
et al. 1990
; Seltzer and Pandya 1991
). Moreover, movement-related auditory responses have been observed in several regions of the brain that are anatomically connected to area LIP, including the frontal eye fields (Russo and Bruce 1994
;
Vaadia et al. 1986
) and the deep layers of the superior
colliculus (Jay and Sparks 1987b
).
Early physiological investigations of LIP and surrounding regions found
no auditory activity in this area (Hyvärinen 1982; Koch and Fuster 1989
; Mountcastle et al.
1975
). More recently, however, Mazzoni et al.
(1996a)
and Stricanne et al. (1996)
recorded responses to auditory stimulation in area LIP in the context of an
auditory memory-saccade task. Monkeys were trained to remember the
location of an auditory stimulus and to make a saccade to the
remembered location after a delay. Neurons in area LIP were active not
only during the movement and delay phases of this task, but also during
the auditory stimulus presentation (Mazzoni et al.
1996a
; Stricanne et al. 1996
). These recent
results, which show that neurons in area LIP respond to auditory
stimuli during an auditory-saccade task, seem to contradict the earlier
studies, which reported no evidence for activity in area LIP
during auditory stimulation.
There are several possible explanations for this apparent discrepancy. One possibility is that neurons that respond to auditory stimulation exist in area LIP but were overlooked in early studies of posterior parietal cortex. A second possibility is that LIP neurons respond to auditory stimuli after auditory-saccade training, regardless of the immediate behavioral context of the auditory stimulation after training. A third possibility is that neurons in area LIP respond to auditory stimuli only when the animal is engaged in an auditory-saccade task. Finally, a fourth possibility is that LIP neurons develop responses to auditory stimuli through auditory-saccade training, and subsequently display auditory activity primarily but not exclusively during an auditory-saccade task. Auditory responses of this type would be affected both by the animal's training history and by the immediate behavioral context in which an auditory stimulus appeared after training.
The companion paper (Grunewald et al. 1999) excludes the
first and third of these four possibilities, by demonstrating both that
auditory responses do not appear in area LIP before auditory-saccade training, and that auditory responses are observed after training when
the animal is just fixating. The present study addresses the second and
fourth possibilities, which concern the effects of immediate behavioral
context on auditory responses in the trained animal. The experiments
show that neurons in area LIP respond more strongly to auditory stimuli
when monkeys are engaged in a memory-saccade task than when they are
engaged in a fixation task. This behavioral modulation of auditory
responses resembles behavioral modulation of delay-period activity. The
experiments also reveal that LIP neurons with auditory responses tend
to have visual responses, and to exhibit delay or saccade activity.
Together, the present study and the companion paper (Grunewald
et al. 1999
) demonstrate that responses to auditory stimuli in
LIP are dependent both on long-term training history and on short-term
behavioral context. Furthermore, the results suggest that auditory
responses in area LIP are best considered supramodal responses, rather
than modality-specific sensory responses. Task-dependent increases in
responses to auditory stimuli in area LIP seem to reflect the selection
of auditory stimuli as targets for eye movements. Preliminary reports
of these results have appeared in abstract form (Grunewald et
al. 1997
; Linden et al. 1998
).
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METHODS |
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Animals, animal care, and surgical procedures
Animals, animal care, and surgical procedures, explained in
detail in the companion paper (Grunewald et al. 1999),
are summarized only briefly here. Two adult male Macaca
mulatta monkeys were used as subjects in these experiments. A
stainless steel head post, dental acrylic head cap, scleral search
coil, and stainless steel recording chamber were implanted in each
monkey using standard techniques (Judge et al. 1980
;
Mountcastle et al. 1975
). The recording chamber was
mounted normal to the surface of posterior parietal cortex (stereotaxic
coordinates at center: 6 mm posterior, 12 mm lateral) over the left
hemisphere of monkey B, and over the right hemisphere of
monkey Y. After surgery, monkeys were given at least 1 wk to
recover before behavioral training or recording began. All surgical
procedures and animal care protocols were approved by the California
Institute of Technology Institutional Animal Care and Use Committee and
were in accordance with National Institutes of Health guidelines.
Experimental setup
The experimental setup is described in the companion paper
(Grunewald et al. 1999). All experiments were conducted
in complete darkness, in a double-walled sound-attenuating anechoic
chamber (Industrial Acoustics Company). While inside the chamber, the monkey was monitored continuously with an infrared camera and a
microphone. The animal faced a fixed stimulus array consisting of a
concave rectangular grid of concentrically mounted piezoelectric speakers and light-emitting diodes (LEDs).
Free-field auditory stimuli were 500-ms bursts of band-limited noise
(5-10 kHz, 5-ms rise/fall times, 70 dB SPL). This noise band was
chosen because macaque monkeys have been reported to localize 5- to
10-kHz bandlimited noise well in azimuth (Brown et al.
1980), and because the frequency responses of the speakers were
relatively flat (±10 dB SPL) within this range. For most of the
experiments reported here, the input to each speaker was adjusted to
equalize the output amplitude spectrum to ±2 dB SPL within the 5- to
10-kHz frequency band, as measured at the location where the monkey's
head would be during an experiment. There were no qualitative
differences in behavioral or neurophysiological results obtained before
and after the speakers were equalized. Visual stimuli were 500-ms
flashes of 70-cd/m2 red light from the LEDs, each
of which subtended 0.4° of visual angle.
The monkey's head was held fixed during all behavioral training and recording sessions. Locations of stimuli are specified relative to the center of the monkey's head, in degrees azimuth right or left of the median sagittal plane and in degrees elevation above or below the visual plane. All stimuli in the concave stimulus array were ~80 cm from the monkey's head.
Behavioral paradigms
Neural recordings were obtained while the monkeys were
performing two tasks: the memory-saccade task and the fixation task (Fig. 1). Two fixed stimulus locations
were used for all experiments, because the monkeys had great difficulty
making accurate saccades to multiple auditory targets, even after
months of training. For details on training procedures, see the
accompanying paper (Grunewald et al. 1999).
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In both tasks, trials began with the appearance of a fixation light,
usually directly in front of the monkey at (0°, 0°). [For 2 units
recorded in areas that were clearly responsive to downward saccades and
to stimuli in the lower hemifield, the fixation light was positioned at
(0°, +16°), above the 2 stimulus locations.] The fixation light
remained steady after onset in the memory-saccade task, but flashed on
and off for 200 ms (and then stayed on) at the beginning of the
fixation task. This flash cue was provided to indicate to the animal
which type of task he was expected to perform on a given trial. The
monkey was required to fixate the central light within 1 s of its
appearance and to hold his eye position within a circular window of
radius 2-3° centered on that light. After a 1,000- to 1,500-ms
interval, an auditory or visual stimulus appeared for 500 ms at one of
two possible stimulus locations: left (16°, +8°) or right
(+16°, +8). The fixation light remained illuminated through this
500-ms stimulus presentation period and through a variable delay period
after stimulus offset. For the majority of the experiments, the delay
period was 1,000-1,500 ms; in the earliest experiments, a 500- to
1,000-ms or 800- to 1,300-ms delay period was used. The monkey was
required to maintain fixation through the stimulus and delay periods in
both the memory-saccade and the fixation tasks. Except for the flashing
LED at the start of fixation trials, all differences between the two
tasks occurred after the fixation light was extinguished.
In the memory-saccade task, the monkey was required to make a saccade
within 500 ms after fixation light offset, to bring his eye position
into an 8 to 16°-radius window centered 0-6° above the location at
which the auditory or visual stimulus had earlier appeared. Eye
position window parameters were adjusted within this range for each
monkey to accommodate individual variability in memory-saccade
trajectories. As previous studies have shown (Gnadt et al.
1991; White et al. 1994
), visual memory saccades display a characteristic upshift and are far more variable in endpoint
than visually guided saccades. Auditory memory saccades recorded in the
present study showed comparable upshift and endpoint variability but
were slightly larger in total amplitude (and, for monkey B,
slower in both latency and peak speed) than visual memory saccades made
under identical behavioral conditions.
After completing a memory saccade, the monkey was required to hold his eyes within the eye position window for 500 ms. Then an LED was illuminated at the true target location. To complete the memory-saccade trial and receive a reward, the monkey was required to make a corrective saccade to this visual stimulus within 100-250 ms and to hold his eye position for 500 ms within a 4°-radius window centered on the visual stimulus.
In the fixation task, the monkey was required to continue fixating straight ahead in total darkness after fixation light offset. The animal had to keep his eye position steady for 500 ms within a 4°-radius window centered on the fixation point. Then the fixation light was reilluminated. The monkey's eye position was required to be within a 2 to 3°-radius window around the fixation light within 50 ms of its reappearance; after holding his eye position steady on the reilluminated fixation light for 500 ms, the animal received a reward. The time course of the fixation task was therefore very similar to the time course of the memory-saccade task, except that the animal was required to hold fixation, not to make a saccade, when the fixation light was extinguished. Eye position was recorded for at least 500 ms after the reward, so that very late saccadic eye movements could be monitored.
All behavioral requirements, including eye position window parameters, were identical for auditory and visual trials of the same task. Moreover, auditory and visual stimulus presentations at the left and right stimulus locations were always interleaved (and presented in a balanced pseudorandom order, so that each of the 4 trial conditions appeared at least once in every set of 10 successful trials for each task). The monkey was rewarded with a drop of water or juice for fulfilling all of the behavioral conditions in a given trial. The success rate for memory-saccade trials was usually 80-90%. The success rate for fixation trials was usually >90%.
Recording procedures
Details of the recording procedures are described in the
accompanying paper (Grunewald et al. 1999). Briefly,
single-unit extracellular recording was performed using tungsten
microelectrodes, and all penetrations were approximately normal to the
gyral surface. To help ensure that recordings came from area LIP
(within the intraparietal sulcus) rather than area 7a (on the gyrus),
the electrode was advanced to 2,500-3,000 µm below the dura at the start of each recording session.
Monkeys performed the auditory and visual memory-saccade tasks
described above while the recording electrode was advanced in search of
neurons. Once a neuron had been isolated, data were collected during a
complete block (~10 trials per condition) of interleaved auditory and
visual memory-saccade trials. In each trial, an auditory or visual
stimulus appeared at one of the two possible stimulus locations,
(16°, +8°) or (+16°, +8°); locations of auditory and visual
stimuli were not optimized for the cell's receptive field. If the
neuron seemed (by visual inspection of responses) to show modulation of
its response in any period of either the auditory or the visual
memory-saccade task, data collection continued with a block of
interleaved auditory and visual fixation trials, during which stimuli
were presented at the same two locations. Memory-saccade trial blocks
were alternated with fixation trial blocks for as long as the isolation
could be maintained. Typically, one or two blocks were recorded for
each task, with about 10 trials per condition in each block.
Eye position was monitored using the scleral search coil technique
(Judge et al. 1980) and was recorded at 1,000 samples/s. At the start of each behavioral training or recording session, the
animal was required to fixate visual stimuli at each of the stimulus
locations used in the experiment, and eye position recording equipment
was calibrated.
Analysis
Unless noted otherwise, analyses are conducted on data pooled across monkeys; all significant results for pooled data are significant in data for the first monkey (monkey B) alone, and either significant or evident as a consistent trend in data for the second monkey (monkey Y, from whom fewer cells were recorded). Because pooled data combine recordings made from different hemispheres in the two monkeys, stimulus locations are identified throughout the text as contralateral or ipsilateral, relative to the hemisphere in which recordings were made. All analyses involve comparison of mean firing rates between contralateral trials (trials involving contralateral stimulus presentations) and ipsilateral trials (trials involving ipsilateral stimulus presentations). Only differences between contralateral and ipsilateral trials are analyzed, because changes in firing rate that are equivalent for contralateral and ipsilateral trials cannot be distinguished from general arousal effects. However, the trends discussed in this paper persist when such nonspecific responses are also considered.
Neural responses are analyzed in four different intervals: the prestimulus period (the 500-ms interval before auditory or visual stimulus onset), the stimulus period (the 500-ms interval from stimulus onset to stimulus offset), the delay period (the 300- to 1,300-ms interval extending from 200 ms after stimulus offset to fixation offset), and the saccade/hold period (the 500- to 800-ms interval from fixation offset to onset of the corrective visual cue). Note that the animal's behavior during the prestimulus, stimulus, and delay periods was identical in the memory-saccade and fixation tasks. During the saccade/hold period, the animal either made a saccade (in the memory-saccade task) or held his eye position steady without a fixation point (in the fixation task). All analyses are based on correctly completed trials from neural recordings that included at least one block of memory-saccade trials and at least one block of fixation trials.
Analyses of response differentials in a given period involve, for each neuron in the population, calculation of the difference between the mean firing rate in that period during contralateral trials and the mean firing rate during ipsilateral trials. The response differential is therefore the component of the neuron's response that varies with stimulus location, a measure of spatial tuning. An individual neuron has a significant spatially tuned response (or a significant response differential) in a given period if there is a significant difference in mean firing rate between contralateral and ipsilateral trials during that period (Mann-Whitney test, significance level 0.05).
Throughout the text, firing rates and response differentials are expressed in spikes per second (Hz), and nonparametric analysis methods are used wherever possible. All statistical tests are two tailed, and the critical significance level is 0.05 (n.s. means "not significant at the 0.05 significance level"). Applications of bootstrap methods involve 1,000 iterations; in each iteration, a new bootstrap data set is constructed from the original data set by sampling with replacement.
Histology
Electrolytic lesions were placed at two penetration sites in
monkey B at the end of these experiments. Histological
reconstruction of these lesion sites, described in the companion paper
(Grunewald et al. 1999), indicated that the electrode
penetrations were made in the lateral bank of the intraparietal sulcus.
Monkey Y is still a subject in ongoing experiments.
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RESULTS |
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Database
The database consists of 160 unit recordings (99 neurons from monkey B, left hemisphere; 61 neurons from monkey Y, right hemisphere) for which data were collected during at least one block of memory-saccade trials and one block of fixation trials. As explained in METHODS, the animals performed blocks of memory-saccade trials and blocks of fixation trials in alternation during each recording, for as long as the neuronal isolation seemed stable. Most of the recordings (134 neurons) include equal numbers of memory-saccade and fixation blocks (79 neurons, 1 block of each task; 54 neurons, 2 blocks of each task; 1 neuron, 3 blocks of each task). The remaining few recordings (26 neurons) ended after the second memory-saccade trial block and therefore include two memory-saccade blocks and one fixation block. Auditory and visual (and contralateral and ipsilateral) trials were interleaved within each task block.
Behavioral modulation: stimulus period
Many neurons recorded in area LIP responded more strongly to auditory stimuli during the memory-saccade task than during the fixation task. Figure 2 displays the activity of an LIP neuron during presentations of auditory stimuli at the contralateral and ipsilateral stimulus locations, in the memory-saccade task and in the fixation task. Like many other neurons in the database, this neuron has a spatially tuned auditory response; the contralateral auditory stimulus evokes significantly stronger firing than the ipsilateral auditory stimulus in both tasks (Mann-Whitney test on mean firing rates in the stimulus period: memory-saccade task, P < 0.001; fixation task, P < 0.05). Moreover, like other neurons in the database, this cell is more strongly activated by auditory stimuli in the memory-saccade task than in the fixation task.
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In contrast, many visually responsive neurons recorded in area LIP responded similarly in the memory-saccade and fixation tasks. Figure 3 shows the activity of an LIP neuron during presentations of visual stimuli. This neuron has a spatially tuned visual response in both tasks; the mean firing rate in the stimulus period is significantly higher for contralateral trials than for ipsilateral trials (Mann-Whitney test, P < 0.001 for both tasks). However, unlike the spatially tuned auditory response of the neuron in Fig. 2, the spatially tuned visual response of this cell appears almost equally strong in the memory-saccade and fixation tasks.
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Behavioral modulation of auditory and visual responses across the population is illustrated in Fig. 4. The four plots in this figure show response differentials (differences in mean firing rate between contralateral and ipsilateral trials) for the fixation task plotted against response differentials for the memory-saccade task, for the stimulus and prestimulus periods of both auditory and visual trials. All 160 neurons in the database are included in this figure, so that an unbiased estimate of behavioral modulation across the population can be obtained; because many of the neurons have no spatially tuned response (because stimulus locations were not optimized for each cell), a large cluster appears near the origin in all four plots. Behavioral modulation is assessed in two ways for the data in each plot. First, the number of neurons for which the absolute value of the response differential is greater in the memory-saccade task than in the fixation task is compared with the number of neurons for which the reverse is true. (Absolute values of response differentials are used for this categorization so that excitatory and inhibitory responses are treated similarly.) Binomial test results printed on each plot indicate the significance level for rejection of the null hypothesis that equal numbers of neurons fall into the two categories; P < 0.05 implies significant behavioral modulation of response differentials across the population. Second, the two-dimensional least-mean-squares linear fit to the data (line minimizing sum of squared perpendicular distances to data points, i.e., direction of greatest variance in the data) is determined, and 95% confidence intervals on the slope of this line are calculated using a bootstrap technique. The shaded area in each plot indicates the extent of the 95% confidence intervals. (Note that because the confidence intervals are determined through a bootstrap procedure, they are not constrained to be angularly symmetrical around the best-fit line.) If the response differential in the memory-saccade task were equivalent to the response differential in the fixation task for each cell, then the slope of the linear fit would be one; this hypothesis can be rejected if the 95% confidence intervals on the slope of the best-fit line do not include one.
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These analyses reveal that responses to auditory stimuli are modulated by behavioral task. Across the population, stimulus-period response differentials for auditory trials (Fig. 4A) are significantly larger in magnitude during the memory-saccade task than during the fixation task (binomial test, P < 0.005; slope of best-fit line significantly less than 1). In contrast, stimulus-period response differentials for visual trials (Fig. 4B) are not significantly different in the memory-saccade task and the fixation task (binomial test n.s.; slope of best-fit line not significantly different from 1). Behavioral modulation of visual responses is therefore weak or nonexistent. (Some evidence for weak behavioral modulation of visual responses does exist in the data; although behavioral modulation of visual responses is not significant for either monkey individually according to the binomial test, the slope of the best-fit line is significantly below 1 for monkey Y.) For comparison, response differentials in the prestimulus period are presented in Fig. 4, C and D. The prestimulus period response differentials are not significantly modulated by task during either auditory or visual trials (binomial tests n.s.; slopes not significantly different from 1).
The data in Fig. 4A cover a smaller range than the data in
Fig. 4B, indicating that response differentials in the
stimulus period are generally weaker during auditory trials than during visual trials. Could this difference in spatial tuning strength account
for the apparent behavioral modulation of responses to auditory but not
visual stimuli? If weakly tuned responses were modulated by task, but
strongly tuned responses were not, then the analyses would indicate
much more behavioral modulation for auditory than for visual responses.
According to this explanation for the apparent behavioral modulation of
auditory responses, weakly tuned visual responses should also be
modulated by task. Figure 5, which is
analogous to Fig. 4B, shows data from the 134 neurons with
weak stimulus-period spatial tuning during visual trials. Neurons
included in this plot have visual stimulus-period response
differentials that are within the observed range of auditory stimulus-period response differentials (10.1-17.2 Hz). Even for these weakly tuned neurons, no behavioral modulation of visual responses can be detected (binomial test n.s.; slope not significantly different from 1 in pooled data, or in each monkey's data
individually). Behavioral modulation is therefore not a necessary
consequence of weak spatial tuning.
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These results suggest that behavioral modulation might be a distinctive characteristic of auditory responses. Another possibility, however, is that behavioral modulation might be a characteristic of auditory cells, rather than of auditory responses. In other words, the apparent behavioral modulation of auditory responses might be occurring within a small subpopulation of cells for which visual responses are also modulated by task. To address this possibility, behavioral modulation during the stimulus period was analyzed exclusively for the subpopulation of 45 auditory cells: cells that have significant spatially tuned responses to auditory stimuli in at least one of the two tasks. The results of this analysis (not shown) indicate that all trends evident in Fig. 4 persist when the data set is restricted to include only auditory cells. Thus, even among neurons with significant (and strongly task-dependent) auditory responses, visual responses are not significantly modulated by behavioral task. Behavioral modulation is therefore a specific characteristic of auditory responses in area LIP, rather than a general feature of both auditory and visual responses for a distinct subpopulation of LIP neurons.
Behavioral modulation: delay and saccade/hold periods
Many neurons recorded in area LIP responded during the delay and saccade periods of both auditory and visual memory-saccade trials, but not during the delay and hold periods of fixation trials. Figure 6 shows an example of stimulus-period, delay-period, and saccade-period activity recorded from a single LIP neuron during auditory and visual trials of the memory-saccade task. As in Fig. 2, neural activity is aligned on stimulus onset. The response of this neuron is spatially tuned in the delay and saccade periods as well as in the stimulus period, for both auditory and visual memory-saccade trials (Mann-Whitney test, P < 0.005 for all 3 periods and both trial types). In the fixation task (not shown), only the response in the visual stimulus period is significantly tuned.
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Across the population, spatially tuned responses tend to be stronger during the delay and saccade periods of the memory-saccade task than during the delay and hold periods of the fixation task, as illustrated in Fig. 7. This figure is identical to Fig. 4, except that response differentials for the delay and saccade/hold periods are displayed instead of response differentials for the stimulus and prestimulus periods. Response differentials for the delay period and the saccade/hold period are significantly modulated by task in both auditory and visual trials (binomial test, P < 0.01 in all plots; all slopes significantly less than 1). Note that behavioral modulation in the delay period (Fig. 7, A and B) resembles behavioral modulation in the stimulus period of auditory trials (Fig. 4A). The slopes of the best-fit lines in Fig. 7, A and B (and in Fig. 4A) are significantly less than one but greater than zero, whereas the slopes in Fig. 7, C and D, are not significantly greater than zero.
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As the slopes in Fig. 7, A and B, suggest, response differentials in the memory-saccade task and the fixation task are significantly correlated in the delay period for both auditory trials (Spearman rank correlation coefficient rs = 0.23, P < 0.005) and visual trials (rs = 0.40, P < 0.001). Note that in the delay period, the only difference between the two tasks is the presumed behavioral state of the animal. In the memory-saccade task, the monkey is assumed to be remembering the location of the stimulus and planning an eye movement, whereas in the fixation task, the monkey is assumed to be concentrating on fixating. If these assumptions were incorrect (if, for instance, the monkey were planning to make a saccade to the remembered stimulus location after the reward in the fixation task), then response differentials in the delay period of the fixation task might be correlated with response differentials in the delay period of the memory-saccade task. In other words, one possible explanation for the correlation between memory-saccade and fixation response differentials during the delay period is that the monkeys interpreted the fixation task as an unusually complicated, very-long-delay version of the memory-saccade task.
One piece of evidence against this hypothesis is that correlation
between the two tasks is much weaker in the saccade/hold period
(rs = 0.08, n.s. for auditory
trials; rs = 0.17, P < 0.05 for visual trials). If the monkeys were making saccades after the reward in the fixation task, correlation between the two tasks should have persisted in the saccade/hold period, because neural activity associated with saccade preparation should have appeared in
both the saccade period of the memory-saccade task and the hold period
of the fixation task. The relatively weak response correlation in the
saccade/hold period might therefore be interpreted as an indication
that the monkeys were not planning memory saccades after the reward in
the fixation task. However, because the behavioral requirements of the
two tasks are different in the saccade/hold period, it is conceivable
that response correlation might decrease in that period regardless of
the monkey's behavior after the reward.
The possibility still remains, then, that delay-period correlations might arise because the monkeys made memory saccades after the reward in the fixation task. To address this possibility directly, eye position was recorded after the reward in every fixation trial, and saccadic eye movements were identified using eye velocity criteria (optimized by visual inspection of eye traces). In the majority of fixation trials, the monkey did indeed make a single saccade within 500 ms after the reward. However, these postreward eye movements did not appear to be directed toward the stimulus locations. Postreward saccades, when they occurred, were similar for contralateral and ipsilateral trials, and seemed to be highly stereotyped movements toward a default eye position slightly off the fixation point. To quantify these observations, eye positions at the end of the first postreward saccade (or at the end of the postreward recording period, for trials in which no saccade could be detected) were analyzed separately for every neural recording in the database. Recordings for which horizontal eye position distributions after the reward differed significantly between contralateral and ipsilateral fixation trials (Kolmogorov-Smirnov test, significance level 0.05) were judged to be contaminated by possible goal-directed movements. By this test, possible goal-directed eye movements occurred after auditory fixation trials in 6 of 160 recordings, and after visual fixation trials in 31 of 160 recordings. When these potentially problematic recordings are excluded from further consideration, memory-saccade and fixation response differentials are still significantly correlated in the delay period (rs = 0.22, P < 0.01 for auditory trials in reduced dataset; rs = 0.41, P < 0.001 for visual trials in reduced dataset). Therefore the observed correlation between delay activity in the memory-saccade task and delay activity in the fixation task cannot be attributed to overt postreward eye movements in the fixation task. It is possible, however, that goal-directed eye movements might be planned in the delay period of the fixation task but then canceled in the hold period.
Correlation between auditory and visual trials: stimulus period
Like the cell shown in Fig. 6, many neurons recorded in area LIP
responded to both auditory and visual stimuli in at least one of the
two tasks. The association between auditory and visual responses across
the population is illustrated in Fig. 8.
Response differentials in the stimulus period of auditory trials are
significantly correlated with response differentials in the stimulus
period of visual trials (Fig. 8, A and B) for
both the memory-saccade task (rs = 0.38, P < 0.001) and the fixation task
(rs = 0.25, P < 0.005). The correlation coefficients for both tasks are not only
significantly different from zero but also positive, indicating that
the direction of spatial tuning tends to be similar for auditory and
visual responses recorded from the same neuron. The low slopes of the
best-fit lines in Fig. 8, A and B, confirm
earlier observations that responses to auditory stimuli are generally
weaker than responses to visual stimuli. For comparison, response
differentials in the prestimulus period are shown in Fig. 8,
C and D; no correlation between auditory and
visual trials is evident in the prestimulus period for either task
(rs = 0.03, n.s. for both tasks).
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Further evidence that auditory responses tend to be associated with
visual responses emerges from the anatomic distribution of neurons with
auditory or visual responses. Figure 9
shows the distribution across electrode penetration sites of neurons
with significant spatially tuned auditory or visual responses in the stimulus period of the memory-saccade task. [A similar figure in the
accompanying paper (Grunewald et al. 1999) shows the
distribution of neurons with significant spatially tuned auditory or
visual responses in the stimulus period of the fixation task.] In both monkeys, all penetration sites that produced cells with spatially tuned
auditory responses also produced cells with spatially tuned visual
responses. Moreover, neurons with auditory responses and neurons with
visual responses are distributed across all the penetration sites, with
no evident clustering. This overlap of auditory and visual data across
penetration sites suggests that neurons with spatially tuned responses
to auditory stimuli are well integrated with visually responsive
neurons across area LIP.
|
Correlation between auditory and visual trials: delay and saccade/hold periods
Correlation between auditory and visual trials occurs in the delay and saccade periods of the memory-saccade task, as well as in the stimulus period. Across the population of recorded cells, response differentials for auditory and visual trials are significantly correlated in the delay (rs = 0.57, P < 0.001) and the saccade (rs = 0.66, P < 0.001) periods of the memory-saccade task (Fig. 10, A and C). Like the stimulus-period correlation coefficients, these delay- and saccade-period correlation coefficients are not only significantly different from zero but also positive, indicating consistent spatial tuning for delay/saccade activity recorded from the same neuron during auditory and visual memory-saccade trials. No significant correlation between auditory and visual trials is evident in response differentials for either the delay period or the hold period of the fixation task (Fig. 10, B and D).
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Correlation between stimulus, delay, and saccade periods
Studies of visual responses in area LIP have noted that
many visually responsive neurons are active in the delay or saccade periods of a memory-saccade task (Barash et al. 1991a).
Are cells with auditory responses even more likely to exhibit delay
or saccade activity than cells with visual responses? Because auditory
responses tend to co-occur with visual responses, this question is best addressed through comparison of two populations of neurons selected to
be distinct: those with significantly tuned auditory (and possibly visual) responses in the stimulus period, and those with significantly tuned visual but not auditory responses. In the memory-saccade task,
66% (23/35) of neurons with spatially tuned auditory responses in the
stimulus period also have delay-period responses, whereas 39% (25/64)
of neurons with exclusively visual stimulus-period responses are active
during the delay period. Thus neurons with auditory stimulus-period
responses are significantly more likely than neurons with exclusively
visual stimulus-period responses to exhibit delay activity
(Fisher-Irwin test, P < 0.05). Delay-period responses
were pooled across auditory and visual trials to obtain the above
results; however, significant associations between auditory responses
and delay activity are also found when delay-period responses are
considered separately for auditory and visual trials.
Results for the saccade period are similar. Over 77% (27/35) of neurons with auditory stimulus-period responses in the memory-saccade task respond during the saccade period, whereas 52% (33/64) of exclusively visual cells respond during the saccade period. Neurons with auditory responses in the stimulus period are therefore significantly more likely to show saccade activity than neurons with exclusively visual stimulus-period responses (Fisher-Irwin test, P < 0.05). Again, this trend is evident not only when saccade-period responses are pooled across auditory and visual trials, but also when auditory and visual trials are considered separately.
These results indicate that auditory responses in the stimulus period of the memory-saccade task are more closely linked to delay and saccade activity than are exclusively visual responses. Could auditory responses be used to identify a subpopulation of visually responsive neurons in area LIP that are likely to be active in later phases of the memory-saccade task? To find out, two populations of visually responsive neurons can be compared (Fig. 11): bimodal cells, defined to be neurons with spatially tuned stimulus-period responses during both visual and auditory memory-saccade trials; and unimodal (exclusively visual) cells, defined to be neurons with spatially tuned stimulus-period responses during visual but not auditory memory-saccade trials. Figure 11, A-D, shows data taken from visual trials of the memory-saccade task; Fig. 11, A and C, displays data from bimodal cells, whereas Fig. 11, B and D, displays data from unimodal visual cells. The division of visually responsive neurons between the left and right halves of the figure is therefore determined entirely by the presence or absence of auditory responses. As shown in the figure, the correlation between stimulus-period response differentials and delay-period response differentials during visual trials is much stronger for neurons with both auditory and visual stimulus-period responses than for neurons with exclusively visual stimulus-period responses (bimodal cells: rs = 0.70, P < 0.001; unimodal visual cells: rs = 0.20, n.s.). The difference between the two correlation coefficients is significant (Fisher z-transformation test, P < 0.01), and the slope of the best-fit line in Fig. 11A is significantly greater than the slope of the best-fit line in Fig. 11B. The distinction between bimodal and unimodal visual cells is weaker in the saccade period (Fig. 11, C and D); although the correlation coefficient is slightly larger and the slope of the best-fit line higher for bimodal cells than for unimodal visual cells, these differences are not significant.
|
The association between auditory responses and activity in later periods of the memory-saccade task suggests that auditory responses themselves might be saccade related. Analysis of error trials (memory-saccade trials in which the monkeys made saccades to the incorrect location) could, in principle, be used to determine whether auditory responses are in fact more dependent on the upcoming saccade trajectory than on the auditory stimulus location. Unfortunately, the statistical power of error trial analysis was very low for this data set, because there were few error trials. Comparison of stimulus-period response differentials for error trials with stimulus-period response differentials for correct trials revealed neither significant anti-correlation nor significant correlation, and was therefore inconclusive. Analyses of possible relationships between auditory responses and saccade parameters in correct trials were also inconclusive.
Control for response measure
Raw response differentials reflect the magnitude of spatial tuning, a quantity that is only indirectly related to the significance of spatial tuning. Analyses of response-differential distributions (Figs. 4, 5, 7, 8, 10, and 11) might therefore overemphasize data from high-firing but poorly tuned cells. To control for possible artifacts associated with the use of raw response differentials, all analyses of response-differential distributions were repeated using three different normalized response measures: 1) the response differential normalized by the mean prestimulus-period firing rate, a measure of spatial tuning relative to background activity; 2) the response differential normalized by the response sum (mean contralateral response plus mean ipsilateral response), a measure of spatial tuning relative to overall response; and 3) the response differential normalized by its estimated standard error, a direct measure of the significance of spatial tuning. Results obtained using all three normalized measures are consistent with those shown for raw response differentials.
Control for block order
For each neural recording in this experiment, blocks of memory-saccade and fixation trial data were always collected in the same order: first a block of memory-saccade trials, then a block of fixation trials, and so on in alternation, for as long as the isolation could be maintained. On average, then, blocks of fixation trials were collected later in each recording than blocks of memory-saccade trials. Stronger spatial tuning in the memory-saccade task than in the fixation task could, in principle, arise from systematic changes (such as a decrease in overall firing rate) over the course of each recording. One control for such effects has already been shown; response differentials in the prestimulus period do not appear to be modulated by task (Fig. 4, C and D). As an additional control, response differentials in the first block of fixation trials were compared with response differentials in the second block of memory-saccade trials (for the 81 recordings with at least 1 block of fixation trials and 2 blocks of memory-saccade trials). Thus for this analysis, data were selected such that fixation blocks were collected earlier in each recording than memory-saccade blocks. All trends in Figs. 4, 5, and 7 were also evident in this control analysis, confirming that observed behavioral modulation effects are not an artifact of block order.
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DISCUSSION |
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The main result of the present study is that neurons in area LIP respond more strongly to auditory stimuli when monkeys are engaged in a memory-saccade task than when they are engaged in a fixation task. Additional findings are as follows: 1) visual responses, unlike auditory responses, are not significantly modulated by behavioral task; 2) behavioral modulation of auditory responses resembles behavioral modulation of delay-period activity; 3) auditory responses are associated with visual responses in both the memory-saccade task and the fixation task; and 4) auditory responses are also associated with delay or saccade activity. Taken together, these results imply that auditory responses in area LIP are best considered supramodal (cognitive or motor) responses, rather than modality-specific sensory responses.
In combination with the results of the companion paper
(Grunewald et al. 1999), which show that auditory
responses appear in the fixation task only after auditory-saccade
training, these findings indicate that the last of the four
possibilities raised in the INTRODUCTION is correct:
responses to auditory stimuli in area LIP depend both on training and
on behavioral context. Therefore the resolution to the apparent
discrepancy between early studies of area LIP, which found no responses
to auditory stimulation (Hyvärinen 1982
;
Koch and Fuster 1989
; Mountcastle et al.
1975
), and later studies, which did find auditory responses in
LIP (Mazzoni et al. 1996a
; Stricanne et al.
1996
), is that the monkeys had both learned an auditory-saccade
task and been required to perform this task in the latter but not the
former study. Further implications of the results, and interpretations
in light of previous studies, are discussed below.
Behavioral modulation of auditory responses
Responses to auditory stimuli in area LIP are strongly modulated by behavior, whereas responses to visual stimuli do not appear to be dependent on task. Behavioral modulation of auditory responses is not a necessary consequence of weak spatial tuning, nor a general feature of all stimulus-period responses for cells that respond to auditory stimuli. Moreover, no behavioral modulation is observed in the prestimulus period, and behavioral modulation is not an artifact of trial block order. Behavioral modulation therefore seems to be a robust and distinctive characteristic of auditory responses in area LIP.
This study is the first to show that auditory responses in area LIP are
dependent on behavioral task. However, behavioral modulation of
auditory responses has previously been observed in several regions of
the brain that are directly interconnected with area LIP. Neurons in
the deep layers of the superior colliculus, for example, respond to
auditory stimuli in the context of a saccade task, but habituate
rapidly to auditory stimuli when no saccade is required (Jay and
Sparks 1984, 1987b
). Neurons in the prefrontal cortex also respond to auditory stimuli more strongly in the context of
goal-directed (arm and eye) movements than in the context of an
auditory detection or a passive listening task (Vaadia et al. 1986
). Responses to auditory stimuli in these areas, and
responses to auditory stimuli in area LIP, may best be considered
cognitive or motor responses, related primarily to the signficance of
the stimulus as a potential target for movement.
No behavioral modulation of visual responses?
Across the population of neurons recorded in this study, visual
responses and background (prestimulus) activity are not significantly modulated by behavioral task. This result seems to contradict recent
reports that visual responses and background activity in area LIP are
enhanced in a memory-saccade task relative to a fixation task
(Colby et al. 1996). Even when reanalyzed using the
analysis methods described in Colby et al. (1996)
, to
compare maximal responses rather than response differentials in the two
tasks, the data collected in the present experiment still show no
evidence for behavioral modulation of visual responses in the stimulus
period (for either monkey alone or for both together), and no evidence for modulation of responses in the prestimulus period. The apparent discrepancies between the present study and Colby et al.
(1996)
are therefore not likely to be due to differences in
data analysis methods.
The discrepancies between the present study and that of Colby et
al. (1996) might, however, arise from differences in behavioral paradigms and recording procedures. For the present experiments, two
fixed stimulus locations were used, and stimulus presentations were
randomized across the two locations. The monkeys therefore did not know
which of the two possible stimulus locations would be relevant on any
given trial until the stimulus actually appeared. In contrast,
Colby et al. (1996)
optimized the stimulus location for
each cell and then used that one stimulus location for all experiments
on the cell. Their monkeys therefore knew the location of the relevant
stimulus even before it appeared on a given trial. Colby et al.
(1996)
did suggest that the background enhancement they
observed in the memory-saccade task might have arisen because the
monkeys were anticipating the onset of the behaviorally relevant stimulus in the receptive field. Another possibility is that
enhancement of both background activity and visual responses occurred
in the memory-saccade task because the monkeys were planning the
impending movement (Bracewell et al. 1996
;
Mazzoni et al. 1996b
; Platt and Glimcher
1997
; Shadlen and Newsome 1996
).
Behavioral modulation of delay activity
Neurons in area LIP are more active in the delay and saccade periods of the memory-saccade task than in the delay and hold periods of the fixation task, for both auditory and visual trials. This result was expected. In the memory-saccade task, the monkey must remember the location of a previously presented stimulus, plan an eye movement, and execute a saccade. Delay activity is thought to reflect motor intention or spatial attention that would be engaged in the delay period of the memory-saccade task but not in the delay period of the fixation task. Similarly, saccade activity should occur only in the saccade period of the memory-saccade task, not in the hold period of the fixation task.
A more unexpected finding is that behavioral modulation in the delay period resembles behavioral modulation in the auditory stimulus period. Like auditory responses, delay-period responses are weaker, on average, during fixation trials than during memory-saccade trials, but some activity does persist in the fixation task. Indeed, response differentials in the delay period of fixation trials are significantly correlated with response differentials in the delay period of memory-saccade trials. This correlation might be considered evidence that the animals did not fully realize that they were supposed to be performing a fixation task (rather than a very-long-delay version of the memory-saccade task). Certainly, delay-period activity is usually associated with movement planning or peripherally directed attention, neither of which was required in the fixation task. For three reasons, however, it seems very unlikely that the animals were misinterpreting the fixation task. First of all, the behavioral paradigm for fixation trials ensured that eye movements toward the stimulus locations within 1,500-2,500 ms after stimulus offset would cause the trial to be aborted. Second, the use of trial blocking and task cues (steady fixation light onset in memory-saccade trials, flashing onset in fixation trials) made the presentation of fixation trials entirely predictable. Third, the correlation does not disappear when the data set is restricted to recordings that are unlikely to be contaminated by very late, goal-directed eye movements in the fixation task.
Rather than aberrant behavioral strategies, the observed correlation in
delay-period response differentials may reflect covert orienting
responses or attentional effects. Auditory and visual stimuli may evoke
default movement plans or sustained attentional orienting that activate
area LIP during the delay period of the fixation task, even though the
fixation task does not require either an eye movement or a redirection
of attention. In support of this view, previous studies have
demonstrated that movement plans are represented in LIP even when the
movement is never executed (Bracewell et al. 1996;
Snyder et al. 1997
, 1998
). The apparent similarity between behavioral modulation of delay activity and behavioral modulation of auditory responses therefore raises the possibility that both delay activity and auditory responses reflect default movement plans.
Association between auditory and visual responses
Neurons with auditory stimulus-period responses tend to have visual stimulus-period responses with similar spatial tuning, in both the memory-saccade task and the fixation task. Moreover, neurons that respond during the delay or saccade periods of auditory memory-saccade trials are likely to respond similarly during the corresponding periods of visual memory-saccade trials. No such correlation between auditory and visual trials can be detected in the delay or hold periods of the fixation task, or in the prestimulus period of either task. Thus correlations between auditory and visual trials occur specifically during stimulus presentations in both tasks, and during the later phases of the memory-saccade task.
These findings are consistent with the results of previous studies of
auditory and visual responses, both in area LIP and in regions of the
brain that are anatomically connected to area LIP. In an earlier
investigation of LIP activity during auditory and visual memory-saccade
trials, Mazzoni et al. (1996a) concluded that neurons
active during the stimulus, delay, or saccade periods of an auditory
memory-saccade task tended to be active during the same periods of a
visual memory-saccade task. The present study confirms those results
and further demonstrates that an association between auditory and
visual trials also exists during the stimulus period, but not later
periods, of a fixation task. Similar response correlations between
auditory and visual trials, either during sensory stimulation or during
later phases of a movement task, have also been noted in the superior
colliculus (Jay and Sparks 1984
, 1987a
;
Wallace et al. 1996
), frontal cortex (Vaadia et
al. 1986
), frontal and supplementary eye fields (Russo and Bruce 1994
; Schall 1991b
), and supplementary
motor areas (Schall 1991a
).
The observed correlations between auditory and visual trials during the delay and saccade periods of the memory-saccade task could be viewed as confirmation that activity during these periods is related to target selection or movement planning. Movement cues of different sensory modalities evoke similar delay and saccade activity in LIP; therefore this activity probably reflects supramodal processes, such as motor intention or spatial attention. By extension, the association between auditory and visual responses in the stimulus period implies that some component of stimulus-evoked activity in area LIP also reflects movement planning or target selection. The results therefore lend support to the idea that responses to auditory stimuli in area LIP are supramodal intentional or attentional responses, rather than modality-specific sensory responses.
Association between auditory and delay/saccade activity
Neurons with auditory stimulus-period responses are much more likely to display delay or saccade activity than neurons with exclusively visual stimulus-period responses. Moreover, in the visual memory-saccade task, correlation between stimulus-period and delay-period activity is higher for neurons with both auditory and visual stimulus-period responses than for neurons with exclusively visual stimulus-period responses. These findings suggest that neurons in area LIP that respond to auditory stimuli are more directly involved in eye-movement planning than neurons that respond to visual stimuli alone. Given the physiological similarities between area LIP, the frontal eye fields, and the deep layers of the superior colliculus, a similar association between auditory and delay- or saccade-related activity may be evident in the frontal eye fields and the superior colliculus. Previous studies of these areas have not provided data appropriate for direct comparison with the present results.
Experimental considerations
The results of the present study indicate that auditory responses in area LIP are dependent on behavioral task, associated with visual responses, and predictive of delay or saccade activity. It should be noted, however, that these findings may be dependent on the choice of experimental conditions. Four possible caveats seem especially worthy of consideration.
First, the auditory stimuli used in the present study were bursts of high-frequency band-limited white noise (5-10 kHz), which probably have little ethological significance to monkeys. Sounds with different spectral characteristics (e.g., macaque vocalizations) might conceivably elicit auditory responses in area LIP that are less dependent on behavioral task than the responses observed in the present study.
Second, in these experiments, auditory stimuli were presented only at locations within the visual field, at relatively small eccentricities (16° in azimuth, 8° in elevation; ~18° in eccentricity). Because primates may use auditory spatial cues primarily for localizing targets outside of the visual field, it is possible that auditory stimuli presented at large eccentricities might evoke auditory responses in area LIP that are not associated with visual responses. Moreover, if neurons in area LIP have auditory receptive fields that are more peripheral than their visual receptive fields, then the two fixed stimulus locations used in the present experiment might occasionally have been optimal for a neuron's visual receptive field, but might never have been optimal for any neuron's auditory receptive field. Apparent behavioral modulation of responses to auditory stimuli might turn out to be behavioral modulation of responses to suboptimal stimuli. This scenario seems unlikely, because weakly tuned visual responses (which presumably represent responses to suboptimal visual stimuli) do not appear to be modulated by task (Fig. 5); however, the possibility cannot be ruled out on the basis of the present data.
Third, the position of the pinnae was not controlled in these
experiments. Therefore, the apparent link between auditory responses and eye movements might actually reflect an association between auditory responses and pinna movement. Moreover, if the monkeys moved
their pinnae differently during the stimulus periods of memory-saccade
and fixation trials, auditory stimuli might have been filtered
differently by the ears in the two tasks, producing apparent behavioral
modulation of auditory responses. Although these possibilities cannot
be excluded, they seem very unlikely. Previous studies have shown that
the incidence of auditory responses in area LIP, and the tuning of
auditory responses in superior colliculus, are not significantly
altered by pinna restraint in awake monkeys (Jay and Sparks
1987b; Stricanne et al. 1996
). Furthermore, although pinna movements have not been studied intensively in monkeys,
a recent behavioral study in cats suggests that pinna movements could
not account for the observed behavioral modulation of auditory
responses. Cats make auditory-evoked pinna movements, which do not
appear to be dependent on behavioral task, and orienting pinna
movements, which occur in conjunction with eye movements (Populin and Yin 1998
). If we assume that these results
generalize to monkeys, pinna movements in response to auditory
stimulation should have been the same for the two behavioral tasks, and
pinna movements in conjunction with eye movements should not have
occurred until long after the auditory stimulus period.
Finally, the monkeys used in the present study performed all the
behavioral tasks with their heads immobilized. Under more natural
conditions, primates orient to auditory and visual stimuli with a
combined movement of the head and eyes (Goldring et al. 1996; Whittington et al. 1981
). Because auditory
targets can be perceived at larger eccentricities than visual targets,
and can therefore evoke larger orienting movements, responses to
auditory stimuli may be strongly associated with free head movement.
Responses to auditory stimuli in area LIP might therefore be most
robust in the context of head movements, rather than eye movements.
Although these potential caveats should not be overlooked, it seems
likely that the present results will generalize to other experimental
conditions, because the findings are consistent with previous studies
of auditory responses in areas that are anatomically interconnected
with LIP. In particular, behavioral modulation of auditory responses,
and associations between auditory and visual responses, have been
observed in both superior colliculus and frontal cortex under a range
of different experimental conditions (superior colliculus: Jay
and Sparks 1987b; Wallace et al. 1996
; frontal
cortex: Russo and Bruce 1994
; Vaadia et al.
1986
). The present findings are also consistent with current
interpretations of LIP function, as discussed further in the following section.
Interpretations
The present study demonstrates that responses to auditory stimuli in area LIP are dependent on behavioral task, associated with visual responses, and predictive of delay or saccade activity. These results imply that responses to auditory stimuli in area LIP are best considered supramodal responses, not modality-specific sensory responses. Several different interpretations of these findings, and of the role of area LIP in auditory-to-oculomotor processing, are possible.
For example, auditory activity in area LIP may be related to spatial
attention that is not modality specific (Colby et al. 1996; Gottlieb et al. 1998
). According to this
interpretation, LIP responses to auditory stimuli are stronger in the
memory-saccade task than in the fixation task because the animal must
attend more closely to the spatial information present in the auditory cue when a localization movement is required. The fact that auditory responses in area LIP are weaker and more dependent on behavioral task
than visual responses implies, in this scenario, that auditory stimuli
do not capture spatial attention as effectively as visual stimuli.
Indeed, the auditory stimuli used in this experiment were probably less
easy to localize (and perhaps less spatially salient) than the visual
stimuli, given that the monkeys required months of training to
master the auditory-saccade task but only a few days to master the
visual-saccade task (see Grunewald et al. 1999
).
The results of the present study are also consistent with the view that
activity in area LIP reflects movement intention (Bracewell et
al. 1996; Mazzoni et al. 1996b
; Platt and
Glimcher 1997
; Snyder et al. 1997
,
1998
). According to this interpretation, responses to
auditory stimuli in area LIP are modulated by behavioral task because
auditory stimuli evoke more definite movement plans in the
memory-saccade task than in the fixation task; similarly, auditory
responses are more task dependent than visual responses because
auditory orienting is less reflexive than visual orienting (at least
for the stimuli used in this study). Residual activity in the stimulus
period of auditory fixation trials, discussed further in the companion
paper (Grunewald et al. 1999
), represents a suppressed
intention to make an eye movement to an auditory target made familiar
by months of saccade training. Consistent with this interpretation, the
link between auditory stimulus-period responses and delay or saccade
activity in the memory-saccade task implies that responses to auditory
stimuli in LIP are directly related to movement intention.
A third possible interpretation of the data is that responses to
auditory stimuli in area LIP reflect oculomotor significance: the
significance of the stimuli as potential targets for eye movements. By
this argument, the stimulus-period auditory activity in the fixation
task reflects the learned significance of the auditory stimulus as a
possible eye movement target (Grunewald et al. 1999). When the sound becomes an obligate target for an eye movement in the
memory-saccade task, its significance increases further. However, in
the memory-saccade task, the increase in the auditory stimulus-period
response is linked to the presence of continued activity in the delay
period, and other experiments have shown that delay-period activity
generally reflects the monkey's intention to make eye movements
(Snyder et al. 1997
, 1998
). Thus a
simpler explanation for the increase in stimulus-period activity in the auditory memory-saccade task may be that movement-planning activity is
added to activity reflecting the learned significance of the auditory stimulus.
Finally, a fourth possibility is that spatial attention, motor intention, and oculomotor significance are artificial psychological distinctions for area LIP, which performs sensory-to-motor transformations for saccades. According to this view, increased activity in the stimulus period of the auditory memory-saccade task simply reflects a graded increase in the preparation for a sensory-guided eye movement.
The present study was designed to resolve discrepancies between early
and more recent reports regarding auditory activity in LIP, not to
distinguish between the four possible interpretations of auditory
responses described above. Further research will be required to
determine the degree to which behavioral modulation of auditory
activity supports these different interpretations. For instance, if
future experiments show that auditory stimuli evoke stronger responses
in LIP when a monkey plans a saccade to an auditory target than when he
plans a reach to the same target, then a significant component of
auditory activity in LIP represents intention to make a saccade,
independent of spatial attention. Because delay activity in LIP is
linked to the eye movement plan (Snyder et al. 1997,
1998
), the close association between delay activity and
responses to auditory stimuli suggests that activity in the auditory
stimulus period does contain a substantial intentional component.
Therefore, behavioral modulation of responses to auditory stimuli in
area LIP may primarily reflect selection of auditory stimuli as targets
for eye movements.
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ACKNOWLEDGMENTS |
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The authors thank M. Sahani for data acquisition software and technical assistance, B. Gillikin for technical assistance, C. Reyes for administrative assistance, and Drs. M. Sahani, Y. E. Cohen, and K. V. Shenoy for helpful comments on the manuscript.
This work was supported by the National Institutes of Health and by the Boswell Foundation. Support for J. F. Linden was provided by a Howard Hughes Medical Institute Predoctoral Fellowship. Support for A. Grunewald was provided by the McDonnell-Pew Program in Cognitive Neuroscience.
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FOOTNOTES |
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Address for reprint requests: R. A. Andersen, Division of Biology, California Institute of Technology, Mail Code 216-76, Pasadena, CA 91125.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 14 August 1998; accepted in final form 17 March 1999.
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REFERENCES |
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