Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation.

1. In the companion paper we reported that the predominant signal of the population of neurons in the lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) encode the next intended saccadic eye movement during the delay period of a memory-saccade task. This result predicts that, should be monkey change his intention of what the next saccade will be, LIP activity should change accordingly to reflect the new plan. We tested this prediction by training monkeys to change their saccadic plan on command and recording the activity of LIP neurons across plan changes. 2. We trained rhesus monkeys (Macaca mulatta) to maintain fixation on a light spot as long as this spot remained on. During this period we briefly presented one, two, or three peripheral visual stimuli in sequence, each followed by a delay (memory period, M). After the final delay the fixation spot was extinguished, and the monkey had to quickly make a saccade to the location of the last target to have appeared. The monkey could not predict which stimuli, nor how many, would appear on each trial. He thus had to plan a saccade to each stimulus as it appeared and change his saccade plan whenever a stimulus appeared at a different location. 3. We recorded the M period activity of 81 area LIP neurons (from 3 hemispheres of 2 monkeys) in this task. We predicted that, if a neuron's activity reflected the monkey's planned saccade, its activity should be high while the monkey planned a saccade in the neuron's motor field (MF), and low while the planned saccade was in the opposite direction. The activity of most of the neurons in our sample changed in accordance with our hypothesis as the monkey's planned saccade changed. 4. In one condition the monkey was instructed by visual stimuli to change his plan from a saccade in the neuron's preferred direction to a saccade planned in the opposite direction. In this condition activity decreased significantly (P < 0.05) in 65 (80%) of 81 neurons tested. These neurons' activity changed to reflect the new saccade plan even though the cue for this change was not presented in their RF. 5. As a control we randomly interleaved, among trials requiring a plan change, trials in which the monkey had to formulate two consecutive plans to make a saccade in the neuron's preferred direction. The activity remained unchanged (P < 0.05) in 22 of 31 neurons tested (79%), indicating that the neurons continued to encode the same saccade plan. 6. In a variant of the task, the cue to the location of the required saccade was either a light spot or a noise burst from a loudspeaker. Of 22 neurons tested in this task, 16 (73%) showed activity changes consistent with plan changes cued by visual or auditory stimuli. 7. Alterations in the monkey's intentions, even in the absence of overt behavior, are manifested in altered LIP activity. These activity changes could be induced whether visual or auditory cues were used to indicate the required plan changes. Most LIP neurons thus do not encode only the locations of visual stimuli, but also the intention to direct gaze to specific locations, independently of whether a gaze shift actually occurs.

Recordings in the lateral intraparietal area (LIP) reveal that parietal cortex encodes variables related to spatial decision-making, the selection of desirable targets in space. It has been unclear whether parietal cortex is involved in spatial decision-making in general, or whether specific parietal compartments subserve decisions made using specific actions. To test this, we engaged monkeys (Macaca mulatta) in a reward-based decision task in which they selected a target based on its desirability. The animals' choice behavior in this task followed the molar matching law, and in each trial was governed by the desirability of the choice targets. Critically, animals were instructed to make the choice using one of two actions: eye movements (saccades) and arm movements (reaches). We recorded the discharge activity of neurons in area LIP and the parietal reach region (PRR) of the parietal cortex. In line with previous studies, we found that both LIP and PRR encode a reward-based decision variable, the target desirability. Crucially, the target desirability was encoded in LIP at least twice as strongly when choices were made using saccades compared with reaches. In contrast, PRR encoded target desirability only for reaches and not for saccades. These data suggest that decisions can evolve in dedicated parietal circuits in the context of specific actions. This finding supports the hypothesis of an intentional representation of developing decisions in parietal cortex. Furthermore, the close link between the cognitive (decision-related) and bodily (action-related) processes presents a neural contribution to the theories of embodied cognition.

Decision Making in Recurrent Neuronal Circuits

Categorization is an essential cognitive and perceptual process for decision-making and recognition. The posterior parietal cortex, particularly the lateral intraparietal (LIP) area has been suggested to transform visual feature encoding into abstract categorical representations. By contrast, areas closer to sensory input, such as the middle temporal (MT) area, encode stimulus features but not more abstract categorical information during categorization tasks. Here, we compare the contributions of the medial superior temporal (MST) and LIP areas in category computation by recording neuronal activity in both areas from two male rhesus macaques trained to perform a visual motion categorization task. MST is a core motion-processing region interconnected with MT and is often considered an intermediate processing stage between MT and LIP. We show that MST exhibits robust decision-correlated motion category encoding and working memory encoding similar to LIP, suggesting that MST plays a substantial role in cognitive computation, extending beyond its widely recognized role in visual motion processing.SIGNIFICANCE STATEMENT Categorization requires assigning incoming sensory stimuli into behaviorally relevant groups. Previous work found that parietal area LIP shows a strong encoding of the learned category membership of visual motion stimuli, while visual area MT shows strong direction tuning but not category tuning during a motion direction categorization task. Here we show that the medial superior temporal (MST) area, a visual motion-processing region interconnected with both LIP and MT, shows strong visual category encoding similar to that observed in LIP. This suggests that MST plays a greater role in abstract cognitive functions, extending beyond its well known role in visual motion processing.

Neurons in the lateral intraparietal (LIP) area of macaque monkey parietal cortex respond to cues predicting rewards and penalties of variable size in a manner that depends on the motivational salience of the predicted outcome (strong for both large reward and large penalty) rather than on its value (positive for large reward and negative for large penalty). This finding suggests that LIP mediates the capture of attention by salient events and does not encode value in the service of value-based decision making. It leaves open the question whether neurons elsewhere in the brain encode value in the identical task. To resolve this issue, we recorded neuronal activity in the amygdala in the context of the task employed in the LIP study. We found that responses to reward-predicting cues were similar between areas, with the majority of reward-sensitive neurons responding more strongly to cues that predicted large reward than to those that predicted small reward. Responses to penalty-predicting cues were, however, markedly different. In the amygdala, unlike LIP, few neurons were sensitive to penalty size, few penalty-sensitive neurons favored large over small penalty, and the dependence of firing rate on penalty size was negatively correlated with its dependence on reward size. These results indicate that amygdala neurons encoded cue value under circumstances in which LIP neurons exhibited sensitivity to motivational salience. However, the representation of negative value, as reflected in sensitivity to penalty size, was weaker than the representation of positive value, as reflected in sensitivity to reward size.NEW & NOTEWORTHY This is the first study to characterize amygdala neuronal responses to cues predicting rewards and penalties of variable size in monkeys making value-based choices. Manipulating reward and penalty size allowed distinguishing activity dependent on motivational salience from activity dependent on value. This approach revealed in a previous study that neurons of the lateral intraparietal (LIP) area encode motivational salience. Here, it reveals that amygdala neurons encode value. The results establish a sharp functional distinction between the two areas.

1. Extracellular discharges were recorded from neurons in the inferior temporal cortex (area TE) of three macaque monkeys while they performed visual fixation and pattern discrimination tasks. For the pattern discrimination task, monkey was trained to release the lever quickly at the onset of one of two pattern stimuli and to release the lever at the dimming of the other pattern. During this task, neutral light stimulus (light bar) to which the monkey was not required to respond was presented once a trial either prior to the onset of the discriminandum or during presentation of the pattern that dimmed later. The neuronal activities evoked by the neutral stimulus under these two conditions were compared. 2. When the discriminanda were located at the center or at 5 degrees in the contralateral visual field, one-half of the neurons showed significantly smaller responses to the neutral stimulus when it was presented during presentation of the dimming pattern than when it was presented prior to the onset of the discriminandum. 3. The suppressive effect depended on the location of the two stimuli. When the neutral stimulus was located in the ipsilateral visual field and the pattern was located in the contralateral visual field, the response to the neutral stimulus was suppressed. However, when the pattern was located in the ipsilateral visual field (5 degrees visual angle), still within the receptive field for many neurons, the suppressive effect of the pattern on the response to the neutral stimulus in the contralateral visual field was almost undetectable. 4. When the pattern was located nearer the fovea than was the neutral stimulus, the suppressive effect was greater than when the pattern was located more peripherally to the neutral stimulus. Different from the receptive field of more primary visual neurons, this suppressive effect did not appear to be related to the neuron's responsiveness to the patterns nor to precise stimulus location in the receptive field. 5. The magnitude of suppression by the attended pattern on the visual response during the pattern discrimination task correlated with the suppression noted in the presence of a fixation spot during the fixation tasks, while the animals did not fixate on the attended pattern. The response of some neurons to the neutral stimulus prior to pattern presentation during the pattern discrimination task was enhanced slightly compared with the response recorded during the simple fixation task.(ABSTRACT TRUNCATED AT 400 WORDS)

Neurons in both the lateral intraparietal area (LIP) of the monkey parietal cortex and the intermediate layers of the superior colliculus (SC) are activated well in advance of the initiation of saccadic eye movements. To determine whether there is a progression in the covert processing for saccades from area LIP to SC, we systematically compared the discharge properties of LIP output neurons identified by antidromic activation with those of SC neurons collected from the same monkeys. First, we compared activity patterns during a delayed saccade task and found that LIP and SC neurons showed an extensive overlap in their responses to visual stimuli and in their sustained activity during the delay period. The saccade activity of LIP neurons was, however, remarkably weaker than that of SC neurons and never occurred without any preceding delay activity. Second, we assessed the dependence of LIP and SC activity on the presence of a visual stimulus by contrasting their activity in delayed saccade trials in which the presentation of the visual stimulus was either sustained (visual trials) or brief (memory trials). Both the delay and the presaccadic activity levels of the LIP neuronal sample significantly depended on the sustained presence of the visual stimulus, whereas those of the SC neuronal sample did not. Third, we examined how the LIP and SC delay activity relates to the future production of a saccade using a delayed GO/NOGO saccade task, in which a change in color of the fixation stimulus instructed the monkey either to make a saccade to a peripheral visual stimulus or to withhold its response and maintain fixation. The average delay activity of both LIP and SC neuronal samples significantly increased by the advance instruction to make a saccade, but LIP neurons were significantly less dependent on the response instruction than SC neurons, and only a minority of LIP neurons was significantly modulated. Thus despite some overlap in their discharge properties, the neurons in the SC intermediate layers showed a greater independence from sustained visual stimulation and a tighter relationship to the production of an impending saccade than the LIP neurons supplying inputs to the SC. Rather than representing the transmission of one processing stage in parietal cortex area LIP to a subsequent processing stage in SC, the differences in neuronal activity that we observed suggest instead a progressive evolution in the neuronal processing for saccades.

Decisions are often made by accumulating evidence for and against the alternatives. The momentary evidence represented by sensory neurons is accumulated by downstream structures to form a decision variable, linking the evolving decision to the formation of a motor plan. When decisions are communicated by eye movements, neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence bearing on the potential targets for saccades. We now show that reach-related neurons from the medial intraparietal area (MIP) exhibit a gradual modulation of their firing rates consistent with the representation of an evolving decision variable. When decisions were communicated by saccades instead of reaches, decision-related activity was attenuated in MIP, whereas LIP neurons were active while monkeys communicated decisions by saccades or reaches. Thus, for decisions communicated by a hand movement, a parallel flow of sensory information is directed to parietal areas MIP and LIP during decision formation.

Lateral prefrontal and intraparietal cortices have strong connectional and functional associations but it is unclear how their common visuomotor, perceptual and working memory functions arise. The hierarchical scheme of cortical processing assumes that prefrontal cortex issues 'feedback' projections to parietal cortex. However, the architectonic heterogeneity of these cortices raises the question of whether distinct areas have laminar-specific interconnections underlying their complex functional relationship. Using quantitative procedures, we showed that laminar-specific connections between distinct prefrontal (areas 46 and 8) and lateral intraparietal (LIPv, LIPd and 7a) areas in Macaca mulatta, studied with neural tracers, varied systematically according to rules determined by the laminar architecture of the linked areas. We found that axons from areas 46 and rostral 8 terminated heavily in layers I-III of all intraparietal areas, as did caudal area 8 to area LIPv, suggesting 'feedback' communication. However, contrary to previous assumptions, axons from caudal area 8 terminated mostly in layers IV-V of LIPd and 7a, suggesting 'feedforward' communication. These laminar patterns of connections were highly correlated with consistent differences in neuronal density between linked areas. When neuronal density in a prefrontal origin was lower than in the intraparietal destination, most terminations were found in layer I with a concomitant decrease in layer IV. The opposite occurred when the prefrontal origin had a higher neuronal density than the target. These findings indicate that the neuronal density of linked areas can reliably predict their laminar connections and may form the basis of understanding the functional complexity of prefrontal-intraparietal interactions in cognition.

Frontal eye field (FEF) projections to posterior cortical areas were mapped by autoradiography of tritiated amino acids (Leu, Pro) in six macaque monkeys. In three monkeys, the large saccade part of the FEF (IFEF) was identified by microstimulation and injected with tracers. In a fourth monkey, the small saccade part of the FEF (sFEF) was identified by microstimulation and injected with tracer. Tracer injections were placed into the sFEF region of two other monkeys using anatomical landmarks. The IFEF and sFEF generally had distinct and largely segregated projections to posterior cortical areas, and the overall pattern of labeling in visual areas with established topology indicates that IFEF neurons preferentially project to areas having large and eccentric receptive fields, whereas sFEF neurons project to areas having smaller, more centrally located fields. The terminal fields from the sFEF were more widespread than those from IFEF. Projections from sFEF terminated in the lateral intraparietal area (LIP), the ventral intraparietal area (VIP), and the parietal part of visual area V3A, in the fundus of the superior temporal visual area (FST), the middle temporal area (MT), the medial superior temporal area (MST), the temporal part of visual area V4, the inferior temporal area (IT), and the temporal-occipital area (TEO) and in occipital visual areas V2, V3, and V4. Projections from IFEF terminated in parietal areas 7a, LIP, and VIP and the medial part of parietal area PE; in temporal areas MST and the superior temporal polysensory area (STP); and in occipital area V2 and posterior cingulate area 23b. Projections from IFEF and sFEF appeared to terminate in different parts of common target areas in MST, LIP, and V2. The topography of IFEF and sFEF projections to LIP suggests that this posterior eye field may also be organized by saccade amplitude. Most terminal labeling from FEF injections was bilaminar to layers I and V/VI, but labeling in area LIP, area MT, the medial part of area PE, and area 23b was columnar-form to all layers.

The lateral intraparietal area (LIP) contains spatially selective neurons that help guide eye movements and, according to numerous studies, do so by accumulating sensory evidence in favor of one choice (e.g., look left) or another (look right). To examine this functional link, we trained two monkeys on an urgent motion discrimination task, a task with which the evolution of both the recorded neuronal activity and the subject’s choice can be tracked millisecond by millisecond. We found that while choice accuracy increased steeply with increasing sensory evidence, at the same time, the LIP selection signal became progressively weaker, as if it hindered performance. This effect was consistent with the transient deployment of spatial attention to disparate locations away from the relevant sensory cue. The results demonstrate that spatial selection in LIP is dissociable from, and may even conflict with, evidence accumulation during informed saccadic choices.

In experiments designed to uncover the neural basis of adaptive decision making in a foraging environment, neuroscientists have reported single-cell activities in the lateral intraparietal cortex (LIP) that are correlated with choice options and their subjective values. To investigate the underlying synaptic mechanism, we considered a spiking neuron model of decision making endowed with synaptic plasticity that follows a reward-dependent stochastic Hebbian learning rule. This general model is tested in a matching task in which rewards on two targets are scheduled randomly with different rates. Our main results are threefold. First, we show that plastic synapses provide a natural way to integrate past rewards and estimate the local (in time) "return" of a choice. Second, our model reproduces the matching behavior (i.e., the proportional allocation of choices matches the relative reinforcement obtained on those choices, which is achieved through melioration in individual trials). Our model also explains the observed "undermatching" phenomenon and points to biophysical constraints (such as finite learning rate and stochastic neuronal firing) that set the limits to matching behavior. Third, although our decision model is an attractor network exhibiting winner-take-all competition, it captures graded neural spiking activities observed in LIP, when the latter were sorted according to the choices and the difference in the returns for the two targets. These results suggest that neurons in LIP are involved in selecting the oculomotor responses, whereas rewards are integrated and stored elsewhere, possibly by plastic synapses and in the form of the return rather than income of choice options.

The barn owl's central auditory system creates a map of auditory space in the external nucleus of the inferior colliculus (ICX). Although the crucial role visual experience plays in the formation and maintenance of this auditory space map is well established, the mechanism by which vision influences ICX responses remains unclear. Surprisingly, previous experiments have found that in the absence of extensive pharmacological manipulation, visual stimuli do not drive neural responses in the ICX. Here we investigated the influence of dynamic visual stimuli on auditory responses in the ICX. We show that a salient visual stimulus, when coincident with an auditory stimulus, can modulate auditory responses in the ICX even though the same visual stimulus may elicit no neural responses when presented alone. For each ICX neuron, the most effective auditory and visual stimuli were located in the same region of space. In addition, the magnitude of the visual modulation of auditory responses was dependent on the context of the stimulus presentation with novel visual stimuli eliciting consistently larger response modulations than frequently presented visual stimuli. Thus the visual modulation of ICX responses is dependent on the characteristics of the visual stimulus as well as on the spatial and temporal correspondence of the auditory and visual stimuli. These results demonstrate moment-to-moment visual enhancements of auditory responsiveness that, in the short-term, increase auditory responses to salient bimodal stimuli and in the long-term could serve to instruct the adaptive auditory plasticity necessary to maintain accurate auditory orienting behavior.

Single-unit recordings in macaque monkeys have identified effector-specific regions in posterior parietal cortex (PPC), but functional neuroimaging in the human has yielded controversial results. Here we used on-line repetitive transcranial magnetic stimulation (rTMS) to determine saccade and reach specificity in human PPC. A short train of three TMS pulses (separated by an interval of 100 ms) was delivered to superior parieto-occipital cortex (SPOC), a region over the midposterior intraparietal sulcus (mIPS), and a site close to caudal IPS situated over the angular gyrus (AG) during a brief memory interval while subjects planned either a saccade or reach with the left or right hand. Behavioral measures then were compared to controls without rTMS. Stimulation of mIPS and AG produced similar patterns: increased end-point variability for reaches and decreased saccade accuracy for contralateral targets. In contrast, stimulation of SPOC deviated reach end points toward visual fixation and had no effect on saccades. Contralateral-limb specificity was highest for AG and lowest for SPOC. Visual feedback of the hand negated rTMS-induced disruptions of the reach plan for mIPS and AG, but not SPOC. These results suggest that human SPOC is specialized for encoding retinally peripheral reach goals, whereas more anterior-lateral regions (mIPS and AG) along the IPS possess overlapping maps for saccade and reach planning and are more closely involved in motor details (i.e., planning the reach vector for a specific hand). This work provides the first causal evidence for functional specificity of these parietal regions in healthy humans.

Distinct role of primate DLPFC and LIP in hierarchical control of learned saccade sequences.