Reward-based decision signals in parietal cortex are partially embodied.

Decision Making in Recurrent Neuronal Circuits

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.

Previous studies have shown that the parietal reach region (PRR) encodes the two dimensional location of frontoparallel reach targets in an eye centered reference frame in early movement plans (Batista 1999; Snyder et al. 2000). Performing a visually guided reach initially requires the ability to perceive the depth of a target in three dimensional space. Beyond that initial perception, however, reach plans may represent the egocentric distance of the target in different ways. To investigate how a reach target is represented in three dimensions, recordings were made of the spiking activity of PRR neurons from two rhesus macaques trained to fixate and perform memory reaches to targets at different depths. Reach and fixation targets were configured to explore whether neural activity directly reflects egocentric distance as the amplitude of the required motor command, which is the absolute depth of the target, or rather the relative depth of the target with reference to fixation depth. This thesis shows that planning activity in PRR represents the depth of the reach target as a function of disparity and fixation depth, the spatial parameters important for encoding the egocentric distance of a reach goal in an eye centered reference frame. Most PRR neurons were found to be sensitive to the disparity of a reach target (82%), and vergence angle (74%) which determines fixation depth. Most PRR neurons carry both disparity and vergence angle signals, and comparisons of several modulation indices and the information carried in firing rates for each variable show a single homogenous PRR population encodes egocentric distance. The strength of modulation by disparity was maintained across vergence angle, where vergence angle gain modulates disparity tuning while preserving the location of peak tuning features in PRR neurons, which allows the absolute depth of the reach target to be decoded from the population activity. Neural activity in PRR shows a wide range of sensitivity to both target disparity and fixation depth that has never been previously tested in a reach task. The results demonstrate a specific role for PRR neurons in supporting eye-hand coordination when decoupling the effector from the point of gaze.

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.

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.

Flexible behavior depending on context is a hallmark of human cognition. During flexible behavior, the frontal and parietal cortices have complex representations that hinder efforts to conceptualize their underlying computations. We now provide evidence that neurons in the lateral intraparietal area accumulate relevant information preferentially depending on context. We suggest that behavioral flexibility is implemented in the form of temporal integration gain control in the parietal cortex.

Distributed Coding of Actual and Hypothetical Outcomes in the Orbital and Dorsolateral Prefrontal Cortex

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.

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.

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.

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.

Neurons in the parietal reach region (PRR) have been implicated in the sensory-to-motor transformation required for reaching toward visually defined targets. The neurons in each cortical hemisphere might be specifically involved in planning movements of just one limb, or the PRR might code reach endpoints generically, independent of which limb will actually move. Previous work has shown that the preferred directions of PRR neurons are similar for right and left limb movements but that the amplitude of modulation may vary greatly. We now test the hypothesis that frames of reference and eye and hand gain field modulations will, like preferred directions, be independent of which hand moves. This was not the case. Many neurons show clear differences in both the frame of reference as well as in direction and strength of gain field modulations, depending on which hand is used to reach. The results suggest that the information that is conveyed from the PRR to areas closer to the motor output (the readout from the PRR) is different for each limb and that individual PRR neurons contribute either to controlling the contralateral-limb or else bimanual-limb control.

The parietal reach region (PRR) is known to be involved in the preparation of visually guided arm movements to single targets. We explored whether PRR encodes only the target of the next movement or, alternatively, also a subsequent goal in a double-reach sequence. Two monkeys were trained to memorize the locations of two peripheral cues and to prepare for a memory-guided delayed double-reach sequence. Upon a GO-signal they had to reach in a predefined order to both remembered target locations without breaking eye fixation. The movement goals were arranged such that either the first or the second target was inside the response field of an isolated neuron. We analyzed the neural activity of single cells in PRR during the late memory period between cue offset and the GO-signal. During this memory period, most PRR cells encoded the first as well as the second goal of the planned reaching sequence. The results indicate that the posterior parietal cortex is involved in the spatial planning of more complex action patterns and represents immediate and subsequent movement goals.

A Sensorimotor Numerosity System.