Jacqueline Gottlieb

The representation of visual salience in monkey parietal cortex.

When natural scenes are viewed, a multitude of objects that are stable in their environments are brought in and out of view by eye movements. The posterior parietal cortex is crucial for the analysis of space, visual attention and movement. Neurons in one of its subdivisions, the lateral intraparietal area (LIP), have visual responses to stimuli appearing abruptly at particular retinal locations (their receptive fields). We have tested the responses of LIP neurons to stimuli that entered their receptive field by saccades. Neurons had little or no response to stimuli brought into their receptive field by saccades, unless the stimuli were behaviourally significant. We established behavioural significance in two ways: either by making a stable stimulus task-relevant, or by taking advantage of the attentional attraction of an abruptly appearing stimulus. Our results show that under ordinary circumstances the entire visual world is only weakly represented in LIP. The visual representation in LIP is sparse, with only the mostsalient or behaviourally relevant objects being strongly represented.

Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task

The close relationship between saccadic eye movements and vision complicates the identification of neural responses associated with each function. Visual and saccade-related responses are especially closely intertwined in a subdivision of posterior parietal cortex, the lateral parietal area (LIP). We analyzed LIP neurons using an antisaccade task in which monkeys made saccades away from a salient visual cue. The vast majority of neurons reliably signaled the location of the visual cue. In contrast, most neurons had only weak, if any, saccade-related activity independent of visual stimulation. Thus, whereas the great majority of LIP neurons reliably encoded cue location, only a small minority encoded the direction of the upcoming saccade.

Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior.

Neural activity in the lateral intraparietal area (LIP) has been associated with attention to a location in visual space, and with the intention to make saccadic eye movement. In this study we show that neurons in LIP respond to recently flashed task-irrelevant stimuli and saccade targets brought into the receptive field by a saccade, although they respond much to the same stimuli when they are stable in the environment. LIP neurons respond to the appearance of a flashed distractor even when a monkey is planning a memory-guided delayed saccade elsewhere. We then show that a monkeys attention, as defined by an increase in contrast sensitivity, is pinned to the goal of a memory-guided saccade throughout the delay period, unless a distractor appears, in which case attention transiently moves to the site of the distractor and then returns to the goal of the saccade. LIP neurons respond to both the saccade goal and the distractor, and this activity correlates with the monkeys locus of attention. In particular, the activity of LIP neurons predicts when attention migrates from the distractor back to the saccade goal. We suggest that the activity in LIP provides a salience map that is interpreted by the oculomotor system as a saccade goal when a saccade is appropriate, and simultaneously is used by the visual system to determine the locus of attention.

Reward Modulates Attention Independently of Action Value in Posterior Parietal Cortex

While numerous studies have explored the mechanisms of reward-based decisions (the choice of action based on expected gain), few have asked how reward influences attention (the selection of information relevant for a decision). Here we show that a powerful determinant of attentional priority is the association between a stimulus and an appetitive reward. A peripheral cue heralded the delivery of reward or no reward (these cues are termed herein RC+ and RC−, respectively); to experience the predicted outcome, monkeys made a saccade to a target that appeared unpredictably at the same or opposite location relative to the cue. Although the RC had no operant associations (did not specify the required saccade), they automatically biased attention, such that an RC+ attracted attention and an RC− repelled attention from its location. Neurons in the lateral intraparietal area (LIP) encoded these attentional biases, maintaining sustained excitation at the location of an RC+ and inhibition at the location of an RC−. Contrary to the hypothesis that LIP encodes action value, neurons did not encode the expected reward of the saccade. Moreover, at odds with an adaptive decision process, the cue-evoked biases interfered with the required saccade, and these biases increased rather than abating with training. After prolonged training, valence selectivity appeared at shorter latencies and automatically transferred to a novel task context, suggesting that training produced visual plasticity. The results suggest that reward predictors gain automatic attentional priority regardless of their operant associations, and this valence-specific priority is encoded in LIP independently of the expected reward of an action.

The role of the lateral intraparietal area of the monkey in the generation of saccades and visuospatial attention.

Abstract: The brain cannot monitor or react towards the entire world at a given time. Instead, using the process of attention, it selects objects in the world for further analysis. Neuronal activity in the monkey intraparietal area has the properties appropriate for a neuronal substrate of attention: instead of all objects being represented in the parietal cortex, only salient objects are. Such objects can be salient because of their physical properties (recently flashed objects or moving objects) or because they can be made important to the animal by virtue of a task. Although lateral intraparietal area (LIP) neurons respond through the delay period of a memory‐guided saccade, they also respond in an enhanced manner to distractors flashed during the delay period of a memory‐guided saccade being generated to a position outside the receptive field. This activity parallels the monkeys psychophysical attentional process: attention is ordinarily pinned at the goal of a memory‐guided saccade, but it shifts briefly to the locus of a task‐irrelevant distractor flashed briefly during the delay period and then returns to the goal. Although neurons in LIP have been implicated as being directly involved in the generation of saccadic eye movements, their activity does not predict where, when, or if a saccade will occur. The ensemble of activity in LIP, however, does accurately describe the locus of attention.

Information-seeking, curiosity, and attention: computational and neural mechanisms.

Intelligent animals devote much time and energy to exploring and obtaining information, but the underlying mechanisms are poorly understood. We review recent developments on this topic that have emerged from the traditionally separate fields of machine learning, eye movements in natural behavior, and studies of curiosity in psychology and neuroscience. These studies show that exploration may be guided by a family of mechanisms that range from automatic biases toward novelty or surprise to systematic searches for learning progress and information gain in curiosity-driven behavior. In addition, eye movements reflect visual information searching in multiple conditions and are amenable for cellular-level investigations. This suggests that the oculomotor system is an excellent model system for understanding information-sampling mechanisms.

Intrinsic circuitry and physiological properties of pyramidal neurons in rat barrel cortex.

Abstract Pyramidal neurons in the rat posteromedial barrel subfield (PMBSF) were characterized physiologically and filled with biocytin in in vitro brain slices. Intrinsic axons belonging to supragranular neurons pro-jected horizontally and vertically, arborizing in layers II/III and V, but had few or no projections to layers IV or VI. These axons projected horizontally for up to 2 mm, spanning two to seven barrel columns. Layer V neurons had more diffuse axon arbors that projected either vertically, arborizing in layers III to V, or horizontally, branching profusely in layers V and VI. The basal dendritic trees of neurons in layers II/III, V and VI spanned one or two barrel columns without being skewed toward particular barrel columns. Physiologically, regular- spiking neurons were classified as ”RS1” or ”RS2” according to their degree of late spike frequency adaptation. RS1 neurons were found in superficial and deep layers, whereas RS2 neurons were significantly more prevalent in the latter. Infragranular, but not supragranular neurons showed slow, inward rectification at hyperpolarized potentials. All neurons generated fast and medium afterhyperpolarizations following individual spikes; however, only infragranular pyramids had depolarizing afterpotentials interposed between the two afterhyperpolarizations. RS1 neurons had larger cell bodies, longer total basal dendritic lengths, and more densely branched proximal dendritic trees than RS2 neurons. These findings indicate that pyramidal neurons in the deep and superficial layers of the rat PMBSF have distinct patterns of intracortical axon arbors and distinct physiological properties. These features are probably involved in shaping and modulating the response properties of PMBSF neurons.

Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe

The posterior parietal cortex and the prefrontal cortex are associated with eye movements and visual attention, but their specific contributions are poorly understood. We compared the dorsolateral prefrontal cortex (dlPFC) and the lateral intraparietal area (LIP) in monkeys using a memory saccade task in which a salient distractor flashed at a variable timing and location during the memory delay. We found that the two areas had similar responses to target selection, but made distinct contributions to distractor suppression. Distractor responses were more strongly suppressed and more closely correlated with performance in the dlPFC relative to LIP. Moreover, reversible inactivation of the dlPFC produced much larger increases in distractibility than inactivation of LIP. These findings suggest that LIP and dlPFC mediate different aspects of selective attention. Although both areas can contribute to the perceptual selection of salient information, the dlPFC has a decisive influence on whether and how attended stimulus is linked with actions.

Attention, learning, and the value of information.

Despite many studies on selective attention, fundamental questions remain about its nature and neural mechanisms. Here I draw from the animal and machine learning fields that describe attention as a mechanism for active learning and uncertainty reduction and explore the implications of this view for understanding visual attention and eye movement control. I propose that a closer integration of these different views has the potential greatly to expand our understanding of oculomotor control and our ability to use this system as a window into high level but poorly understood cognitive functions, including the capacity for curiosity and exploration and for inferring internal models of the external world.

Attention as a decision in information space

Decision formation and attention are two fundamental processes through which we select, respectively, appropriate actions or sources of information. Although both functions have been studied in the oculomotor system, we lack a unified view explaining both forms of selection. We review evidence showing that parietal neurons encoding saccade motor decisions also carry signals of attention (perceptual selection) that are independent of the metrics, modality and reward of an action. We propose that attention implements a specialized form of decision based on the utility of information. Thus, oculomotor control depends on two interacting but distinct processes: attentional decisions that assign value to sources of information and motor decisions that flexibly link the selected information with action.