Neurons of Macaque Frontal Eye Field Signal Reward-Related Surprise.

The frontal eye field (FEF) plays a well-established role in the control of visual attention. The strength of an FEF neuron's response to a visual stimulus presented in its receptive field is enhanced if the stimulus captures spatial attention by virtue of its salience. A stimulus can be rendered salient by cognitive factors as well as by physical attributes.

Independent repetition suppression in macaque area V2 and inferotemporal cortex.

When a complexly structured natural image is presented twice in succession, first as adapter and then as test, neurons in area TE of macaque inferotemporal cortex exhibit repetition suppression, responding less strongly to the second presentation than to the first. This phenomenon, which has been studied primarily in TE, might plausibly be argued to arise in TE because TE neurons respond selectively to complex images and thus carry information adequate for determining whether an image is or is not a repeat. However, the idea has never been put to a direct test.

Contribution of individual features to repetition suppression in macaque inferotemporal cortex.

When an image is presented twice in succession, neurons in area TE of macaque inferotemporal cortex exhibit repetition suppression, responding less strongly to the second presentation than to the first. Suppression is known to occur if the adapter and the test image are subtly different from each other. However, it is not known whether cross suppression occurs between images that are radically different from each other but that share a subset of features.

Neural Correlate of Visual Familiarity in Macaque Area V2.

Neurons in macaque inferotemporal cortex (ITC) respond less strongly to familiar than to novel images. It is commonly assumed that this effect arises within ITC because its neurons respond selectively to complex images and thus encode in an explicit form information sufficient for identifying a particular image as familiar. However, no prior study has examined whether neurons in low-order visual areas selective for local features also exhibit familiarity suppression.

Prediction suppression and surprise enhancement in monkey inferotemporal cortex.

Exposing monkeys, over the course of days and weeks, to pairs of images presented in fixed sequence, so that each leading image becomes a predictor for the corresponding trailing image, affects neuronal visual responsiveness in area TE. At the end of the training period, neurons respond relatively weakly to a trailing image when it appears in a trained sequence and, thus, confirms prediction, whereas they respond relatively strongly to the same image when it appears in an untrained sequence and, thus, violates prediction. This effect could arise from prediction suppression (reduced firing in response to the occurrence of a probable event) or surprise enhancement (elevated firing in response to the omission of a probable event).

In monkeys making value-based decisions, amygdala neurons are sensitive to cue value as distinct from cue salience.

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.

Prediction suppression in monkey inferotemporal cortex depends on the conditional probability between images.

When monkeys view two images in fixed sequence repeatedly over days and weeks, neurons in area TE of the inferotemporal cortex come to exhibit prediction suppression. The trailing image elicits only a weak response when presented following the leading image that preceded it during training. Induction of prediction suppression might depend either on the contiguity of the images, as determined by their co-occurrence and captured in the measure of joint probability P(A,B), or on their contingency, as determined by their correlation and as captured in the measures of conditional probability P(A|B) and P(B|A).

Macaque monkeys experience visual crowding.

In peripheral vision, objects that are easily discriminated on their own become less discriminable in the presence of surrounding clutter. This phenomenon is known as crowding.The neural mechanisms underlying crowding are not well understood.

Image familiarization sharpens response dynamics of neurons in inferotemporal cortex.

Repeated viewing of an image over days and weeks induces a marked reduction in the strength with which neurons in monkey inferotemporal cortex respond to it. The processing advantage that attaches to this reduction is unknown. One possibility is that truncation of the response to a familiar image leaves neurons in a state of readiness to respond to ensuing images and thereby enhances their ability to track rapidly changing displays.

Statistical learning of serial visual transitions by neurons in monkey inferotemporal cortex.

If monkeys repeatedly, over the course of weeks, view displays in which two images appear in fixed sequence, then neurons of inferotemporal cortex (ITC) come to exhibit prediction suppression. The response to the trailing image is weaker if it follows the leading image with which it was paired during training than if it follows some other leading image. Prediction suppression is a plausible neural mechanism for statistical learning of visual transitions such as has been demonstrated in behavioral studies of human infants and adults.

Intracortical microstimulation of supplementary eye field impairs ability of monkeys to make serially ordered saccades.

Neurons in the supplementary eye field (SEF) of the macaque monkey exhibit rank selectivity, firing differentially as a function of the phase attained during the performance of a task requiring the execution of saccades to a series of objects in fixed order. The activity of these neurons is commonly thought to represent ordinal position in the service of serial-order performance. However, there is little evidence causally linking neuronal activity in the SEF to sequential behavior.

Response to comment on "In monkeys making value-based decisions, LIP neurons encode cue salience and not action value".

Newsome et al. question neither our key result, that large-penalty cues elicited stronger responses than small-penalty cues, nor our key conclusion, that neurons early in the trial signaled cue salience and not action value. Instead, they focus on subsequent neuronal activity.

In monkeys making value-based decisions, LIP neurons encode cue salience and not action value.

In monkeys deciding between alternative saccadic eye movements, lateral intraparietal (LIP) neurons representing each saccade fire at a rate proportional to the value of the reward expected upon its completion. This observation has been interpreted as indicating that LIP neurons encode saccadic value and that they mediate value-based decisions between saccades. Here, we show that LIP neurons representing a given saccade fire strongly not only if it will yield a large reward but also if it will incur a large penalty.

Statistical learning of visual transitions in monkey inferotemporal cortex.

One of the most fundamental functions of the brain is to predict upcoming events on the basis of the recent past. A closely related function is to signal when a prediction has been violated. The identity of the brain regions that mediate these functions is not known.

Bayesian nonparametric analysis of neuronal intensity rates.

We propose a flexible hierarchical Bayesian nonparametric modeling approach to compare the spiking patterns of neurons recorded under multiple experimental conditions. In particular, we showcase the application of our statistical methodology using neurons recorded from the supplementary eye field region of the brains of two macaque monkeys trained to make delayed eye movements to three different types of targets. The proposed Bayesian methodology can be used to perform either a global analysis, allowing for the construction of posterior comparative intervals over the entire experimental time window, or a pointwise analysis for comparing the spiking patterns locally, in a predetermined portion of the experimental time window.

Relation of ordinal position signals to the expectation of reward and passage of time in four areas of the macaque frontal cortex.

Neurons in several areas of the monkey frontal cortex exhibit rank selectivity, firing differentially as a function of the stage attained during the performance of a serial order task. The activity of these neurons is commonly thought to represent ordinal position within the trial. However, they might also be sensitive to factors correlated with ordinal position including time elapsed during the trial (which is greater for each successive stage) and the degree of anticipation of reward (which probably increases at each successive stage).

Responses to compound objects in monkey inferotemporal cortex: the whole is equal to the sum of the discrete parts.

It is commonly thought that neurons in monkey inferotemporal cortex are conjunction selective--that a neuron will respond to an image if and only if it contains a required combination of parts. However, this view is based on the results of experiments manipulating closely adjacent or confluent parts. Neurons may have been sensitive not to the conjunction of parts as such but to the presence of a unique feature created where they abut.

Rank signals in four areas of macaque frontal cortex during selection of actions and objects in serial order.

Neurons in several areas of monkey frontal cortex exhibit ordinal position (rank) selectivity during the performance of serial order tasks. It has been unclear whether rank selectivity or the dependence of rank selectivity on task context varies across the areas of frontal cortex. To resolve this issue, we recorded from neurons in the supplementary motor area (SMA), presupplementary motor area (pre-SMA), supplementary eye field (SEF), and dorsolateral prefrontal cortex (dlPFC) as monkeys performed two oculomotor tasks, one requiring the selection of three actions in sequence and the other requiring the selection of three objects in sequence.

Global image dissimilarity in macaque inferotemporal cortex predicts human visual search efficiency.

Finding a target in a visual scene can be easy or difficult depending on the nature of the distractors. Research in humans has suggested that search is more difficult the more similar the target and distractors are to each other. However, it has not yielded an objective definition of similarity.

Representing the forest before the trees: a global advantage effect in monkey inferotemporal cortex.

Hierarchical stimuli (large shapes composed of small shapes) have long been used to study how humans perceive the global and the local content of a scene--the forest and the trees. Studies using these stimuli have revealed a global advantage effect: humans consistently report global shape faster than local shape. The neuronal underpinnings of this effect remain unclear.

Monkey supplementary eye field neurons signal the ordinal position of both actions and objects.

When a monkey executes a learned series of eye movements (for example, rightward followed by upward followed by leftward), neurons in the supplementary eye field (SEF) fire differentially in conjunction with the first, second, and third movements. It has not been clear whether such ordinal position signals are truly general, accompanying all forms of sequential behavior, or accompany only learned sequences of movements. To resolve this issue, we trained monkeys to perform both a serial action task (making saccades in a fixed sequence of directions) and a serial object task (making saccades to a fixed sequence of objects).

Linearly additive shape and color signals in monkey inferotemporal cortex.

How does the brain represent a red circle? One possibility is that there is a specialized and possibly time-consuming process whereby the attributes of shape and color, carried by separate populations of neurons in low-order visual cortex, are bound together into a unitary neural representation. Another possibility is that neurons in high-order visual cortex are selective, by virtue of their bottom-up input from low-order visual areas, for particular conjunctions of shape and color. A third possibility is that they simply sum shape and color signals linearly.

Bayesian correction for attenuation of correlation in multi-trial spike count data.

When correlation is measured in the presence of noise, its value is decreased. In single-neuron recording experiments, for example, the correlation of selectivity indices in a pair of tasks may be assessed across neurons, but, because the number of trials is limited, the measured index values for each neuron will be noisy. This attenuates the correlation.

Neuronal activity related to anticipated reward in frontal cortex: does it represent value or reflect motivation?

It is thought that neuronal activity in orbitofrontal cortex (OFC) represents the value of anticipated reward; however activity in many other brain areas also seems to reflect expected reward value. For example, we have shown that in monkeys performing a memory-guided saccade task for a reward of variable size, activity in numerous areas of frontal cortex is stronger when the monkey anticipates a larger reward. The activity of these neurons might be related to the value of the expected reward or to the degree of motivation induced by expectation of the reward.

Testing equality of several functions: analysis of single-unit firing-rate curves across multiple experimental conditions.

We consider the problem of comparing noisy functions, here trial-averaged neuronal firing-rate curves, across multiple experimental conditions. Of interest are comparisons both within neurons and also among populations of individually recorded neurons. We propose likelihood ratio tests to perform comparisons either pointwise or globally over the entire experimental time.