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Carl R Olson

Publications and source records attributed to Carl R Olson.

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Impact of experience on the representation of object-centered space in the macaque supplementary eye field.

Many neurons in the macaque supplementary eye field (SEF) exhibit object-centered spatial selectivity, firing at different rates when the monkey plans a saccade to the left or right end of a horizontal bar. Is this property natural to the SEF or is it a product of specialized training in the laboratory? To answer this question, we monitored the activity of single SEF neurons in two monkeys before and after training to select eye-movement targets by an object-centered rule. During stage 1, the monkeys performed a color delayed-match-to-sample (DMS) task in which a red or green central cue dictated an eye movement to the matching end of a horizontal bar. Many neurons at this stage exhibited object-centered spatial selectivity. During stage 2, the monkeys performed a color-conditional object-centered task in which a green or red central cue instructed an eye movement to the left or right end of a gray bar. More neurons exhibited object-centered spatial selectivity during this stage than during stage 1. During stage 3, the monkeys again performed the color DMS task. The fraction of neurons exhibiting object-centered spatial selectivity remained at a level comparable to that observed during stage 2 and above that observed during stage 1. Thus object-centered spatial selectivity was present before training on an object-centered rule, was enhanced as a product of object-centered training, and outlasted active use of an object-centered rule. We conclude that neural representations of object-centered space, naturally present in the primate brain, can be sharpened by training.

Action Potentials↗

Neuronal activity in primate orbitofrontal cortex reflects the value of time.

Neurons in monkey orbitofrontal cortex (OF) are known to respond to reward-predicting cues with a strength that depends on the value of the predicted reward as determined 1) by intrinsic attributes including size and quality and 2) by extrinsic factors including the monkey's state of satiation and awareness of what other rewards are currently available. We pose here the question whether another extrinsic factor critical to determining reward value-the delay expected to elapse before delivery-influences neuronal activity in OF. To answer this question, we recorded from OF neurons while monkeys performed a memory-guided saccade task in which a cue presented early in each trial predicted whether the delay before the monkey could respond and receive a reward of fixed size would be short or long. OF neurons tended to fire more strongly in response to a cue predicting a short delay. The tendency to fire more strongly in anticipation of a short delay was correlated across neurons with the tendency to fire more strongly before a large reward. We conclude that neuronal activity in OF represents the time-discounted value of the expected reward.

Action Potentials↗

Competitive dynamics in cortical responses to visual stimuli.

Neurons in the visual cortex of the macaque monkey exhibit a variety of competitive behaviors, including normalization and oscillation, when presented with multiple visual stimuli. Here we argue that a biophysically plausible cortical circuit with opponent inhibition, spike-frequency adaptation, and synaptic depression can account for the full range of behaviors. The governing parameter is the strength of inhibition between competing neuronal pools. As the strength of inhibition is increased, the pattern of network behavior shifts from normalization mode to oscillatory mode, with oscillations occurring at progressively lower frequency until, at the extreme, winner-take-all behavior appears.

Action Potentials↗

Low-frequency oscillations arising from competitive interactions between visual stimuli in macaque inferotemporal cortex.

Some neurons in the inferotemporal cortex (IT) of the macaque monkey respond to visual stimuli by firing action potentials in a series of sharply defined bursts at a frequency of about 5 Hz. The aim of the present study was to test the hypothesis that the oscillatory responses of these neurons depend on competitive interactions with other neurons selective for different stimuli. To test this hypothesis, we monitored responses to probe images displayed in the presence of other already visible backdrop images. Two stimuli were used in testing each neuron: a foveal image that, when displayed alone, elicited an excitatory response (the "object") and a peripheral image that, when displayed alone, elicited little or no activity (the "flanker"). We assessed the results of presenting these images separately and together in monkeys trained to maintain central fixation. Two novel phenomena emerged. First, displaying the object in the presence of the flanker enhanced the strength of the oscillatory component of the response to the object. This effect varied in strength across task contexts and may have depended on the monkey's allocating attention to the flanker. Second, displaying the flanker in the presence of the object gave rise to sometimes strong oscillations in which the initial phase was negative. This was all the more striking because the flanker by itself elicited little or no response. This effect was robust and invariant across task contexts. These results can be accounted for by competition between two neuronal populations, one selective for the object and the other for the flanker, if it is assumed that the visual responses of each population are subject to fatigue.

Action Potentials↗

Neuronal activity dependent on anticipated and elapsed delay in macaque prefrontal cortex, frontal and supplementary eye fields, and premotor cortex.

In macaque monkeys performing a memory-guided saccade task for a reward of variable size, neuronal activity in several areas of frontal cortex is stronger when the monkey anticipates a larger reward. This effect might depend on either the size or the value of the reward. To distinguish between these possibilities, we recorded from neurons in frontal cortex while controlling value through a manipulation of time rather than amount. A cue presented at the beginning of each trial, predicted the length of the delay during which the monkey would have to maintain fixation before performing a saccade and receiving a reward of fixed size. Predicting a short delay had effects closely similar to those of predicting a large reward: 1) monkeys were more motivated when working for a reward at short delay, 2) neurons tended to fire more strongly before a short delay, 3) individual neurons firing more strongly before a short delay tended also to fire more strongly before a large reward, and 4) the tendency to fire more strongly before a short delay was far more pronounced in premotor areas caudal to the arcuate sulcus than in association areas rostral to it. The association areas, in contrast, were marked by a tendency for neurons to fire more strongly at the end of the long delay. We conclude that predicting a short delay, like predicting a large reward, induces an enhancement of neuronal activity related to motivational modulation of the monkey's preparatory state.

Animals↗

Neuronal activity in macaque SEF and ACC during performance of tasks involving conflict.

It has been suggested on the basis of previous studies involving functional MRI (fMRI) and single-neuron recording that neurons of the supplementary eye field (SEF) and anterior cingulate cortex (ACC) monitor conflict. To test this idea, we carried out microelectrode recording in monkeys performing a color-conditional eye movement task in which red and green cues instructed leftward and rightward saccades, respectively. In a variant inducing conflict by spatial incompatibility, the cue was presented either at the location of the target (no conflict) or opposite the location of the target (conflict). In a variant inducing conflict by reversal, the foveal cue either remained one color (no conflict) or reversed color after 100 ms (conflict), with the monkey required to follow the instruction conveyed by the second color. In both tasks, conflict was evident in behavioral measures (reduced percent correct and slowed reaction time) and in physiological measures (reduced strength of directional activity among direction-selective neurons). In the SEF, there was a tendency for neurons to fire more strongly on trials involving conflict, but this effect took the form of modulation of task-related activity among direction-selective neurons, not of a pure conflict-monitoring signal. In the ACC, there was no conflict-related enhancement. These results are incompatible with the idea that the SEF and ACC contain populations of neurons specialized for monitoring conflict.

Action Potentials↗

Neuronal activity related to reward value and motivation in primate frontal cortex.

In several areas of the macaque brain, neurons fire during delayed-response tasks at a rate determined by the value of the reward expected at the end of the trial. 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. We describe results indicating that the nature of reward-dependent activity varies across areas. Neuronal activity in orbitofrontal cortex represents the value of the expected reward, whereas neuronal activity in premotor cortex reflects the degree of motivation.

Action Potentials↗

Role of attention and perceptual grouping in visual statistical learning.

Statistical learning has been widely proposed as a mechanism by which observers learn to decompose complex sensory scenes. To determine how robust statistical learning is, we investigated the impact of attention and perceptual grouping on statistical learning of visual shapes. Observers were presented with stimuli containing two shapes that were either connected by a bar or unconnected. When observers were required to attend to both locations at which shapes were presented, the degree of statistical learning was unaffected by whether the shapes were connected or not. However, when observers were required to attend to just one of the shapes' locations, statistical learning was observed only when the shapes were connected. These results demonstrate that visual statistical learning is not just a passive process. It can be modulated by both attention and connectedness, and in natural scenes these factors may constrain the role of stimulus statistics in learning.

Attention↗

Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex.

In several regions of the macaque brain, neurons fire during delayed response tasks at a rate determined by the value of the reward expected at the end of the trial. The activity of these neurons might be related either to the internal representation of the appetitive value of the expected reward or to motivation-dependent variations in the monkey's level of motor preparation or motor output. According to the first interpretation, reward-related activity should be most prominent in areas affiliated with the limbic system. According to the second interpretation, it should be most prominent in areas affiliated with the motor system. To distinguish between these alternatives, we carried out single-neuron recording while monkeys performed a memory-guided saccade task in which a visual cue presented early in each trial indicated whether the reward would be large or small. Neuronal activity accompanying task performance was monitored in the dorsolateral prefrontal cortex (PFC), the frontal eye field (FEF), a transitional zone caudal to the frontal eye field (FEF/PM), premotor cortex (PM), the supplementary eye field (SEF), and the rostral part of the supplementary motor area (SMAr). The tendency for neuronal activity to increase after cues that predicted a large reward became progressively stronger in progressively more posterior areas both in the lateral sector of the frontal lobe (PFC < FEF < FEF/PM < PM) and in the medial sector (SEF < SMAr). The very strong reward-related activity of premotor neurons was presumably attributable to the monkey's motivation-dependent level of motor preparation or motor output. This finding points to the need to determine whether reward-related activity in other nonlimbic brain areas, including dorsolateral prefrontal cortex and the dorsal striatum, genuinely represents the value of the expected reward or, alternatively, is related to motivational modulation of motor signals.

Action Potentials↗

Brain representation of object-centered space in monkeys and humans.

Visuospatial cognition requires taking into account where things are relative to each other and not just relative to the viewer. Consequently it would make sense for the brain to form an explicit representation of object-centered and not just of ego-centered space. Evidence bearing on the presence and nature of neural maps of object-centered space has come from two sources: single-neuron recording in behaving monkeys and assessment of the visual abilities of human patients with hemispatial neglect. Studies of the supplementary eye field of the monkey have revealed that it contains neurons with object-centered spatial selectivity. These neurons fire when the monkey has selected, as target for an eye movement or attention, a particular location defined relative to a reference object. Studies of neglect have revealed that in some patients the condition is expressed with respect to an object-centered and object-aligned reference frame. These patients neglect one side of an object, as defined relative to its intrinsic midline, regardless of its location and orientation relative to the viewer. The two sets of observations are complementary in the sense that the loss of neurons, such as observed in the monkey, could explain the spatial distribution of neglect in these patients.

Animals↗

Neuronal activity related to rule and conflict in macaque supplementary eye field.

Neuronal activity in macaque supplementary eye field (SEF) is enhanced during performance of the antisaccade task. This could be related to the selection of targets by a difficult rule (move to a location diametrically opposite the cue) or to conflict between the automatic tendency to look at the cue and the voluntary intention to look away. To distinguish between rule- and conflict-based mechanisms of enhancement, we monitored neuronal activity in the SEF during performance of a delayed response task in which monkeys selected saccade targets in response to peripheral visual cues. In spatial trials, the monkey had to select as target the location marked by the cue. In color trials, the monkey had to select as target the location associated with the color of the cue. 'Color-congruent' trials resembled spatial trials in that saccades were directed to the location occupied by the cue. Nevertheless, many SEF neurons were sensitive to the rule being used, with the majority firing more strongly under the color-rule condition. 'Color-incongruent' trials resembled 'color-congruent' trials in that a color rule guided target selection. Nevertheless, many SEF neurons were sensitive to the spatial relation between cue and saccade, with the majority firing more strongly on trials in which they were incongruent. We conclude that neuronal activity in the SEF is enhanced in connection both with the use of a more difficult rule and with conflict.

Animals↗

Impact of learning on representation of parts and wholes in monkey inferotemporal cortex.

Here we investigated the impact of visual discrimination training on neuronal responses to parts of images and to whole images in inferotemporal (IT) cortex. Monkeys were trained to discriminate among 'baton' stimuli consisting of discrete top and bottom parts joined by a vertical stem. With separate features at each end, we were able to manipulate the two parts of each baton independently. After training the monkeys, we used single-cell recording to compare neuronal responses to learned and unlearned batons. Responses to learned batons, though not enhanced in strength, were enhanced in selectivity for both individual parts and for whole batons. Whole-baton selectivity arose from a form of conjunctive encoding whereby two parts together exerted a greater influence on neuronal activity than predicted by the additive influence of each part considered individually. These results indicate a possible neural mechanism for holistic or configural effects in expert versus novice observers.

Animals↗

Statistical analysis of temporal evolution in single-neuron firing rates.

A fundamental methodology in neurophysiology involves recording the electrical signals associated with individual neurons within brains of awake behaving animals. Traditional statistical analyses have relied mainly on mean firing rates over some epoch (often several hundred milliseconds) that are compared across experimental conditions by analysis of variance. Often, however, the time course of the neuronal firing patterns is of interest, and a more refined procedure can produce substantial additional information. In this paper we compare neuronal firing in the supplementary eye field of a macaque monkey across two experimental conditions. We take the electrical discharges, or 'spikes', to be arrivals in a inhomogeneous Poisson process and then model the firing intensity function using both a simple parametric form and more flexible splines. Our main interest is in making inferences about certain characteristics of the intensity, including the timing of the maximal firing rate. We examine data from 84 neurons individually and also combine results into a hierarchical model. We use Bayesian estimation methods and frequentist significance tests based on a nonparametric bootstrap procedure. We are thereby able to conclude that a substantial fraction of the neurons exhibit important temporal differences in firing intensity across the two conditions, and we quantify the effect across the population of neurons.

Journal Article↗

Neurons with object-centered spatial selectivity in macaque SEF: do they represent locations or rules?

In macaque monkeys performing a task that requires eye movements to the leftmost or rightmost of two dots in a horizontal array, some neurons in the supplementary eye field (SEF) fire differentially according to which side of the array is the target regardless of the array's location on the screen. We refer to these neurons as exhibiting selectivity for object-centered location. This form of selectivity might arise from involvement of the neurons in either of two processes: representing the locations of targets or representing the rules by which targets are selected. To distinguish between these possibilities, we monitored neuronal activity in the SEF of two monkeys performing a task that required the selection of targets by either an object-centered spatial rule or a color rule. On each trial, a sample array consisting of two side-by-side dots appeared; then a cue flashed on one dot; then the display vanished and a delay ensued. Next a target array consisting of two side-by-side dots appeared at an unpredictable location and another delay ensued; finally the monkey had to make an eye movement to one of the target dots. On some trials, the monkey had to select the dot on the same side as the cue (right or left). On other trials, he had to select the target of the same color as the cue (red or green). Neuronal activity robustly encoded the object-centered locations first of the cue and then of the target regardless of the whether the monkey was following a rule based on object-centered location or color. Neuronal activity was at most weakly affected by the type of rule the monkey was following (object-centered-location or color) or by the color of the cue and target (red or green). On trials involving a color rule, neuronal activity was moderately enhanced when the cue and target appeared on opposite sides of their respective arrays. We conclude that the general function of SEF neurons selective for object-centered location is to represent where the cue and target are in their respective arrays rather than to represent the rule for target selection.

Animals↗