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William T Newsome

Publications and source records attributed to William T Newsome.

15 recordsLinked to original sources

Local field potential in cortical area MT: stimulus tuning and behavioral correlations.

Low-frequency electrical signals like those that compose the local field potential (LFP) can be detected at substantial distances from their point of origin within the brain. It is thus unclear how useful the LFP might be for assessing local function, for example, on the spatial scale of cortical columns. We addressed this problem by comparing speed and direction tuning of LFPs obtained from middle temporal area MT with the tuning of multiunit (MU) activity recorded simultaneously. We found that the LFP can be well tuned for speed and direction and is highly correlated with that of MU activity, particularly for frequencies at and above the gamma band. LFP tuning is substantially poorer for lower frequencies, although tuning for direction extends to lower frequencies than does tuning for speed. Our data suggest that LFP signals at and above the gamma band reflect neural processing on the spatial scale of cortical columns, within a few hundred micrometers of the electrode tip. Consistent with this notion, we also found that frequencies at and above the gamma band measured during a speed discrimination task exhibit an effect known as "choice probability," which reveals a particularly close relationship between neural activity and behavioral choices. In the LFP, this signature of the perceptual choice comprises a shift in relative power from low-frequency bands (alpha and beta) to the gamma band. It remains to be determined how LFP choice probability, which is a temporal signature, is related to conventional choice probability effects observed in spike rates.

Action Potentials↗

Cone signal interactions in direction-selective neurons in the middle temporal visual area (MT).

Many experimental measurements support the hypothesis that the middle temporal visual area (MT) of the rhesus monkey has a central role in processing visual motion. Most of these studies were performed using luminance stimuli, leaving open the question of how color information is used during motion processing. We investigated the specific question of how S-cone signals, an important source of color information, interact with L,M-cone signals, the dominant source of luminance information. In MT, S-cone-initiated signals combine synergistically with L,M-cone (luminance) signals over most of the stimulus range, regardless of whether the stimuli are added or subtracted. A quantitative analysis of the responses to the combination of S- and L,M-cone signals shows that for a significant minority of cells, these S-cone signals are carried to MT by a color-opponent ("blue-yellow") pathway, such that in certain limited contrast ranges, a small amount of S- and L,M-cone cancellation is observed. Both S- and L,M-cone responses are direction-selective, suggesting that MT processes a wide range of motion signals, including those carried by luminance and color. To investigate this possibility further, we measured MT responses while monkeys discriminated the direction of motion of luminance and S-cone-initiated gratings. The sensitivity of single MT neurons and the correlation between trial-to-trial variations in single neuron firing and perception are similar for S- and L,M-cone stimuli, further supporting a role for MT in processing chromatic motion.

Animals↗

Correlation between speed perception and neural activity in the middle temporal visual area.

We conducted electrophysiological recording and microstimulation experiments to test the hypothesis that the middle temporal visual area (MT) plays a direct role in perception of the speed of moving visual stimuli. We trained rhesus monkeys on a speed discrimination task in which monkeys chose the faster speed of two moving random dot patterns presented simultaneously in spatially segregated apertures. In electrophysiological experiments, we analyzed the activity of speed-tuned MT neurons and multiunit clusters during the discrimination task. Neural activity was correlated with the monkeys' behavioral choices on a trial-to-trial basis (choice probability), and the correlation was predicted by the speed-tuning properties of each unit. In microstimulation experiments, we activated clusters of MT neurons with homogeneous speed-tuning properties during the same speed discrimination task. In one monkey, microstimulation biased speed judgments toward the preferred speed of the stimulated neurons. Together, evidence from these two experiments suggests that MT neurons play a direct role in the perception of visual speed. Comparison of psychometric and neurometric thresholds revealed that single and multineuronal signals were, on average, considerably less sensitive than were the monkeys perceptually, suggesting that signals must be pooled across neurons to account for performance.

Action Potentials↗

A general mechanism for decision-making in the human brain?

A new fMRI study by Heekeren and colleagues suggests that left dorsolateral prefrontal cortex (DLPFC) contains a region that integrates sensory evidence supporting perceptual decisions. DLPFC meets two criteria posited by Heekeren et al. for such a region: (1) its activity is correlated in time with the output of sensory areas of the visual cortex measured simultaneously, and (2) as expected of an integrator, its activity is greater on trials for which the sensory evidence is substantial than on trials for which the sensory evidence is weak. Complementary experiments in humans and monkeys now offer a realistic hope of elucidating decision-making networks in the primate brain.

Animals↗

Choosing the greater of two goods: neural currencies for valuation and decision making.

To make adaptive decisions, animals must evaluate the costs and benefits of available options. The nascent field of neuroeconomics has set itself the ambitious goal of understanding the brain mechanisms that are responsible for these evaluative processes. A series of recent neurophysiological studies in monkeys has begun to address this challenge using novel methods to manipulate and measure an animal's internal valuation of competing alternatives. By emphasizing the behavioural mechanisms and neural signals that mediate decision making under conditions of uncertainty, these studies might lay the foundation for an emerging neurobiology of choice behaviour.

Animals↗

Linear-Nonlinear-Poisson models of primate choice dynamics.

The equilibrium phenomenon of matching behavior traditionally has been studied in stationary environments. Here we attempt to uncover the local mechanism of choice that gives rise to matching by studying behavior in a highly dynamic foraging environment. In our experiments, 2 rhesus monkeys (Macacca mulatta) foraged for juice rewards by making eye movements to one of two colored icons presented on a computer monitor, each rewarded on dynamic variable-interval schedules. Using a generalization of Wiener kernel analysis, we recover a compact mechanistic description of the impact of past reward on future choice in the form of a Linear-Nonlinear-Poisson model. We validate this model through rigorous predictive and generative testing. Compared to our earlier work with this same data set, this model proves to be a better description of choice behavior and is more tightly correlated with putative neural value signals. Refinements over previous models include hyperbolic (as opposed to exponential) temporal discounting of past rewards, and differential (as opposed to fractional) comparisons of option value. Through numerical simulation we find that within this class of strategies, the model parameters employed by animals are very close to those that maximize reward harvesting efficiency.

Animals↗

Microstimulation of the superior colliculus focuses attention without moving the eyes.

The superior colliculus (SC) is part of a network of brain areas that directs saccadic eye movements, overtly shifting both gaze and attention from position to position, in space. Here, we seek direct evidence that the SC also contributes to the control of covert spatial attention, a process that focuses attention on a region of space different from the point of gaze. While requiring monkeys to keep their gaze fixed, we tested whether microstimulation of a specific location in the SC spatial map would enhance visual performance at the corresponding region of space, a diagnostic measure of covert attention. We find that microstimulation improves performance in a spatially selective manner: thresholds decrease at the location in visual space represented by the stimulated SC site, but not at a control location in the opposite hemifield. Our data provide direct evidence that the SC contributes to the control of covert spatial attention.

Animals↗

Direction-selective visual responses in macaque superior colliculus induced by behavioral training.

In a previous report, we described a heretofore undetected population of neurons in the intermediate and deep layers of the monkey superior colliculus (SC) that yielded directionally selective visual responses to stimuli presented within the central 4 degrees of the visual field. We observed these neurons in three monkeys that had been extensively trained to perform a visual direction discrimination task in this region of the visual field. The task required the monkeys to report the perceived direction of motion by making a saccadic eye movement to one of two targets aligned with the two possible directions of motion. We hypothesized that these neurons reflect a learned association between visual motion direction and saccade direction formed through extensive training on the direction discrimination task. We tested this hypothesis by searching for direction-selective visual responses in two monkeys that had been trained to perform a similar motion discrimination task in which the direction of stimulus motion was dissociated from the direction of the operant saccade. Strongly directional visual responses were absent in these monkeys, consistent with the notion that extensive training can induce highly specific visual responses in a subpopulation of SC neurons.

Animals↗

Matching behavior and the representation of value in the parietal cortex.

Psychologists and economists have long appreciated the contribution of reward history and expectation to decision-making. Yet we know little about how specific histories of choice and reward lead to an internal representation of the "value" of possible actions. We approached this problem through an integrated application of behavioral, computational, and physiological techniques. Monkeys were placed in a dynamic foraging environment in which they had to track the changing values of alternative choices through time. In this context, the monkeys' foraging behavior provided a window into their subjective valuation. We found that a simple model based on reward history can duplicate this behavior and that neurons in the parietal cortex represent the relative value of competing actions predicted by this model.

Animals↗

Perceptual "read-out" of conjoined direction and disparity maps in extrastriate area MT.

Cortical neurons are frequently tuned to several stimulus dimensions, and many cortical areas contain intercalated maps of multiple variables. Relatively little is known about how information is "read out" of these multidimensional maps. For example, how does an organism extract information relevant to the task at hand from neurons that are also tuned to other, irrelevant stimulus dimensions? We addressed this question by employing microstimulation techniques to examine the contribution of disparity-tuned neurons in the middle temporal (MT) visual area to performance on a direction discrimination task. Most MT neurons are tuned to both binocular disparity and the direction of stimulus motion, and MT contains topographic maps of both parameters. We assessed the effect of microstimulation on direction judgments after first characterizing the disparity tuning of each stimulation site. Although the disparity of the stimulus was irrelevant to the required task, we found that microstimulation effects were strongly modulated by the disparity tuning of the stimulated neurons. For two of three monkeys, microstimulation of nondisparity-selective sites produced large biases in direction judgments, whereas stimulation of disparity-selective sites had little or no effect. The binocular disparity was optimized for each stimulation site, and our result could not be explained by variations in direction tuning, response strength, or any other tuning property that we examined. When microstimulation of a disparity-tuned site did affect direction judgments, the effects tended to be stronger at the preferred disparity of a stimulation site than at the nonpreferred disparity, indicating that monkeys can selectively monitor direction columns that are best tuned to an appropriate conjunction of parameters. We conclude that the contribution of neurons to behavior can depend strongly upon tuning to stimulus dimensions that appear to be irrelevant to the current task, and we suggest that these findings are best explained in terms of the strategy used by animals to perform the task.

Animals↗

Representation of an abstract perceptual decision in macaque superior colliculus.

We recorded from neurons in the intermediate and deep layers of the superior colliculus (SC) while monkeys performed a novel direction discrimination task. In contrast to the task we used previously, the new version required the monkey to dissociate perceptual judgments from preparation to execute specific operant saccades. The monkey discriminated between 2 opposed directions of motion in a random-dot motion stimulus and was required to maintain the decision in memory throughout a delay period before the target of the required operant saccade was revealed. We hypothesized that perceptual decisions made in this paradigm would be represented in an "abstract" or "categorical" form within the brain, probably in the frontal cortex, and that decision-related neural activity would be eliminated from spatially organized preoculomotor structures such as the SC. To our surprise, however, a small population of neurons in the intermediate and deep layers of the SC fired in a choice-specific manner early in the trial well before the monkey could plan the operant saccade. Furthermore, the representation of the decision during the delay period appeared to be spatial: the active region in the SC map corresponded to the region of space toward which the perceptually discriminated stimulus motion flowed. Electrical microstimulation experiments suggested that these decision-related SC signals were not merely related to covert saccade planning. We conclude that monkeys may employ, in part, a spatially referenced mnemonic strategy for representing perceptual decisions, even when an abstract, categorical representation might appear more likely a priori.

Algorithms↗

What electrical microstimulation has revealed about the neural basis of cognition.

Neurophysiologists have shown repeatedly that neural activity in different brain structures can be correlated with specific perceptual and cognitive functions, but the causal efficacy of the observed activity has generally been a matter of conjecture. By contrast, electrical microstimulation, which allows the experimenter to manipulate the activity of small groups of neurons with spatial and temporal precision, can now be used to demonstrate causal links between neural activity and specific cognitive functions. Here, we review this growing literature, including applications to the study of attention, visual and somatosensory perception, 'read-out' mechanisms for interpreting sensory maps, and contextual effects on perception. We also discuss potential applications of microstimulation to studies of higher cognitive functions such as decision-making and subjective experience.

Action Potentials↗

Functional organization of speed tuned neurons in visual area MT.

We analyzed the functional organization of speed tuned neurons in extrastriate visual area MT. We sought to determine whether neurons tuned for particular speeds are clustered spatially and whether such spatial clusters are elongated normal to the cortical surface so as to form speed columns. Our data showed that MT neurons are indeed clustered according to preferred speed. Multiunit recordings were speed tuned, and the speed tuning of these signals was well correlated with the speed tuning of single neurons recorded simultaneously. To determine whether speed columns exist in MT, we compared the rates at which preferred speed changed in electrode tracks that traversed MT obliquely and normally to the cortical surface. If speed columns exist, the preferred speed should change at a faster rate during oblique electrode tracks. We found, however, that preferred speed changed at similar rates for either type of penetration. In the same data set, the rate of change of preferred direction and preferred disparity differed substantially in normal and oblique penetrations as expected from the known columnar organization of MT. Thus our results suggest that a columnar organization for speed tuned neurons does not exist in MT.

Animals↗

Middle temporal visual area microstimulation influences veridical judgments of motion direction.

Microstimulation of direction columns in the middle temporal visual area (MT, or V5) provides a powerful tool for probing the relationship between cortical physiology and visual motion perception. In the current study we obtained "veridical" reports of perceived motion from rhesus monkeys by permitting a continuous range of possible responses that mapped isomorphically onto a continuous range of possible motion directions. In contrast to previous studies, therefore, the animals were freed from experimenter-imposed "categories" that typify forced choice tasks. We report three new findings: (1) MT neurons with widely disparate preferred directions can cooperate to shape direction estimates, inconsistent with a pure "winner-take-all" read-out algorithm and consistent with a distributed coding scheme like vector averaging, whereas neurons with nearly opposite preferred directions seem to compete in a manner consistent with the winner-take-all hypothesis, (2) microstimulation can influence direction estimates even when paired with the most powerful motion stimuli available, and (3) microstimulation effects can be elicited when a manual response (instead of our standard oculomotor response) is used to communicate the perceptual report.

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