Comparison of Decision-Related Signals in Sensory and Motor Preparatory Responses of Neurons in Area LIP.

Neurons in the lateral intraparietal (LIP) area of Macaques exhibit both sensory and oculomotor preparatory responses. During perceptual decision making, the preparatory responses have been shown to track the state of the evolving evidence leading to the decision. The sensory responses are known to reflect categorical properties of visual stimuli, but it is not known whether these responses also track evolving evidence. We recorded neural responses from lateral intraparietal area of 2 female rhesus monkeys during a direction discrimination task. We compared sensory and oculomotor-preparatory responses in the same neurons when either the discriminandum (random dot motion) or an eye movement choice-target was in the neuron's response field. The neural responses in both configurations reflected the strength and direction of motion and were correlated with the animal's choice, albeit more prominently when the choice-target was in the response field. However, the variance and autocorrelation pattern of only the motor preparatory responses reflected the process of evidence accumulation. Simulations suggest that the task related activity of sensory responses could be inherited through lateral interactions with neurons that are carrying evidence accumulation signals in their motor-preparatory responses. The results are consistent with the proposal that evolving decision processes are supported by persistent neural activity in the service of actions or intentions, as opposed to high-order representations of stimulus properties.SIGNIFICANCE STATEMENT Perceptual decision making is the process of choosing an appropriate motor action based on perceived sensory information. Association areas of the cortex play an important role in this sensory-motor transformation. The neurons in these areas show both sensory- and motor-related activity. We show here that, in the macaque parietal association area LIP, signatures of the process of evidence accumulation that underlies the decisions are predominantly reflected in the motor-related activity. This finding supports the proposal that perceptual decision making is implemented in the brain as a process of choosing between available motor actions rather than as a process of representing the properties of the sensory stimulus.

Truncation of the flash-lag effect by a fixed spatial landmark.

The flash-lag effect is a visual illusion where a moving image is perceived to be advanced in its spatial location relative to a flashed image. Multiple studies have shown that the flash-lag effect can be enhanced by increasing the uncertainty of the moving and/or flashed images. However, little is known about the effect of task-irrelevant visual objects on the flash-lag effect. We were interested to see whether a task-irrelevant spatial landmark might reduce uncertainty and hence reduce the flash-lag effect. We placed a fixed bar between moving and flashed bars while measuring the flash-lag effect in six participants. For most participants, the fixed bar substantially truncated the flash-lag effect. The effect was maximal when the fixed bar was aligned with the flashed bar and decreased when the fixed bar was positioned more peripherally. A second experiment with two participants used a smaller fixed bar; the smaller bar had less truncation effect in one participant, while the other participant showed similar truncation regardless of the fixed bar size. Our results support models that place the locus of the flash-lag effect in higher-order brain areas, e.g., the parietal lobe.

Robust quantification of orientation selectivity and direction selectivity.

Neurons in the visual cortex of all examined mammals exhibit orientation or direction tuning. New imaging techniques are allowing the circuit mechanisms underlying orientation and direction selectivity to be studied with clarity that was not possible a decade ago. However, these new techniques bring new challenges: robust quantitative measurements are needed to evaluate the findings from these studies, which can involve thousands of cells of varying response strength. Here we show that traditional measures of selectivity such as the orientation index (OI) and direction index (DI) are poorly suited for quantitative evaluation of orientation and direction tuning. We explore several alternative methods for quantifying tuning and for addressing a variety of questions that arise in studies on orientation- and direction-tuned cells and cell populations. We provide recommendations for which methods are best suited to which applications and we offer tips for avoiding potential pitfalls in applying these methods. Our goal is to supply a solid quantitative foundation for studies involving orientation and direction tuning.

Elapsed decision time affects the weighting of prior probability in a perceptual decision task.

Decisions are often based on a combination of new evidence with prior knowledge of the probable best choice. Optimal combination requires knowledge about the reliability of evidence, but in many realistic situations, this is unknown. Here we propose and test a novel theory: the brain exploits elapsed time during decision formation to combine sensory evidence with prior probability. Elapsed time is useful because (1) decisions that linger tend to arise from less reliable evidence, and (2) the expected accuracy at a given decision time depends on the reliability of the evidence gathered up to that point. These regularities allow the brain to combine prior information with sensory evidence by weighting the latter in accordance with reliability. To test this theory, we manipulated the prior probability of the rewarded choice while subjects performed a reaction-time discrimination of motion direction using a range of stimulus reliabilities that varied from trial to trial. The theory explains the effect of prior probability on choice and reaction time over a wide range of stimulus strengths. We found that prior probability was incorporated into the decision process as a dynamic bias signal that increases as a function of decision time. This bias signal depends on the speed-accuracy setting of human subjects, and it is reflected in the firing rates of neurons in the lateral intraparietal area (LIP) of rhesus monkeys performing this task.

Experience with moving visual stimuli drives the early development of cortical direction selectivity.

The onset of vision occurs when neural circuits in the visual cortex are immature, lacking both the full complement of connections and the response selectivity that defines functional maturity. Direction-selective responses are particularly vulnerable to the effects of early visual deprivation, but it remains unclear how stimulus-driven neural activity guides the emergence of cortical direction selectivity. Here we report observations from a motion training protocol that allowed us to monitor the impact of experience on the development of direction-selective responses in visually naive ferrets. Using intrinsic signal imaging techniques, we found that training with a single axis of motion induced the rapid emergence of direction columns that were confined to cortical regions preferentially activated by the training stimulus. Using two-photon calcium imaging techniques, we found that single neurons in visually naive animals exhibited weak directional biases and lacked the strong local coherence in the spatial organization of direction preference that was evident in mature animals. Training with a moving stimulus, but not with a flashed stimulus, strengthened the direction-selective responses of individual neurons and preferentially reversed the direction biases of neurons that deviated from their neighbours. Both effects contributed to an increase in local coherence. We conclude that early experience with moving visual stimuli drives the rapid emergence of direction-selective responses in the visual cortex.

A role for neural integrators in perceptual decision making.

Decisions based on uncertain information may benefit from an accumulation of information over time. We asked whether such an accumulation process may underlie decisions about the direction of motion in a random dot kinetogram. To address this question we developed a computational model of the decision process using ensembles of neurons whose spiking activity mimics neurons recorded in the extrastriate visual cortex (area MT or V5) and a sensorimotor association area of the parietal lobe (area LIP). The model instantiates the hypothesis that neurons in sensorimotor association areas compute the time integral of sensory signals from the visual cortex, construed as evidence for or against a proposition, and that the decision is made when the integrated evidence reaches a threshold. The model explains a variety of behavioral and physiological measurements obtained from monkeys.

Microstimulation of visual cortex affects the speed of perceptual decisions.

Direction-selective neurons in the middle temporal visual area (MT) are crucially involved in motion perception, although it is not known exactly how the activity of these neurons is interpreted by the rest of the brain. Here we report that in a two-alternative task, the activity of MT neurons is interpreted as evidence for one direction and against the other. We measured the speed and accuracy of decisions as rhesus monkeys performed a direction-discrimination task. On half of the trials, we stimulated direction-selective neurons in area MT, thereby causing the monkeys to choose the neurons' preferred direction more often. Microstimulation quickened decisions in favor of the preferred direction and slowed decisions in favor of the opposite direction. Even on trials in which microstimulation did not induce a preferred direction choice, it still affected response times. Our findings suggest that during the formation of a decision, sensory evidence for competing propositions is compared and accumulates to a decision-making threshold.