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Shadlen, M. N.

Publications and source records attributed to Shadlen, M. N..

28 records · Page 2Linked to original sources

Sequential sampling from memory underlies action selection during abstract decision making

The study of perceptual decision making in monkeys has provided insights into the process by which sensory evidence is integrated towards a decision. When monkeys make decisions with the knowledge of the motor actions the decisions bear upon, the process of evidence integration is instantiated by neurons involved in the selection of said actions. It is less clear how monkeys make decisions when unaware of the actions required to communicate their choice--what we refer to as abstract decisions. We investigated this by training monkeys to associate the direction of motion of a noisy random-dot display with the color of two targets. Crucially, the targets were displayed at unpredictable locations after the motion stimulus was extinguished. We found that monkeys postponed decision formation until the targets were revealed. Neurons in the parietal association area LIP represented the integration of evidence leading to a choice, but as the stimulus was no longer visible, the samples of evidence must have been retrieved from short-term memory. Our results imply that when decisions are temporally unyoked from the motor actions they bear upon, decision formation is protracted until they can be framed in terms of motor actions.

neuroscience↗

Multiple decisions about one object involve parallel sensory acquisition but time-multiplexed evidence incorporation

The brain is capable of processing several streams of information that bear on different aspects of the same problem. Here we address the problem of making two decisions about one object, by studying difficult perceptual decisions about the color and motion of a dynamic random dot display. We find that the accuracy of one decision is unaffected by the difficulty of the other decision. However, the response times reveal that the two decisions do not form simultaneously. We show that both stimulus dimensions are acquired in parallel for the initial ~0.1 s but are then incorporated serially in time-multiplexed bouts. Thus there is a bottleneck that precludes updating more than one decision at a time, and a buffer that stores samples of evidence while access to the decision is blocked. We suggest that this bottleneck is responsible for the long timescales of many cognitive operations framed as decisions.

neuroscience↗

Differentiating between integration and non-integration strategies in perceptual decision making

Many tasks used to study decision-making encourage subjects to integrate evidence over time. Such tasks are useful to understand how the brain operates on multiple samples of information over prolonged timescales, but only if subjects actually integrate evidence to form their decisions. We explored the behavioral observations that corroborate evidence-integration in a number of task-designs. Several commonly accepted signs of integration were also predicted by non-integration strategies. Furthermore, an integration model could fit data generated by non-integration models. We identified the features of non-integration models that allowed them to mimic integration and used these insights to design a motion discrimination task that disentangled the models. In human subjects performing the task, we falsified a non-integration strategy in each and confirmed prolonged integration in all but one subject. The findings illustrate the difficulty of identifying a decision-makers strategy and support solutions to achieve this goal.

neuroscience↗

Context-dependent decision making in a premotor circuit

Cognitive capacities afford contingent associations between sensory information and behavioral responses. We studied this problem using an olfactory delayed match to sample task whereby a sample odor specifies the association between a subsequent test odor and rewarding action. Multi-neuron recordings revealed representations of the sample and test odors in olfactory sensory and association cortex, which were sufficient to identify the test odor as match/non-match. Yet, inactivation of a downstream premotor area (ALM), but not orbitofrontal cortex, confined to the epoch preceding the test odor, led to gross impairment. Olfactory decisions that were not context dependent were unimpaired. Therefore, ALM may not receive the outcome of a match/non-match decision from upstream areas but contextual information--the identity of the sample--to establish the mapping between test odor and action. A novel population of pyramidal neurons in ALM layer 2 may mediate this process.

neuroscience↗

Delay activity dynamics: task dependent time encoding and low dimensional trajectories

Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding we analyze neural activity recorded during delays in four experiments on non-human primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data, and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low dimensional. These constraints rule out working memory models that rely on constant, sustained activity, and neural networks with high dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time encoding properties and the dimensionality observed in the data.

neuroscience↗

Focal optogenetic suppression in macaque area MT biases direction discrimination and choice confidence, but only transiently

Insights from causal manipulations of brain activity depend on targeting the spatial and temporal scale most relevant for behavior. Using a sensitive perceptual decision task in monkeys, we examined the effects of randomly-interleaved, rapid, reversible inactivation on a spatial scale previously achieved only with electrical microstimulation. Inactivating neurons in area MT with consistent direction tuning produced systematic effects on choice and confidence. Behavioral effects were attenuated over the course of each session, suggesting compensatory adjustments in the downstream readout of MT over tens of minutes. Compensation also occurred on a sub-second time scale: behavior was largely unaffected on trials with visual stimuli (and concurrent suppression) longer than [~]350ms. These trends were similar for choice and confidence, consistent with the idea of a common mechanism underlying both measures. The findings demonstrate the utility of hyperpolarizing opsins for linking neural population activity at fine spatial and temporal scales to cognitive functions in primates.

neuroscience↗

Value-based decisions involve sequential sampling from memory

Deciding between two equally appealing options can take considerable time. This observation has puzzled economists and philosophers, because more deliberation only delays the reward. Here we show that this seemingly irrational behavior is explained by the constructive use of memory. Using functional brain imaging in humans, we show that how long it takes to decide between two familiar food items is related to activity in the hippocampus, within specific regions shown to be associated with the retrieval of long-term memories. Moreover, we show that value is partially constructed during deliberation to resolve preference, and this constructive process changes behavior and brain responses. These results render memory as a supplier of evidence in value-based decisions, resolving a central paradox of choice.

animal behavior and cognition↗

Counterfactual reasoning underlies the learning of priors in decision making

Accurate decisions require knowledge of prior probabilities (e.g., prevalence or base rate) but it is unclear how prior probability is learned in the absence of a teacher. We hypothesized that humans could learn base rates from experience making decisions, even without feedback. Participants made difficult decisions about the direction of dynamic random dot motion. For each block of 15-42 trials, the base rate favored left or right by a different amount. Participants were not informed of the base rate, yet they gradually biased their choices and thereby increased accuracy and confidence in their decisions. They achieved this by updating knowledge of base rate after each decision, using a counterfactual representation of confidence that simulates a neutral prior. The strategy is consistent with Bayesian updating of belief and suggests that humans represent both true confidence, that incorporates the evolving belief of the prior, and counterfactual confidence that discounts the prior.

neuroscience↗

Comparison of decision-related signals in sensory and motor preparatory responses of neurons in Area LIP

Neurons in the lateral intraparietal area (LIP) 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 if these responses also track evolving evidence. We compared sensory and oculomotor-preparatory responses in the same neurons during a direction discrimination task when either the discriminandum (random dot motion) or an eye movement choice-target was in the neurons response field. Both configurations elicited task related activity, but only the motor preparatory responses reflected evidence accumulation. 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.\n\nSIGNIFICANCE STATEMENTPerceptual 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.

neuroscience↗

Cause for pause before leaping to conclusions about stepping

Many neurons in parietal and prefrontal association cortex undergo gradual changes in firing rate during the formation of some perceptual decisions. These dynamics are often ramp-like increases or decreases depending on the sign and strength of the sensory evidence and are thus hypothesized to represent the accumulation of noisy samples of evidence, analogous to biased diffusion. This idea was challenged recently. An analysis of sequences of action potentials recorded from neurons in the lateral intraparietal cortex (area LIP) suggests that the spikes on single trials are explained by rates that undergo a discrete step from an intermediate rate to either a low or high rate at a random time during deliberation. The average of such steps, like the average of biased diffusion, is consistent with the ramp-like firing rates observed in LIP, but a Bayesian model comparison deemed stepping superior. Here we show that a shortcoming in the mathematical depiction of drift-diffusion led to a severe bias in the model comparison. We conclude that at present there is no compelling evidence that favors the stepping account.

neuroscience↗