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Ziemba, C. M.

Publications and source records attributed to Ziemba, C. M..

7 recordsLinked to original sources

Reassessing Choice Probability: What 59 Macaque Studies Tell Us About Decision-Related Activity in Visual Cortex

Choice probability (CP) quantifies the trial-by-trial covariation between a sensory neurons response and perceptual reports. Despite extensive interest in CP as a window into how perception is linked to the activity of sensory neurons, the usefulness of CP remains debated. On one hand, reported CP magnitudes vary widely across seemingly equivalent studies, questioning its utility as a metric. On the other hand, the absence of clear patterns in CP variability has made it difficult to use it to adjudicate between competing models of visual perception. Here, we performed a meta-analysis of 150 CP estimates from 59 macaque neurophysiology studies to identify factors that systematically influence CP. We confirmed the positive relationship between CP and neuronal sensitivity both across and within individual studies. When controlled for sensitivity, we found remarkable consistency in CP across varying tasks and brain regions with two notable exceptions. First, CPs were higher in tasks involving bistable percepts, reinforcing the link between CP magnitude and subjective perception. Second, CPs were smaller in area V1, supporting prior suggestions about V1s special role in visual processing. We further found a significant effect of stimulus duration on CP, providing evidence against strictly feedforward models and favoring models with substantial feedback and recurrent processing. Finally, we offer recommendations for future studies to enhance the cross-study comparability and theoretical utility of choice signals as the field transitions to large-scale population recordings. More broadly, our findings demonstrate the benefits of meta-studies that expose patterns across many different tasks and animals - yielding insights that complement large-scale population recordings.

neuroscience↗

Computational characterization of metacognitive ability in subjective decision-making

Metacognition is the process of reflecting on and controlling ones own thoughts and behaviors. Metacognitive ability is often measured through modeling the relationship between confidence reports and choice behavior in tasks where performance can be objectively measured. Previous work has explored whether metacognitive ability is conserved across different types of tasks, and across different domains such as perception and memory. However, it is unclear whether approaches to the assessment of metacognitive ability that have worked in these contexts can be extended to value-based decision-making where objective accuracy cannot be evaluated. Here, we compare metacognitive ability across different tasks spanning perception and valuation, using Bayesian hierarchical estimation of the parameters of a computational process model of confidence. This model captures metacognitive ability as the uncertainty of an individuals own decision uncertainty, and can do so in the space of any decision variable, regardless of whether it indexes external features or internal, subjective states. We find that metacognitive ability can be reliably estimated in both objective and subjective decision-making tasks, and is relatively well conserved across tasks, especially within domains and similar confidence reporting paradigms.

neuroscience↗

Sensory population activity reveals confidence computations in the primate visual system

Perception is fallible1-3. Humans know this4-6, and so do some non-human animals like macaque monkeys7-14. When monkeys report more confidence in a perceptual decision, that decision is more likely to be correct. It is not known how neural circuits in the primate brain assess the quality of perceptual decisions. Here, we test two hypotheses. First, that decision confidence is related to the structure of population activity in sensory cortex. And second, that this relation differs from the one between sensory activity and decision content. We trained macaque monkeys to judge the orientation of ambiguous stimuli and additionally report their confidence in these judgments. We recorded population activity in the primary visual cortex and used decoders to expose the relationship between this activity and the choice-confidence reports. Our analysis validated both hypotheses and suggests that perceptual decisions arise from a neural computation downstream of visual cortex that estimates the most likely interpretation of a sensory response, while decision confidence instead reflects a computation that evaluates whether this sensory response will produce a reliable decision. Our work establishes a direct link between neural population activity in sensory cortex and the metacognitive ability to introspect about the quality of perceptual decisions.

neuroscience↗

Neuronal and behavioral responses to naturalistic texture images in macaque monkeys

The visual world is richly adorned with texture, which can serve to delineate important elements of natural scenes. In anesthetized macaque monkeys, selectivity for the statistical features of natural texture is weak in V1, but substantial in V2, suggesting that neuronal activity in V2 might directly support texture perception. To test this, we investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured behavioral judgments of texture. We generated stimuli along a continuum between naturalistic texture and phase-randomized noise and trained two macaque monkeys to judge whether a sample texture more closely resembled one or the other extreme. Analysis of responses revealed that individual V1 and V2 neurons carried much less information about texture naturalness than behavioral reports. However, the sensitivity of V2 neurons, especially those preferring naturalistic textures, was significantly closer to that of behavior compared with V1. The firing of both V1 and V2 neurons predicted perceptual choices in response to repeated presentations of the same ambiguous stimulus in one monkey, despite low individual neural sensitivity. However, neither population predicted choice in the second monkey. We conclude that neural responses supporting texture perception likely continue to develop downstream of V2. Further, combined with neural data recorded while the same two monkeys performed an orientation discrimination task, our results demonstrate that choice-correlated neural activity in early sensory cortex is unstable across observers and tasks, untethered from neuronal sensitivity, and thus unlikely to reflect a critical aspect of the formation of perceptual decisions. Significance statementAs visual signals propagate along the cortical hierarchy, they encode increasingly complex aspects of the sensory environment and likely have a more direct relationship with perceptual experience. We replicate and extend previous results from anesthetized monkeys differentiating the selectivity of neurons along the first step in cortical vision from area V1 to V2. However, our results further complicate efforts to establish neural signatures that reveal the relationship between perception and the neuronal activity of sensory populations. We find that choice-correlated activity in V1 and V2 is unstable across different observers and tasks, and also untethered from neuronal sensitivity and other features of nonsensory response modulation.

neuroscience↗

How does V1 population activity inform perceptual certainty?

Neural population activity in sensory cortex informs our perceptual interpretation of the environment. Oftentimes, this population activity will support multiple alternative interpretations. The larger the set of plausible alternatives, the more uncertain the selected perceptual interpretation. We test the hypothesis that the reliability of perceptual interpretations can be revealed through simple transformations of sensory population activity. We recorded V1 population activity in fixating macaques while presenting oriented stimuli under different levels of nuisance variability and signal strength. We developed a decoding procedure to infer from V1 activity the most likely stimulus orientation as well as the certainty of this estimate. Our analysis shows that response magnitude, response dispersion, and variability in response gain all offer useful proxies for orientation certainty. Of these three metrics, the last one has the strongest association with the decoders uncertainty estimates. These results clarify that the nature of neural population activity in sensory cortex provides downstream circuits with multiple options to assess the reliability of perceptual interpretations.

neuroscience↗

Confidence as a noisy decision reliability estimate

Decisions vary in difficulty. Humans know this and typically report more confidence in easy than in difficult decisions. However, confidence reports do not perfectly track decision accuracy, but also reflect response biases and difficulty misjudgments. To isolate the quality of confidence reports, we developed a model of the decision-making process underlying choice-confidence data. In this model, confidence reflects a subjects estimate of the reliability of their decision. The quality of this estimate is limited by the subjects uncertainty about the uncertainty of the variable that informs their decision ("meta-uncertainty"). This model provides an accurate account of choice-confidence data across a broad range of perceptual and cognitive tasks, revealing that meta-uncertainty varies across subjects, is stable over time, generalizes across some domains, and can be manipulated experimentally. The model offers a parsimonious explanation for the computational processes that underlie and constrain the sense of confidence.

animal behavior and cognition↗

Representation of uncertainty in macaque visual cortex

Uncertainty is intrinsic to perception. Neural circuits which process sensory information must therefore also represent the reliability of this information. How they do so is a topic of debate. We propose a view of visual cortex in which average neural response strength encodes stimulus features, while cross-neuron variability in response gain encodes the uncertainty of these features. To test our theory, we studied spiking activity of neurons in macaque V1 and V2 elicited by repeated presentations of stimuli whose uncertainty was manipulated in distinct ways. We show that gain variability of individual neurons is tuned to stimulus uncertainty, that this tuning is invariant to the source of uncertainty, and that it is specific to the features encoded by these neurons. We demonstrate that this behavior naturally arises from known gain-control mechanisms, and derive how downstream circuits can jointly decode stimulus features and their uncertainty from sensory population activity.

neuroscience↗