The processes of attention and working memory are conspicuously interlinked, suggesting that they may involve overlapping neural mechanisms. Working memory (WM) is the ability to maintain information in the absence of sensory input. Attention is the process by which a specific target is selected for further processing, and neural resources directed toward that target. The content of WM can be used to direct attention, and attention can in turn determine which information is encoded into WM. Here we discuss the similarities between attention and WM and the role prefrontal cortex (PFC) plays in each. First, at the theoretical level, we describe how attention and WM can both rely on models based on attractor states. Then we review the evidence for an overlap between the areas involved in both functions, especially the frontal eye field (FEF) portion of the prefrontal cortex. We also discuss similarities between the neural changes in visual areas observed during attention and WM. At the cellular level, we review the literature on the role of prefrontal DA in both attention and WM at the behavioral and neural levels. Finally, we summarize the anatomical evidence for an overlap between prefrontal mechanisms involved in attention and WM. Altogether, a summary of pharmacological, electrophysiological, behavioral, and anatomical evidence for a contribution of the FEF part of prefrontal cortex to attention and WM is provided.
Neurons in sensory areas of the neocortex are known to represent information both about sensory stimuli and behavioral state, but how these 2 disparate signals are integrated across cortical layers is poorly understood. To study this issue, we measured the coding of visual stimulus orientation and of behavioral state by neurons within superficial and deep layers of area V4 in monkeys while they covertly attended or prepared eye movements to visual stimuli. We show that whereas single neurons and neuronal populations in the superficial layers conveyed more information about the orientation of visual stimuli than neurons in deep layers, the opposite was true of information about the behavioral relevance of those stimuli. In particular, deep layer neurons encoded greater information about the direction of planned eye movements than superficial neurons. These results suggest a division of labor between cortical layers in the coding of visual input and visually guided behavior.
Weber's law can be explained either by a compressive scaling of sensory response with stimulus magnitude or by a proportional scaling of response variability. These two mechanisms can be distinguished by asking how quantities are added or subtracted. We trained Rhesus monkeys to associate 26 distinct symbols with 0-25 drops of reward, and then tested how they combine, or add, symbolically represented reward magnitude. We found that they could combine symbolically represented magnitudes, and they transferred this ability to a novel symbol set, indicating that they were performing a calculation, not just memorizing the value of each combination. The way they combined pairs of symbols indicated neither a linear nor a compressed scale, but rather a dynamically shifting, relative scaling.macaque | normalization | number sense | value coding A nimals and humans can estimate the number of various items, and the precision of this approximate number sense decreases with magnitude. For example, although it is easy to recognize the difference between 2 and 4 items, it is more difficult to distinguish 22 from 24 items. This dependence of accuracy on magnitude is a property that the approximate number sense shares with more basic sensory processes. Weber (1) observed that in general, across many sensory modalities, the just noticeable difference between two stimuli is proportional to their magnitude. Fechner (2) proposed that Weber's observation could be explained if sensations were physiologically encoded as a logarithmic function of stimulus magnitude, but Stevens (3) argued instead that sensations obey a power law, with perceptual magnitude being proportional to a power function of the stimulus magnitude, with the power usually less than 1. Both a logarithmic and a power-less-than-one relationship between stimulus and internal coding are compressive, with the same physical difference between stimuli producing incrementally smaller internal differences between successively larger pairs of external stimuli. Any kind of compressive scaling would explain a decrease in discriminability with increasing magnitude if the noise in the internal representation is constant.However, an alternative possibility is that variability in encoding might increase with stimulus magnitude. In fact, the variability in the firing rates of cortical neurons tends to increase with firing rate (4-6). Therefore, to the extent that a stimulus parameter is encoded by the rate of neural firing, an increase in perceptual variability with stimulus magnitude may not require compressive scaling; it is also consistent with a linear neuronal representation with magnitude-dependent variability (7-10).Neurons that are tuned to numerosity have been recorded in monkey posterior parietal and lateral prefrontal cortex (11-13). The width and asymmetry of such tuning is consistent with a compressed scaling (14). However, neurons tuned to particular numerosities, or numerosity ranges, represent a labeled-line code and therefore are not, themselves, scaled to numerosity...
We are constantly faced with decisions between alternatives defined by multiple attributes, necessitating an evaluation and integration of different information sources. Time-varying signals in multiple brain areas are implicated in decision-making; but we lack a rigorous biophysical description of how basic circuit properties, such as excitatory-inhibitory (E/I) tone and cascading nonlinearities, shape attribute processing and choice behavior. Furthermore, how such properties govern choice performance under varying levels of environmental uncertainty is unknown. We investigated two-attribute, two-alternative decision-making in a dynamical, cascading nonlinear neural network with three layers: an input layer encoding choice alternative attribute values; an intermediate layer of modules processing separate attributes; and a final layer producing the decision. Depending on intermediate layer E/I tone, the network displays distinct regimes characterized by linear (I), convex (II) or concave (III) choice indifference curves. In regimes I and II, each option’s attribute information is additively integrated. In regime III, time-varying nonlinear operations amplify the separation between offer distributions by selectively attending to the attribute with the larger differences in input values. At low environmental uncertainty, a linear combination most consistently selects higher valued alternatives. However, at high environmental uncertainty, regime III is more likely than a linear operation to select alternatives with higher value. Furthermore, there are conditions where readout from the intermediate layer could be experimentally indistinguishable from the final layer. Finally, these principles are used to examine multi-attribute decisions in systems with reduced inhibitory tone, leading to predictions of different choice patterns and overall performance between those with restrictions on inhibitory tone and neurotypicals.
Latent causes that give rise to experience are encountered in complex, high-dimensional feature spaces.How then do people approximate the external world with lower-dimensional internal representations that generalize to novel examples or contexts? Theories suggest internal representations could be determined by discriminative boundaries, or based on the distance from prototypes/exemplars. We developed theoretical models that use both discriminative and prototype/exemplar components to form internal representations via action-reward feedback. We then developed three new latent-state learning tasks to test human use of discrimination attention and prototypes/exemplars. The majority of subjects attended to discriminative features, as well as the covariance of features within a prototype. A minority of subjects relied on a single discriminative feature. Behavior of all subjects was captured by a model that forms prototype representations and deploys context-specific discriminative attention. These results provide insights into the human ability to generalize across causal latent states learned in high-dimensional environments.
We investigated two-attribute, two-alternative decision-making in a hierarchical neural network with three layers: an input layer encoding choice alternative attribute values; an intermediate layer of modules processing separate attributes; and a choice layer producing the decision. Depending on intermediate layer excitatory-inhibitory (E/I) tone, the network displays three distinct regimes characterized by linear (I), convex (II) or concave (III) choice indifference curves. In regimes I and II, each option's attribute information is additively integrated. To maximize reward at low environmental uncertainty, the system should operate in regime I. At high environmental uncertainty, reward maximization is achieved in regime III, with each attribute module selecting a favored alternative, and the ultimate decision based upon comparison between outputs of attribute processing modules. We then use these principles to examine multi-attribute decisions with autism-related deficits in E/I balance, leading to predictions of different choice patterns and overall performance between autism and neurotypicals. IntroductionWe are constantly faced with decisions between alternatives defined by multiple attributes. The true value of each attribute is at times clear, and other times uncertain. For example, on Friday one might choose between main courses at a restaurant where the flavor or healthiness attributes of all the dishes are familiar.The following Wednesday might be at a restaurant with an unknown cuisine, where one is highly uncertain as to different items' flavor or healthiness. To ensure the best meal, the brain must be able to optimize choice in both environments.Systems neuroscientists have, for many years, been studying the specific circuits engaged in this kind of multi-attribute decision-making. Based on a robust set of electrophysiology and imaging findings (Xie and Padoa-Schioppa 2016; Raghuraman and Padoa-Schioppa 2014; Padoa-Schioppa and Assad 2006; O'Neill and Schultz 2018; Morrison and Salzman 2009; Conen and Padoa-Schioppa 2015; Chib et al. 2009; Pastor-Bernier, Stasiak, and Schultz 2019), many hold that all attribute signals are available in brain areas proximal to the final decision (Levy and Glimcher 2012; Padoa-Schioppa and Conen 2017). Indeed, when attribute values are clear, multi-attribute choice theoretically is simple: linearly weight and combine all attributes associated with a choice alternative, then select the one with the larger value. Though the subjective value of an attribute might be non-linearly related to the quantity offered, when the final choice is made in an environment without uncertainty, a weighted linear combination of attributes optimizes the choice between options (Nicholson and Snyder 2007).
Callous-unemotional (CU) traits are characterized by a lack of prosocial emotions, which has been demonstrated with prosocial behavior paradigms. While shaping our understanding of prosocial behavior in youth with CU traits, most of this work relies on outcomes that don't reliably capture cognitive processes during prosocial behavior. Examining prosocial cognitive processes can cue researchers into cognitive mechanisms underlying core impairments of CU traits. Drift diffusion modeling is a valuable tool for elucidating more precise outcomes of latent cognitive processes during forced choice tasks such as drift rate (information accumulation toward a decision boundary) and threshold separation (amount of information considered) as well as metrics outside of the decision-making processing including bias (starting point in decision process) and non-decision time (cognitive processes outside of choice). In a sample of 87 adolescents (12-14, 49% female) we applied diffusion modeling to a prosocial behavior task in which participants either accepted or rejected trials where a real monetary value was given to them and taken away from a charity (self-serving trial) or money was given to a charity and taken from them (donation trial). Results revealed that CU traits associated with information accumulation toward accepting self-serving trials. Exploratory sex differences suggested males trended toward rejecting donation trials and females considered more information during selfserving trials. CU trait associations were independent of conduct problems. Results suggest a unique cognitive profile that are differentiated by sex at higher CU traits when making prosocial decisions involving knowledge accumulation toward self-serving decisions.
Callous-unemotional (CU) traits are characterized by a lack of prosocial emotions, which has been demonstrated with prosocial behavior paradigms. While shaping our understanding of prosocial behavior in youth with CU traits, most of this work relies on outcomes that don’t reliably capture cognitive processes during prosocial behavior. Examining prosocial cognitive processes can cue researchers into cognitive mechanisms underlying core impairments of CU traits. Drift diffusion modeling is a valuable tool for elucidating more precise outcomes of latent cognitive processes during forced choice tasks such as drift rate (information accumulation toward a decision boundary) and threshold separation (amount of information considered) as well as metrics outside of the decision-making processing including bias (starting point in decision process) and non-decision time (cognitive processes outside of choice). In a sample of 87 adolescents (12-14, 49% female) we applied diffusion modeling to a prosocial behavior task in which participants either accepted or rejected trials where a real monetary value was given to them and taken away from a charity (self-serving trial) or money was given to a charity and taken from them (donation trial). Results revealed that CU traits associated with information accumulation toward accepting self-serving trials. Sex differences demonstrated males trending toward rejecting donation trials and females considering more information during self-serving trials. CU trait associations were independent of conduct problems. Results suggest a unique cognitive profile that are differentiated by sex at higher CU traits when making prosocial decisions involving knowledge accumulation toward self-serving decisions.
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