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Cross-modal interactions between auditory attention and oculomotor control.
Microsaccades are small, involuntary eye movements that occur during fixation. Their role is debated with recent hypotheses proposing a contribution to automatic scene sampling. Microsaccade inhibition (MSI) refers to the abrupt suppression of microsaccades, typically evoked within 0.1 seconds after new stimulus onset. The functional significance and neural underpinnings of MSI are subjects of ongoing research. It has been suggested that MSI is a component of the brain's attentional re-orienting network which facilitates the allocation of attention to new environmental occurrences by reducing disruptions or shifts in gaze that could interfere with processing.The extent to which MSI is reflexive or influenced by top-down mechanisms remains debated. We developed a task that examines the impact of auditory top-down attention on MSI, allowing us to disentangle ocular dynamics from visual sensory processing. Participants (N=24 and 27; both sexes) listened to two simultaneous streams of tones and were instructed to attend to one stream while detecting specific task "targets." We quantified MSI in response to occasional task-irrelevant events presented in both the attended and unattended streams (frequency steps in Experiment 1, omissions in Experiment 2).The results show that initial stages of MSI are not affected by auditory attention. However, later stages (∼0.25s post event-onset), affecting the extent and duration of the inhibition, are enhanced for sounds in the attended stream compared to the unattended stream. These findings provide converging evidence for the reflexive nature of early MSI stages and robustly demonstrate the involvement of auditory attention in modulating the later stages.Significance Statement Microsaccades are rapid eye movements occurring during fixation. Their precise role is not known but a major hypothesis is that they reflect automatic sampling of the environment. A feature of microsaccades is that they exhibit abrupt suppression (MSI) after the presentation of new stimuli. This is thought to be part of attentional re-orienting. To understand the neural circuit that controls MSI, and by extension, the brain's response to novel events in the environment, it is essential to determine which factors affect MSI. We show, for the first time, that auditory attention affects the latter (but not initial) stages of MSI. Thus, the early stages of MSI are automatic, but subsequent phases are affected by the perceptual state of the individual.
Distributional reinforcement learning in prefrontal cortex.
The prefrontal cortex is crucial for learning and decision-making. Classic reinforcement learning (RL) theories center on learning the expectation of potential rewarding outcomes and explain a wealth of neural data in the prefrontal cortex. Distributional RL, on the other hand, learns the full distribution of rewarding outcomes and better explains dopamine responses. In the present study, we show that distributional RL also better explains macaque anterior cingulate cortex neuronal responses, suggesting that it is a common mechanism for reward-guided learning.
Effort-based decision making and motivational deficits in stroke patients.
Motivational deficits in patients recovering from stroke are common and can reduce active participation in rehabilitation and thereby impede functional recovery. We investigated whether stroke patients with clinically reduced drive, initiation, and endurance during functional rehabilitative training (n = 30) display systematic alterations in effort-based decision making compared to age, sex, and severity-matched stroke patients (n = 30) whose drive appeared unaffected. Notably, the two groups did not differ in self-reported ratings of apathy and depression. However, on an effort-based decision-making task, stroke patients with clinically apparent drive impairment showed intact willingness to accept effort for reward, but were more likely to fail to execute the required effort compared to patients without apparent drive impairments. In other words, the decision behavioural assessment revealed that stroke patients that displayed reduced drive, initiation, and endurance during inpatient neurorehabilitation failed to persist in goal-directed effort production, even over very short periods. These findings indicate that reduced drive during rehabilitative therapy in post-stroke patients is not due to a diminished motivation to invest physical effort, but instead is related to a reduced persistence with effortful behaviour.
The German version of the Oxford Cognitive Screen (D-OCS): Normative data and validation in acute stroke and a mixed neurological sample.
Given the frequency of stroke worldwide, tools for neuropsychological assessment of patients with acute stroke are needed to identify cognitive impairments, guide rehabilitation efforts and allow for a prognosis of outcome. However, requirements for assessment tools for acute cognitive deficits differ substantially from tests for chronic neuropsychological impairments and screening tools for suspected dementia. The Oxford Cognitive Screen (OCS) has been developed as a quick to administer neurocognitive screening for acute neurological patients providing information on various cognitive domains. It is available in different languages. The present study reports cut-off scores, parallel-test reliability and concurrent validity of the German version (D-OCS). Following standardized language adaptation and translation, the D-OCS was administered to 100 healthy individuals to generate cut-off scores (5th percentile). Subsequently, 88 neurological patients were assessed with both versions of the D-OCS as well as other tests to evaluate reliability and validity of the D-OCS subscales. In a further study, the D-OCS was compared to the MoCA test in 65 acute stroke patients revealing comparable sensitivity but also differences between both tools. The cut-off scores were comparable to other international versions of the OCS. Intraclass correlations were highly significant and document reliability of the D-OCS subtests. Scores on subtests correlated significantly with independent tests securing validity. Comparison with the MoCA revealed comparable sensitivity and specificity. The D-OCS is a reliable and valid assessment tool well suited for patients with acute stroke. Differences to the MoCA test are discussed.
Studying Individual Differences in Language Comprehension: The Challenges of Item-Level Variability and Well-Matched Control Conditions.
Translating experimental tasks that were designed to investigate differences between conditions at the group-level into valid and reliable instruments to measure individual differences in cognitive skills is challenging (Hedge et al., 2018; Rouder et al., 2019; Rouder & Haaf, 2019). For psycholinguists, the additional complexities associated with selecting or constructing language stimuli, and the need for appropriate well-matched baseline conditions make this endeavour particularly complex. In a typical experiment, a process-of-interest (e.g. ambiguity resolution) is targeted by contrasting performance in an experimental condition with performance in a well-matched control condition. In many cases, careful between-condition matching precludes the same participant from encountering all stimulus items. Unfortunately, solutions that work for group-level research (e.g. constructing counterbalanced experiment versions) are inappropriate for individual-differences designs. As a case study, we report an ambiguity resolution experiment that illustrates the steps that researchers can take to address this issue and assess whether their measurement instrument is both valid and reliable. On the basis of our findings, we caution against the widespread approach of using datasets from group-level studies to also answer important questions about individual differences.
Mymou: A low-cost, wireless touchscreen system for automated training of nonhuman primates.
Training nonhuman primates (NHPs) to perform cognitive tasks is essential for many neuroscientific investigations, yet laboratory training is a time-consuming process with inherent limitations. Habituating NHPs to the laboratory staff and experimental equipment can take months before NHPs are ready to proceed to the primary tasks. Laboratory training also necessarily separates NHPs from their home-room social group and typically involves some form of restraint or limited mobility, and data collection is often limited to a few hours per day so that multiple NHPs can be trained on the same equipment. Consequently, it can often take a year to train NHPs on complex cognitive tasks. To overcome these issues, we developed a low-cost, open-source, wireless touchscreen training system that can be installed in the home-room environment. The automated device can run continuously all day, including over weekends, without experimenter intervention. The system utilizes real-time facial recognition to initiate subject-specific tasks and provide accurate data logging, without the need for implanted microchips or separation of the NHPs. The system allows NHPs to select their preferred reward on each trial and to work when and for as long as they desire, and it can analyze task performance in real time and adapt the task parameters in order to expedite training. We demonstrate that NHPs consistently use this system on a daily basis to quickly learn complex behavioral tasks. The system therefore addresses many of the welfare and experimental limitations of laboratory-based training of NHPs and provides a platform for wireless electrophysiological investigations in more naturalistic, freely moving environments.
Contrasting reward signals in the orbitofrontal cortex and anterior cingulate cortex.
Damage to the orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC) impairs decision making, but the underlying value computations that cause such impairments remain unclear. Both the OFC and ACC encode a wide variety of signals correlated with decision making. The current challenge is to determine how these two different areas support decision-making processes. Here, we review a series of experiments that have helped define these roles. A special population of neurons in the ACC, but not the OFC, multiplex value information across decision parameters using a unified encoding scheme, and encode reward prediction errors. In contrast, neurons in the OFC, but not the ACC, encode the value of a choice relative to the recent history of choice values. Together, these results suggest complementary valuation processes: OFC neurons dynamically evaluate current choices relative to the value contexts recently experienced, while ACC neurons encode choice predictions and prediction errors using a common valuation currency reflecting the integration of multiple decision parameters.
Encoding of reward and space during a working memory task in the orbitofrontal cortex and anterior cingulate sulcus.
Several lines of research indicate that emotional and motivational information may be useful in guiding the allocation of attentional resources. Two areas of the frontal lobe that are particularly implicated in the encoding of motivational information are the orbital prefrontal cortex (PFo) and the dorsomedial region of prefrontal cortex, specifically the anterior cingulate sulcus (PFcs). However, it remains unclear whether these areas use this information to influence spatial attention. We used single-unit neurophysiology to examine whether, at the level of individual neurons, there was evidence for integration between reward information and spatial attention. We trained two subjects to perform a task that required them to attend to a spatial location across a delay under different expectancies of reward for correct performance. We balanced the order of presentation of spatial and reward information so we could assess the neuronal encoding of the two pieces of information independently and conjointly. We found little evidence for encoding of the spatial location in either PFo or PFcs. In contrast, both areas encoded the expected reward. Furthermore, PFo consistently encoded reward more quickly than PFcs, although reward encoding was subsequently more prevalent and stronger in PFcs. These results suggest a differential contribution of PFo and PFcs to reward encoding, with PFo potentially more important for initially determining the value of rewards predicted by sensory stimuli. They also suggest that neither PFo nor PFcs play a direct role in the control of spatial attention.
Moving to directly cued locations abolishes spatial interference during bimanual actions.
Interference is frequently observed during bimanual movements if the two hands perform nonsymmetric actions. We examined the source of bimanual interference in two experiments in which we compared conditions involving symmetric movements with conditions in which the movements were of different amplitudes or different directions. The target movements were cued either symbolically by letters or directly by the onset of the target locations. With symbolic cues, reaction times were longer when the movements of the two hands were not symmetric. With direct cues, reaction times were the same for symmetric and nonsymmetric movements. These results indicate that directly cued actions can be programmed in parallel for the two hands. Our results challenge the hypothesis that the cost to initiate nonsymmetric movements is due to spatial intetference in a motor-programming stage. Rather the cost appears to be caused by stimulus identification, response-selection processes connected to the processing of symbolic cues, or both.
Neurons in the frontal lobe encode the value of multiple decision variables.
A central question in behavioral science is how we select among choice alternatives to obtain consistently the most beneficial outcomes. Three variables are particularly important when making a decision: the potential payoff, the probability of success, and the cost in terms of time and effort. A key brain region in decision making is the frontal cortex as damage here impairs the ability to make optimal choices across a range of decision types. We simultaneously recorded the activity of multiple single neurons in the frontal cortex while subjects made choices involving the three aforementioned decision variables. This enabled us to contrast the relative contribution of the anterior cingulate cortex (ACC), the orbito-frontal cortex, and the lateral prefrontal cortex to the decision-making process. Neurons in all three areas encoded value relating to choices involving probability, payoff, or cost manipulations. However, the most significant signals were in the ACC, where neurons encoded multiplexed representations of the three different decision variables. This supports the notion that the ACC is an important component of the neural circuitry underlying optimal decision making.
Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables.
Damage to the frontal lobe can cause severe decision-making impairments. A mechanism that may underlie this is that neurons in the frontal cortex encode many variables that contribute to the valuation of a choice, such as its costs, benefits and probability of success. However, optimal decision-making requires that one considers these variables, not only when faced with the choice, but also when evaluating the outcome of the choice, in order to adapt future behaviour appropriately. To examine the role of the frontal cortex in encoding the value of different choice outcomes, we simultaneously recorded the activity of multiple single neurons in the anterior cingulate cortex (ACC), orbitofrontal cortex (OFC) and lateral prefrontal cortex (LPFC) while subjects evaluated the outcome of choices involving manipulations of probability, payoff and cost. Frontal neurons encoded many of the parameters that enabled the calculation of the value of these variables, including the onset and offset of reward and the amount of work performed, and often encoded the value of outcomes across multiple decision variables. In addition, many neurons encoded both the predicted outcome during the choice phase of the task as well as the experienced outcome in the outcome phase of the task. These patterns of selectivity were more prevalent in ACC relative to OFC and LPFC. These results support a role for the frontal cortex, principally ACC, in selecting between choice alternatives and evaluating the outcome of that selection thereby ensuring that choices are optimal and adaptive.
Heterogeneous reward signals in prefrontal cortex.
Neurons encode upcoming rewards throughout frontal cortex. Recent papers have helped to determine that these signals play different roles in different frontal regions. Neurons in orbitofrontal cortex (PFo) appear to be responsible for calculating the specific value of an expected reward, information that can help efficiently guide decision-making. Similar signals are also present in the cingulate sulcus (PFcs). By contrast, reward signals in lateral prefrontal cortex (PFl) are consistent with a role in using reward to guide other cognitive processes, such as the allocation of attentional resources and using value information to guide learning other relationships in the environment such as arbitrary stimulus-response mappings. A remaining issue for future work is to specify the precise roles of PFo and PFcs. These two areas show very different patterns of connectivity with other brain areas, and it is currently unclear how this effects their contribution to decision-making.
Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements.
Rhythmic bimanual movements are highly constrained in the temporal domain, with the gestures of the two hands tightly synchronized. Previous studies have implicated a subcortical locus for temporal coupling based on the observation that these constraints persist in callosotomy patients. We now report that such coupling is restricted to movements entailing a discrete event (such as a movement onset). Three callosotomy patients exhibited a striking lack of temporal coupling during continuous movements, with the two hands oscillating at non-identical frequencies. We propose a subcortical locus of temporal coupling for movements involving discrete events. In contrast, synchronization between the hands during continuous movements depends on interhemispheric transmission across the corpus callosum.
Bimanual cross-talk during reaching movements is primarily related to response selection, not the specification of motor parameters.
Simultaneous reaching movements made with the two hands can show a considerable increase in reaction time (RT) when they differ in terms of direction or extent, compared to when the movements involve the same direction and extent. This cost has been attributed to cross-talk in the specification of the motor parameters for the two hands. However, a recent study [Diedrichsen, Hazeltine, Kennerley, & Ivry, (2001). Psychological Science, 12, 493-498] indicates that when reaching movements are cued by the onset of the target endpoint, no compatibility effects are observed. To determine why directly cued movements are immune from interference, we varied the stimulus onset asynchrony for the two movements and used different combinations of directly cued and symbolically cued movements. In two experiments, compatibility effects were only observed when both movements were symbolically cued. No difference was found between compatible and incompatible movements when both movements were directly cued or when one was directly cued and the other was symbolically cued. These results indicate that interference is not related to the specification of movement parameters but instead emerges from processes associated with response selection. Moreover, the data suggest that cross-talk, when present, primarily shortens the RT of the second movement on compatible trials rather than lengthening this RT on incompatible trials.