Jiefeng Jiang

Determinants of congruency sequence effects without learning and memory confounds.

A common finding in distracter interference (e.g., Flanker) tasks is that the difference in mean reaction time (RT) between incongruent and congruent trials-the congruency effect-is smaller when the previous trial was incongruent relative to congruent. Over the past 2 decades, 2 main accounts of this congruency sequence effect (CSE) have been proposed. One posits that the CSE indexes trial-by-trial adjustments of cognitive control, which are triggered by expectation, response conflict, negative affect, or response suppression. The other holds that the CSE indexes feature integration and/or contingency learning processes that are confounded with congruency sequence in most studies. In 3 online experiments involving over 450 participants, we observed CSEs without such confounds when 2 preconditions were met: (a) stimulus-response translation could be completed more rapidly for the distracter than for the target and (b) the distracter and target appeared at the same location. We also found that CSE magnitude did not vary consistently with the size of the congruency effect. These findings reveal that CSEs can be observed in the absence of feature integration and contingency learning confounds, but impose important new constraints on certain cognitive control accounts of this phenomenon.

Attention Sharpens the Distinction between Expected and Unexpected Percepts in the Visual Brain

Attention, the prioritization of goal-relevant stimuli, and expectation, the modulation of stimulus processing by probabilistic context, represent the two main endogenous determinants of visual cognition. Neural selectivity in visual cortex is enhanced for both attended and expected stimuli, but the functional relationship between these mechanisms is poorly understood. Here, we adjudicated between two current hypotheses of how attention relates to predictive processing, namely, that attention either enhances or filters out perceptual prediction errors (PEs), the PE-promotion model versus the PE-suppression model. We acquired fMRI data from category-selective visual regions while human subjects viewed expected and unexpected stimuli that were either attended or unattended. Then, we trained multivariate neural pattern classifiers to discriminate expected from unexpected stimuli, depending on whether these stimuli had been attended or unattended. If attention promotes PEs, then this should increase the disparity of neural patterns associated with expected and unexpected stimuli, thus enhancing the classifiers ability to distinguish between the two. In contrast, if attention suppresses PEs, then this should reduce the disparity between neural signals for expected and unexpected percepts, thus impairing classifier performance. We demonstrate that attention greatly enhances a neural pattern classifiers ability to discriminate between expected and unexpected stimuli in a region- and stimulus category-specific fashion. These findings are incompatible with the PE-suppression model, but they strongly support the PE-promotion model, whereby attention increases the precision of prediction errors. Our results clarify the relationship between attention and expectation, casting attention as a mechanism for accelerating online error correction in predicting task-relevant visual inputs.

An insula-frontostriatal network mediates flexible cognitive control by adaptively predicting changing control demands

The anterior cingulate and lateral prefrontal cortices have been implicated in implementing context-appropriate attentional control, but the learning mechanisms underlying our ability to flexibly adapt the control settings to changing environments remain poorly understood. Here we show that human adjustments to varying control demands are captured by a reinforcement learner with a flexible, volatility-driven learning rate. Using model-based functional magnetic resonance imaging, we demonstrate that volatility of control demand is estimated by the anterior insula, which in turn optimizes the prediction of forthcoming demand in the caudate nucleus. The caudates prediction of control demand subsequently guides the implementation of proactive and reactive attentional control in dorsal anterior cingulate and dorsolateral prefrontal cortices. These data enhance our understanding of the neuro-computational mechanisms of adaptive behaviour by connecting the classic cingulate-prefrontal cognitive control network to a subcortical control-learning mechanism that infers future demands by flexibly integrating remote and recent past experiences.

Memory Meets Control in Hippocampal and Striatal Binding of Stimuli, Responses, and Attentional Control States

The human brain encodes experience in an integrative fashion by binding together the various features of an event (i.e., stimuli and responses) into memory “event files.” A subsequent reoccurrence of an event feature can then cue the retrieval of the memory file to “prime” cognition and action. Intriguingly, recent behavioral studies indicate that, in addition to linking concrete stimulus and response features, event coding may also incorporate more abstract, “internal” event features such as attentional control states. In the present study, we used fMRI in healthy human volunteers to determine the neural mechanisms supporting this type of holistic event binding. Specifically, we combined fMRI with a task protocol that dissociated the expression of event feature-binding effects pertaining to concrete stimulus and response features, stimulus categories, and attentional control demands. Using multivariate neural pattern classification, we show that the hippocampus and putamen integrate event attributes across all of these levels in conjunction with other regions representing concrete-feature-selective (primarily visual cortex), category-selective (posterior frontal cortex), and control demand-selective (insula, caudate, anterior cingulate, and parietal cortex) event information. Together, these results suggest that the hippocampus and putamen are involved in binding together holistic event memories that link physical stimulus and response characteristics with internal representations of stimulus categories and attentional control states. These bindings then presumably afford shortcuts to adaptive information processing and response selection in the face of recurring events. SIGNIFICANCE STATEMENT Memory binds together the different features of our experience, such as an observed stimulus and concurrent motor responses, into so-called event files. Recent behavioral studies suggest that the observers internal attentional state might also become integrated into the event memory. Here, we used fMRI to determine the brain areas responsible for binding together event information pertaining to concrete stimulus and response features, stimulus categories, and internal attentional control states. We found that neural signals in the hippocampus and putamen contained information about all of these event attributes and could predict behavioral priming effects stemming from these features. Therefore, medial temporal lobe and dorsal striatum structures appear to be involved in binding internal control states to event memories.

Visual Prediction Error Spreads Across Object Features in Human Visual Cortex.

Visual cognition is thought to rely heavily on contextual expectations. Accordingly, previous studies have revealed distinct neural signatures for expected versus unexpected stimuli in visual cortex. However, it is presently unknown how the brain combines multiple concurrent stimulus expectations such as those we have for different features of a familiar object. To understand how an unexpected object feature affects the simultaneous processing of other expected feature(s), we combined human fMRI with a task that independently manipulated expectations for color and motion features of moving-dot stimuli. Behavioral data and neural signals from visual cortex were then interrogated to adjudicate between three possible ways in which prediction error (surprise) in the processing of one feature might affect the concurrent processing of another, expected feature: (1) feature processing may be independent; (2) surprise might “spread” from the unexpected to the expected feature, rendering the entire object unexpected; or (3) pairing a surprising feature with an expected feature might promote the inference that the two features are not in fact part of the same object. To formalize these rival hypotheses, we implemented them in a simple computational model of multifeature expectations. Across a range of analyses, behavior and visual neural signals consistently supported a model that assumes a mixing of prediction error signals across features: surprise in one object feature spreads to its other feature(s), thus rendering the entire object unexpected. These results reveal neurocomputational principles of multifeature expectations and indicate that objects are the unit of selection for predictive vision. SIGNIFICANCE STATEMENT We address a key question in predictive visual cognition: how does the brain combine multiple concurrent expectations for different features of a single object such as its color and motion trajectory? By combining a behavioral protocol that independently varies expectation of (and attention to) multiple object features with computational modeling and fMRI, we demonstrate that behavior and fMRI activity patterns in visual cortex are best accounted for by a model in which prediction error in one object feature spreads to other object features. These results demonstrate how predictive vision forms object-level expectations out of multiple independent features.

Causal evidence for learning-dependent frontal-lobe contributions to cognitive control

The lateral prefrontal cortex (LPFC) plays a central role in the prioritization of sensory input based on task relevance. Such top-down control of perception is of fundamental importance in goal-directed behavior, but can also be costly when deployed excessively, necessitating a mechanism that regulates control engagement to align it with changing environmental demands. We have recently introduced the “flexible control model” (FCM), which explains this regulation as resulting from a self-adjusting reinforcement-learning mechanism that infers latent statistical structure in dynamic task environments to predict forthcoming states. From this perspective, LPFC-based control is engaged as a function of anticipated cognitive demand, a notion for which we previously obtained correlative neuroimaging evidence. Here, we put this hypothesis to a rigorous, causal test by combining the FCM with a transcranial magnetic stimulation (TMS) intervention that transiently perturbed the LPFC. Human participants (male and female) completed a nonstationary version of the Stroop task with dynamically changing probabilities of conflict between task-relevant and task-irrelevant stimulus features. TMS was given on each trial before stimulus onset either over the LPFC or over a control site. In the control condition, we observed adaptive performance fluctuations consistent with demand predictions that were inferred from recent and remote trial history and effectively captured by our model. Critically, TMS over the LPFC eliminated these fluctuations while leaving basic cognitive and motor functions intact. These results provide causal evidence for a learning-based account of cognitive control and delineate the nature of the signals that regulate top-down biases over stimulus processing. SIGNIFICANCE STATEMENT A core function of the human prefrontal cortex is to control the signal flow in sensory brain regions to prioritize processing of task-relevant information. Abundant work suggests that such control is flexibly recruited to accommodate dynamically changing environmental demands, yet the nature of the signals that serve to engage control remains unknown. Here, we combined computational modeling with noninvasive brain stimulation to show that changes in control engagement are captured by a self-adjusting reinforcement-learning mechanism that tracks changing environmental statistics to predict forthcoming processing demands and that transient perturbation of the prefrontal cortex abolishes these adjustments. These findings delineate the learning signals that underpin adaptive engagement of prefrontal control functions and provide causal evidence for their relevance in behavioral control.

External and Internally Generated Task Predictions are Integrated in Prefrontal Cortex to Jointly Guide Cognitive Control

Cognitive control proactively configures information processing to suit expected task demands. Predictions of forthcoming demand can be driven by explicit external cues or be generated internally, based on past experience (cognitive history). However, it is not known whether and how the brain reconciles these two sources of information to guide control. Pairing a probabilistic task-switching paradigm with computational modeling, we found that external and internally generated predictions jointly guide task preparation, with a bias for internal predictions. Using model-based neuroimaging, we then show that the two sources of task prediction are integrated in dorsolateral prefrontal cortex, and jointly inform a representation of the likelihood of a change in task demand, encoded in frontoparietal cortex. Upon task-stimulus onset, dorsomedial prefrontal cortex encoded the need for reactive task-set adjustment. These data reveal, for the first time, how the human brain integrates external cues and cognitive history to prepare for an upcoming task.

Integrated externally and internally generated task predictions jointly guide cognitive control in prefrontal cortex

Cognitive control proactively configures information processing to suit expected task demands. Predictions of forthcoming demand can be driven by explicit external cues or be generated internally, based on past experience (cognitive history). However, it is not known whether and how the brain reconciles these two sources of information to guide control. Pairing a probabilistic task-switching paradigm with computational modeling, we found that external and internally generated predictions jointly guide task preparation, with a bias for internal predictions. Using model-based neuroimaging, we then show that the two sources of task prediction are integrated in dorsolateral prefrontal cortex, and jointly inform a representation of the likelihood of a change in task demand, encoded in frontoparietal cortex. Upon task-stimulus onset, dorsomedial prefrontal cortex encoded the need for reactive task-set adjustment. These data reveal how the human brain integrates external cues and cognitive history to prepare for an upcoming task.

THE CONTRIBUTION OF EARLY ALZHEIMER’S DISEASE MARKERS TO INDIVIDUAL DIFFERENCES IN EPISODIC MEMORY IN COGNITIVELY NORMAL OLDER ADULTS

P4-322 THE CONTRIBUTION OF EARLY ALZHEIMER’S DISEASE MARKERS TO INDIVIDUAL DIFFERENCES IN EPISODIC MEMORY IN COGNITIVELY NORMAL OLDER ADULTS Alexandra N. Trelle, Jeffrey Bernstein, Valerie A. Carr, Gayle Deutsch, Carolyn A. Fredericks, Scott A. Guerin, Wanjia Guo, Marc Harrison, Manasi Jayakumar, Jiefeng Jiang, Geoffrey A. Kerchner, Anna Khazhenzon, Celia Litovsky, Beth C. Mormino, Ayesha Nadiadwala, Sharon Sha, Natalie Tanner, Monica Thieu, Anthony D. Wagner, Stanford University, Stanford, CA, USA; University of California San Diego, San Diego, CA, USA; San Jose State University, San Jose, CA, USA; Stanford Hospital and Clinics, Palo Alto, CA, USA; Genentech, Inc, South San Francisco, CA, USA; Johns Hopkins University, Baltimore, MD, USA; Massachusetts General Hospital, Boston, MA, USA; University of California at Irvine, Irvine, CA, USA; Stanford University, Palo Alto, CA, USA; Columbia University, New York, NY, USA. Contact e-mail: atrelle@stanford.edu