Allen W. Song

Experience-dependent changes in cerebellar contributions to motor sequence learning

Studies in experimental animals and humans have stressed the role of the cerebellum in motor skill learning. Yet, the relative importance of the cerebellar cortex and deep nuclei, as well as the nature of the dynamic functional changes occurring between these and other motor-related structures during learning, remains in dispute. Using functional magnetic resonance imaging and a motor sequence learning paradigm in humans, we found evidence of an experience-dependent shift of activation from the cerebellar cortex to the dentate nucleus during early learning, and from a cerebellar–cortical to a striatal–cortical network with extended practice. The results indicate that intrinsic modulation within the cerebellum, in concert with activation of motor-related cortical regions, serves to set up a procedurally acquired sequence of movements that is then maintained elsewhere in the brain.

Decisions under Uncertainty: Probabilistic Context Influences Activation of Prefrontal and Parietal Cortices

Many decisions are made under uncertainty; that is, with limited information about their potential consequences. Previous neuroimaging studies of decision making have implicated regions of the medial frontal lobe in processes related to the resolution of uncertainty. However, a different set of regions in dorsal prefrontal and posterior parietal cortices has been reported to be critical for selection of actions to unexpected or unpredicted stimuli within a sequence. In the current study, we induced uncertainty using a novel task that required subjects to base their decisions on a binary sequence of eight stimuli so that uncertainty changed dynamically over time (from 20 to 50%), depending on which stimuli were presented. Activation within prefrontal, parietal, and insular cortices increased with increasing uncertainty. In contrast, within medial frontal regions, as well as motor and visual cortices, activation did not increase with increasing uncertainty. We conclude that the brain response to uncertainty depends on the demands of the experimental task. When uncertainty depends on learned associations between stimuli and responses, as in previous studies, it modulates activation in the medial frontal lobes. However, when uncertainty develops over short time scales as information is accumulated toward a decision, dorsal prefrontal and posterior parietal contributions are critical for its resolution. The distinction between neural mechanisms subserving different forms of uncertainty resolution provides an important constraint for neuroeconomic models of decision making.

Neural mechanisms of top-down control during spatial and feature attention.

Theories of visual selective attention posit that both spatial location and nonspatial stimulus features (e.g., color) are elementary dimensions on which top-down attentional control mechanisms can selectively influence visual processing. Neuropsychological and neuroimaging studies have demonstrated that regions of superior frontal and parietal cortex are critically involved in the control of visual-spatial attention. This frontoparietal control network has also been found to be activated when attention is oriented to nonspatial stimulus features (e.g., motion). To test the generality of the frontoparietal network in attentional control, we directly compared spatial and nonspatial attention in a cuing paradigm. Event-related fMRI methods permitted the isolation of attentional control activity during orienting to a location or to a nonspatial stimulus feature (color). Portions of the frontoparietal network were commonly activated to the spatial and nonspatial cues. However, direct statistical comparisons of cue-related activity revealed subregions of the frontoparietal network that were significantly more active during spatial than nonspatial orienting when all other stimulus, task, and attentional factors were equated. No regions of the frontal-parietal network were more active for nonspatial cues in comparison to spatial cues. These findings support models suggesting that subregions of the frontal-parietal network are highly specific for controlling spatial selective attention.

Cerebral White Matter Integrity and Cognitive Aging: Contributions from Diffusion Tensor Imaging

The integrity of cerebral white matter is critical for efficient cognitive functioning, but little is known regarding the role of white matter integrity in age-related differences in cognition. Diffusion tensor imaging (DTI) measures the directional displacement of molecular water and as a result can characterize the properties of white matter that combine to restrict diffusivity in a spatially coherent manner. This review considers DTI studies of aging and their implications for understanding adult age differences in cognitive performance. Decline in white matter integrity contributes to a disconnection among distributed neural systems, with a consistent effect on perceptual speed and executive functioning. The relation between white matter integrity and cognition varies across brain regions, with some evidence suggesting that age-related effects exhibit an anterior–posterior gradient. With continued improvements in spatial resolution and integration with functional brain imaging, DTI holds considerable promise, both for theories of cognitive aging and for translational application.

Diffusion tensor imaging of cerebral white matter integrity in cognitive aging

In this article we review recent research on diffusion tensor imaging (DTI) of white matter (WM) integrity and the implications for age-related differences in cognition. Neurobiological mechanisms defined from DTI analyses suggest that a primary dimension of age-related decline in WM is a decline in the structural integrity of myelin, particularly in brain regions that myelinate later developmentally. Research integrating behavioral measures with DTI indicates that WM integrity supports the communication among cortical networks, particularly those involving executive function, perceptual speed, and memory (i.e., fluid cognition). In the absence of significant disease, age shares a substantial portion of the variance associated with the relation between WM integrity and fluid cognition. Current data are consistent with one model in which age-related decline in WM integrity contributes to a decreased efficiency of communication among networks for fluid cognitive abilities. Neurocognitive disorders for which older adults are at risk, such as depression, further modulate the relation between WM and cognition, in ways that are not as yet entirely clear. Developments in DTI technology are providing a new insight into both the neurobiological mechanisms of aging WM and the potential contribution of DTI to understanding functional measures of brain activity. This article is part of a Special Issue entitled: Imaging Brain Aging and Neurodegenerative disease.

Distinct Value Signals in Anterior and Posterior Ventromedial Prefrontal Cortex

The core feature of an economic exchange is a decision to trade one good for another, based on a comparison of relative value. Economists have long recognized, however, that the value an individual ascribes to a good during decision making (i.e., their relative willingness to trade for that good) does not always map onto the reward they actually experience. Here, we show that experienced value and decision value are represented in distinct regions of ventromedial prefrontal cortex (VMPFC) during the passive consumption of rewards. Participants viewed two categories of rewards—images of faces that varied in their attractiveness and monetary gains and losses—while being scanned using functional magnetic resonance imaging. An independent market task, in which participants exchanged some of the money that they had earned for brief views of attractive faces, determined the relative decision value associated with each category. We found that activation of anterior VMPFC increased with increasing experienced value, but not decision value, for both reward categories. In contrast, activation of posterior VMPFC predicted each individuals relative decision value for face and monetary stimuli. These results indicate not only that experienced value and decision value are represented in distinct regions of VMPFC, but also that decision value signals are evident even in the absence of an overt choice task. We conclude that decisions are made by comparing neural representations of the value of different goods encoded in posterior VMPFC in a common, relative currency.

Functional Parcellation of Attentional Control Regions of the Brain

Recently, a number of investigators have examined the neural loci of psychological processes enabling the control of visual spatial attention using cued-attention paradigms in combination with event-related functional magnetic resonance imaging. Findings from these studies have provided strong evidence for the involvement of a fronto-parietal network in attentional control. In the present study, we build upon this previous work to further investigate these attentional control systems. In particular, we employed additional controls for nonattentional sensory and interpretative aspects of cue processing to determine whether distinct regions in the fronto-parietal network are involved in different aspects of cue processing, such as cue-symbol interpretation and attentional orienting. In addition, we used shorter cue-target intervals that were closer to those used in the behavioral and event-related potential cueing literatures. Twenty participants performed a cued spatial attention task while brain activity was recorded with functional magnetic resonance imaging. We found functional specialization for different aspects of cue processing in the lateral and medial subregions of the frontal and parietal cortex. In particular, the medial subregions were more specific to the orienting of visual spatial attention, while the lateral subregions were associated with more general aspects of cue processing, such as cue-symbol interpretation. Additional cue-related effects included differential activations in midline frontal regions and pretarget enhancements in the thalamus and early visual cortical areas.

Conflict monitoring in the human anterior cingulate cortex during selective attention to global and local object features.

Parallel processing affords the brain many advantages, but processing multiple bits of information simultaneously presents formidable challenges. For example, while one is listening to a speaker at a noisy social gathering, processing irrelevant conversations may lead to the activation of irrelevant perceptual, semantic, and response representations that conflict with those evoked by the speaker. In these situations, specialized brain systems may be recruited to detect and resolve conflict before it leads to incorrect perception and/or behavior. Consistent with this view, recent findings indicate that dorsal/caudal anterior cingulate cortex (dACC), on the medial walls of the frontal lobes, detects conflict between competing motor responses primed by relevant versus irrelevant stimuli. Here, we used a cued global/local selective attention task to investigate whether the dACC plays a general role in conflict detection that includes monitoring for conflicting perceptual or semantic representations. Using event-related functional magnetic resonance imaging (fMRI), we found that the dACC was activated by response conflict in both the global and the local task, consistent with results from prior studies. However, dACC was also activated by perceptual and semantic conflict arising from global distracters during the local task. The results from the local task have implications for recent theories of attentional control in which the dACCs contribution to conflict monitoring is limited to response stages of processing, as well as for our understanding of clinical disorders in which disruptions of attention are associated with dACC dysfunction.

The Involvement of the Dopaminergic Midbrain and Cortico-Striatal-Thalamic Circuits in the Integration of Reward Prospect and Attentional Task Demands

Reward has been shown to promote human performance in multiple task domains. However, an important debate has developed about the uniqueness of reward-related neural signatures associated with such facilitation, as similar neural patterns can be triggered by increased attentional focus independent of reward. Here, we used functional magnetic resonance imaging to directly investigate the neural commonalities and interactions between the anticipation of both reward and task difficulty, by independently manipulating these factors in a cued-attention paradigm. In preparation for the target stimulus, both factors increased activity within the midbrain, dorsal striatum, and fronto-parietal areas, while inducing deactivations in default-mode regions. Additionally, reward engaged the ventral striatum, posterior cingulate, and occipital cortex, while difficulty engaged medial and dorsolateral frontal regions. Importantly, a network comprising the midbrain, caudate nucleus, thalamus, and anterior midcingulate cortex exhibited an interaction between reward and difficulty, presumably reflecting additional resource recruitment for demanding tasks with profitable outcome. This notion was consistent with a negative correlation between cue-related midbrain activity and difficulty-induced performance detriments in reward-predictive trials. Together, the data demonstrate that expected value and attentional demands are integrated in cortico-striatal-thalamic circuits in coordination with the dopaminergic midbrain to flexibly modulate resource allocation for an effective pursuit of behavioral goals.

Amygdala Activation to Sad Pictures During High-Field (4 Tesla) Functional Magnetic Resonance Imaging

Fear-related processing in the amygdala has been well documented, but its role in signaling other emotions remains controversial. The authors recovered signal loss in the amygdala at high-field strength using an inward spiral pulse sequence and probed its response to pictures varying in their degree of portrayed sadness. These pictures were presented as intermittent task-irrelevant distractors during a concurrent visual oddball task. Relative to neutral distractors, sad distractors elicited greater activation along ventral brain regions, including the amygdala, fusiform gyrus, and inferior frontal gyrus. In contrast, oddball targets engaged dorsal sectors of frontal, parietal, and cingulate cortices. The amygdalas role in emotional evaluation thus extends to images of grief and despair as well as to those depicting violence and threat.