Philip C. Burton

When Things Are Better or Worse than Expected: The Medial Frontal Cortex and the Allocation of Processing Resources

Access to limited-capacity neural systems of cognitive control must be restricted to the most relevant information. How the brain identifies and selects items for preferential processing is not fully understood. Anatomical models often place the selection mechanism in the medial frontal cortex (MFC), and one computational model proposes that the mesotelencephalic dopamine (DA) system, via its reward prediction properties, provides a gate through which information gains access to limited-capacity systems. There is a medial frontal event-related potential (ERP) index of attention selection, the anterior positivity (P2a), associated with DA reward system input to the MFC for the identification of task-relevant perceptual representations. The P2a has a similar spatio-temporal distribution as the medial frontal negativity (MFN), elicited to error responses or choices resulting in monetary loss. The MFN has also been linked to DA projections to the MFC but for action monitoring rather than attention selection. This study proposes that the P2a and the MFN reflect the same MFC evaluation function and use a passive reward prediction design containing neither instructed attention nor response to demonstrate that the ERP over medial frontal leads at the P2a/MFN latency is consistent with activity of midbrain DA neurons, positive to unpredicted rewards and negative when a predicted reward is withheld. This result suggests that MFC activity is regulated by DA reward system input and may function to identify items or actions that exceed or fail to meet motivational prediction.

Mechanisms of unconscious priming: I. Response competition, not spreading activation.

Four experiments were conducted to replicate and expand upon A. G. Greenwald, S. C. Draine, and R. L. Abramss (1996) demonstration that unconsciously perceived priming words can influence judgments of other words. The present experiments manipulated 2 types of relationships between priming and target stimuli: (a) whether priming and target stimuli possess a preexisting semantic relationship (an affective relationship in Experiments 1, 2, and 4; an associative relationship in Experiment 3; and an animacy relationship in Experiment 4) and (b) whether the primes and targets produce the same response. Large priming effects were found only when the primes and targets possessed response compatibility. No residual effects for affective, animacy, or semantic relatedness were observed. Although these results strongly support the conclusion that word meaning can be unconsciously activated, they do not support the claim that the unconscious perception effects obtained in Greenwald et al.s (1996) paradigm are caused by automatic spreading activation of word meaning. Instead, the results reported here are consistent with a claim that unconsciously perceived words automatically trigger response tendencies that facilitate or interfere with target responding.

Feedback Contributions to Visual Awareness in Human Occipital Cortex

It has traditionally been assumed that processing within the visual system proceeds in a bottom-up, feedforward manner from retina to higher cortical areas. In addition to feedforward processing, it is now clear that there are also important contributions to sensory encoding that rely upon top-down, feedback (reentrant) projections from higher visual areas to lower ones. By utilizing transcranial magnetic stimulation (TMS) in a metacontrast masking paradigm, we addressed whether feedback processes in early visual cortex play a role in visual awareness. We show that TMS of visual cortex, when timed to produce visual suppression of an annulus serving as a metacontrast mask, induces recovery of an otherwise imperceptible disk. In addition to producing disk recovery, TMS suppression of an annulus was greater when a disk preceded it than when an annulus was presented alone. This latter result suggests that there are effects of the disk on the perceptibility of the subsequent mask that are additive and are revealed with TMS of the visual cortex. These results demonstrate spatial and temporal interactions of conscious vision in visual cortex and suggest that a prior visual stimulus can influence subsequent perception at early stages of visual encoding via feedback projections.

Electrophysiological and Hemodynamic Responses to Reward Prediction Violation

Anterior cingulate cortex has been functionally linked to the detection of outcomes that are worse than expected using both scalp electrophysiological [event-related potential (ERP)] and hemodynamic [functional MRI (fMRI)] responses. This study used a reward prediction violation design which acquired both ERP and fMRI data from the same participants in different sessions. Both the medial frontal negativity (MFN) ERP response and anterior cingulate cortex hemodynamic activity differentiated between reward delivery and expectation with the largest MFN and anterior cingulate cortex response when predicted rewards were not delivered. Inverse modeling placed the MFN source near the anterior cingulate cortex hemodynamic activation. The fMRI study also showed increased striatal response to rewards regardless of prediction indicating dissociation of neural processing of reward and reward expectation.

Visually induced feelings of touch.

Recent studies have reported that vision can enhance tactile perception, even in patients with somatosensory deficits. However, it is unclear in these previous studies whether visual input truly enhances detection of tactile stimuli or induces a higher propensity for reporting touch by changing response criteria. In this study, we demonstrate in neurologically normal subjects that in addition to small increases in tactile sensitivity when a non-informative, suprathreshold visual stimulus is presented, there are highly consistent changes in response criteria for reporting touch with vision, even when no tactile stimulus is delivered. These results suggest that some of the previously reported enhancements of touch from vision may rather be a consequence of strategic sensory encoding processes that rely upon the typical correlations between multisensory events.

Converging functional magnetic resonance imaging evidence for a role of the left inferior frontal lobe in semantic retention during language comprehension

Increasing evidence supports dissociable short-term memory (STM) capacities for semantic and phonological representations. Cognitive neuropsychological data suggest that damage to the left inferior and middle frontal gyri are associated with deficits of semantic STM, while damage to inferior parietal areas is associated with deficits of phonological STM. Patients identified as having semantic STM deficits are also impaired on a number of language comprehension and production paradigms. We used one such comprehension task derived from cognitive neuropsychological data to test predictions with functional magnetic resonance imaging (fMRI) using healthy participants. Using a task that required participants to make semantic anomaly judgements, we found significantly greater activation in areas of the left inferior frontal and middle frontal gyri for phrases that required maintenance of multiple words for eventual integration with a subsequent noun or verb. These data are consistent with our previous patient studies (Hanten & Martin, 2000; R. C. Martin & He, 2004; R. C. Martin & Romani, 1994) that suggest that semantic STM is associated with the left inferior and middle frontal gyri and that deficits of semantic STM have particular consequences for comprehension tasks that require maintenance of several word meanings in unintegrated form.

Representations of Pitch and Timbre Variation in Human Auditory Cortex

Pitch and timbre are two primary dimensions of auditory perception, but how they are represented in the human brain remains a matter of contention. Some animal studies of auditory cortical processing have suggested modular processing, with different brain regions preferentially coding for pitch or timbre, whereas other studies have suggested a distributed code for different attributes across the same population of neurons. This study tested whether variations in pitch and timbre elicit activity in distinct regions of the human temporal lobes. Listeners were presented with sequences of sounds that varied in either fundamental frequency (eliciting changes in pitch) or spectral centroid (eliciting changes in brightness, an important attribute of timbre), with the degree of pitch or timbre variation in each sequence parametrically manipulated. The BOLD responses from auditory cortex increased with increasing sequence variance along each perceptual dimension. The spatial extent, region, and laterality of the cortical regions most responsive to variations in pitch or timbre at the univariate level of analysis were largely overlapping. However, patterns of activation in response to pitch or timbre variations were discriminable in most subjects at an individual level using multivoxel pattern analysis, suggesting a distributed coding of the two dimensions bilaterally in human auditory cortex. SIGNIFICANCE STATEMENT Pitch and timbre are two crucial aspects of auditory perception. Pitch governs our perception of musical melodies and harmonies, and conveys both prosodic and (in tone languages) lexical information in speech. Brightness—an aspect of timbre or sound quality—allows us to distinguish different musical instruments and speech sounds. Frequency-mapping studies have revealed tonotopic organization in primary auditory cortex, but the use of pure tones or noise bands has precluded the possibility of dissociating pitch from brightness. Our results suggest a distributed code, with no clear anatomical distinctions between auditory cortical regions responsive to changes in either pitch or timbre, but also reveal a population code that can differentiate between changes in either dimension within the same cortical regions.

Responses in early visual areas to contour integration are context dependent.

It has been shown that early visual areas are involved in contour processing. However, it is not clear how local and global context interact to influence responses in those areas, nor has the interarea coordination that yields coherent structural percepts been fully studied, especially in human observers. In this study, we used functional magnetic resonance imaging (fMRI) to measure activity in early visual cortex while observers performed a contour detection task in which alignment of Gabor elements and background clutter were manipulated. Six regions of interest (two regions, containing either the cortex representing the target or the background clutter, in each of areas V1, V2, and V3) were predefined using separate target versus background functional localizer scans. The first analysis using a general linear model showed that in the presence of background clutter, responses in V1 and V2 target regions of interest were significantly stronger to aligned than unaligned contours, whereas when background clutter was absent, no significant difference was observed. The second analysis using interarea correlations showed that with background clutter, there was an increase in V1–V2 coordination within the target regions when perceiving aligned versus unaligned contours; without clutter, however, correlations between V1 and V2 were similar no matter whether aligned contours were present or not. Both the average response magnitude and the connectivity analysis suggest different mechanisms support contour processing with or without background distractors. Coordination between V1 and V2 may play a major role in coherent structure perception, especially with complex scene organization.

The effects of orientation and attention during surround suppression of small image features: A 7 Tesla fMRI study

Although V1 responses are driven primarily by elements within a neurons receptive field, which subtends about 1° visual angle in parafoveal regions, previous work has shown that localized fMRI responses to visual elements reflect not only local feature encoding but also long-range pattern attributes. However, separating the response to an image feature from the response to the surrounding stimulus and studying the interactions between these two responses demands both spatial precision and signal independence, which may be challenging to attain with fMRI. The present study used 7 Tesla fMRI with 1.2-mm resolution to measure the interactions between small sinusoidal grating patches (targets) at 3° eccentricity and surrounds of various sizes and orientations to test the conditions under which localized, context-dependent fMRI responses could be predicted from either psychophysical or electrophysiological data. Targets were presented at 8%, 16%, and 32% contrast while manipulating (a) spatial extent of parallel (strongly suppressive) or orthogonal (weakly suppressive) surrounds, (b) locus of attention, (c) stimulus onset asynchrony between target and surround, and (d) blocked versus event-related design. In all experiments, the V1 fMRI signal was lower when target stimuli were flanked by parallel versus orthogonal context. Attention amplified fMRI responses to all stimuli but did not show a selective effect on central target responses or a measurable effect on orientation-dependent surround suppression. Suppression of the V1 fMRI response by parallel surrounds was stronger than predicted from psychophysics but showed a better match to previous electrophysiological reports.

Confidence Intervals for fMRI Activation Maps

Neuroimaging activation maps typically color voxels to indicate whether the blood oxygen level-dependent (BOLD) signals measured among two or more experimental conditions differ significantly at that location. This data presentation, however, omits information critical for interpretation of experimental results. First, no information is represented about trends at voxels that do not pass the statistical test. Second, no information is given about the range of probable effect sizes at voxels that do pass the statistical test. This leads to a fundamental error in interpreting activation maps by naïve viewers, where it is assumed that colored, “active” voxels are reliably different from uncolored “inactive” voxels. In other domains, confidence intervals have been added to data graphics to reduce such errors. Here, we first document the prevalence of the fundamental error of interpretation, and then present a method for solving it by depicting confidence intervals in fMRI activation maps. Presenting images where the bounds of confidence intervals at each voxel are coded as color allows readers to visually test for differences between “active” and “inactive” voxels, and permits for more proper interpretation of neuroimaging data. Our specific graphical methods are intended as initial proposals to spur broader discussion of how to present confidence intervals for fMRI data.