Julie A. Fiez

Common blood flow changes across visual tasks: Ii. decreases in cerebral cortex

Nine previous positron emission tomography (PET) studies of human visual information processing were reanalyzed to determine the consistency across experiments of blood flow decreases during active tasks relative to passive viewing of the same stimulus array. Areas showing consistent decreases during active tasks included posterior cingulate/precuneous (Brodmann area, BA 31/7), left (BAS 40 and 39/19) and right (BA 40) inferior parietal cortex, left dorsolateral frontal cortex (BA S), left lateral inferior frontal cortex (BA 10/47), left inferior temporal gyrus @A 20), a strip of medial frontal regions running along a dorsal-ventral axis (BAs 8, 9, 10, and 32), and the right amygdala. Experiments involving language-related processes tended to show larger decreases than nonlanguage experiments. This trend mainly reflected blood flow increases at certain areas in the passive conditions of the language experiments (relative to a fixation control in which no task stimulus was present) and slight blood flow decreases in the passive conditions of the nonlanguage experiments. When the active tasks were referenced to the fixation condition, the overall size of blood flow decreases in language and nonlanguage tasks were the same, but differences were found across cortical areas. Decreases were more pronounced in the posterior cingulate/precuneous (BAS 31/7) and right inferior parietal cortex (BA 40) during language-related tasks and more pronounced in left inferior frontal cortex (BA 10/47) during nonlanguage tasks. Blood flow decreases did not generally show significant differences across the active task states within an experiment, but a verb-generation task produced larger decreases than a read task in right and left inferior parietal lobe (BA 40) and the posterior cingulate/precuneous (BA 31/7), while the read task produced larger decreases in left lateral inferior frontal cortex (BA 10/47). These effects mirrored those found between experiments in the language-nonlanguage comparison. Consistent active minus passive decreases may reflect decreased activity caused by active task processes that generalize over tasks or increased activity caused by passive task processes that are suspended during the active tasks. Increased activity during the passive condition might reflect ongoing processes, such as unconstrained verbally mediated thoughts and monitoring of the external environment, body, and emotional state.

Cerebellum and Nonmotor Function

Does the cerebellum influence nonmotor behavior? Recent anatomical studies demonstrate that the output of the cerebellum targets multiple nonmotor areas in the prefrontal and posterior parietal cortex, as well as the cortical motor areas. The projections to different cortical areas originate from distinct output channels within the cerebellar nuclei. The cerebral cortical area that is the main target of each output channel is a major source of input to the channel. Thus, a closed-loop circuit represents the major architectural unit of cerebro-cerebellar interactions. The outputs of these loops provide the cerebellum with the anatomical substrate to influence the control of movement and cognition. Neuroimaging and neuropsychological data supply compelling support for this view. The range of tasks associated with cerebellar activation is remarkable and includes tasks designed to assess attention, executive control, language, working memory, learning, pain, emotion, and addiction. These data, along with the revelations about cerebro-cerebellar circuitry, provide a new framework for exploring the contribution of the cerebellum to diverse aspects of behavior.

Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex

Herbster et al. (1997) contribute to the growing literature on the functional neuroanatomy of word reading by evaluating stimulus-specific activation differences. The stimuli—regular words, irregular words, and nonwords—were specifically chosen to help tease apart contributions of orthography, phonology, and semantics to word pronunciation. The results, along with those from related studies [Fiez et al., 1993; Rumsey et al., 1997] have direct relevance for competing models of the transformation between orthography (how words look) and phonology (how words sound). Herbster et al. [1997] conclude that their results are consistent with connectionist models of word reading, and more specifically hypothesize that the left inferior frontal gyrus may be part of a phonological pathwaywhich supportsword reading, whereas the fusiform gyrus may be part of a semantic pathway. Zatorre et al. [1996] and Demonet et al. [1996] recently reviewed a series of neuroimaging studies that suggest the left inferior frontal gyrus is involved in phonological processing. For instance, greater activation in the left inferior frontal gyrus was found when subjects performed a phonological versus a pitch decision about pairs of auditory presented syllables [Zatorre et al., 1992], and when subjects performed a phonological versus an orthographic discrimination task on visually and auditorily presented words [Fiez et al., 1995]. Verbal working memory studies have also implicated this area in articulatory/phonological processes [e.g., see Awh et al., 1996; Paulesu et al., 1993]. However, evidence reviewed below also indicates that the left inferior frontal gyrus contributes to semantic processing. With respect to the conclusions reached by Herbster et al. [1997], this fact raises two questions: 1) How do the contributions of frontal and posterior regions (e.g., the fusiform gyrus) to semantic processing differ, and 2) are phonological versus semantic interpretations of left inferior prefrontal activation competing or complementary interpretations of the neuroimaging data?

Modulation of Caudate Activity by Action Contingency

Research has increasingly implicated the striatum in the processing of reward-related information in both animals and humans. However, it is unclear whether human striatal activation is driven solely by the hedonic properties of rewards or whether such activation is reliant on other factors, such as anticipation of upcoming reward or performance of an action to earn a reward. We used event-related functional magnetic resonance imaging to investigate hemodynamic responses to monetary rewards and punishments in three experiments that made use of an oddball paradigm. We presented reward and punishment displays randomly in time, following an anticipatory cue, or following a button press response. Robust and differential activation of the caudate nucleus occurred only when a perception of contingency existed between the button press response and the outcome. This finding suggests that the caudate is involved in reinforcement of action potentially leading to reward, rather than in processing reward per se.

Neuroimaging studies of the cerebellum: language, learning and memory

During the decade following a functional neuroimaging study of language that showed cerebellar involvement in a cognitive task, PET and fMRI studies have continued to provide evidence that the role of the cerebellum extends beyond that of motor control and that this structure contributes in some way to cognitive operations. In this review, we describe neuroimaging evidence for cerebellar involvement in working memory, implicit and explicit learning and memory, and language, and we discuss some of the problems and limitations faced by researchers who use neuroimaging to investigate cerebellar function. We also raise a set of outstanding questions that need to be addressed through further neuroimaging and behavioral experiments before differing functional accounts of cerebellar involvement in cognition can be resolved.

Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations

The goal of this research was to further our understanding of how the striatum responds to the delivery of affective feedback. Previously, we had found that the striatum showed a pattern of sustained activation after presentation of a monetary reward, in contrast to a decrease in the hemodynamic response after a punishment. In this study, we tested whether the activity of the striatum could be modulated by parametric variations in the amount of financial reward or punishment. We used an event-related fMRI design in which participants received large or small monetary rewards or punishments after performance in a gambling task. A parametric ordering of conditions was observed in the dorsal striatum according to both magnitude and valence. In addition, an early response to the presentation of feedback was observed and replicated in a second experiment with increased temporal resolution. This study further implicates the dorsal striatum as an integral component of a reward circuitry responsible for the control of motivated behavior, serving to code for such feedback properties as valence and magnitude.

Effects of Lexicality, Frequency, and Spelling-to-Sound Consistency on the Functional Anatomy of Reading

Functional neuroimaging was used to investigate three factors that affect reading performance: first, whether a stimulus is a word or pronounceable non-word (lexicality), second, how often a word is encountered (frequency), and third, whether the pronunciation has a predictable spelling-to-sound correspondence (consistency). Comparisons between word naming (reading) and visual fixation scans revealed stimulus-related activation differences in seven regions. A left frontal region showed effects of consistency and lexicality, indicating a role in orthographic to phonological transformation. Motor cortex showed an effect of consistency bilaterally, suggesting that motoric processes beyond high-level representations of word phonology influence reading performance. Implications for the integration of these results into theoretical models of word reading are discussed.

Prefrontal responses to drug cues: a neurocognitive analysis

The construct of craving has been central to addiction research for more than 50 years. Only recently have investigators begun to apply functional neuroimaging techniques to the study of drug cue reactivity, and a small but growing number of studies implicate a distributed system of brain regions in the pathogenesis of craving. The internal consistency of this burgeoning literature has thus far been disappointing, however, leaving open the question of which brain regions contribute to craving. Here we review neuroimaging studies of cue-elicited craving in the context of a framework drawn from behavioral research indicating that perceived drug use opportunity significantly affects responses to the presentation of drug cues. Using this framework provides a way to reconcile discrepant findings among brain-imaging studies of cue-elicited craving.

Pet studies of auditory and phonological processing: Effects of stimulus characteristics and task demands

Positron emission tomography (PET) was used to investigate the functional anatomy of auditory and phonological processing. Stimulus sets were designed to determine areas of the brain significantly activated during speech and nonspeech acoustic processing for stimuli with or without rapidly changing acoustic cues. Performance of auditory target detection tasks using these stimulus sets produced increased activation in superior temporal, frontal opercular, and medial frontal (SMA) cortices, relative to a visual fixation control task. While the medial frontal and superior temporal changes are best explained by motor and sensory components of the task, respectively, the frontal opercular changes were dependent upon the task performed upon the auditory input (mere presentation of the stimuli did not result in significant activation). On the left, the frontal opercular increases were larger when subjects performed an auditory detection task upon stimuli that incorporated rapid temporal changes (words, syllables, and tone sequences) than steady-state vowels. A converging study involving performance of orthographic (ascending letter) and phonological (long vowel sound) word discrimination tasks supports anatomical and behavioral evidence suggesting the left frontal opercular region is important for certain types of auditory/temporal analysis, as well as high-level articulatory coding. In addition to the activation increases associated with performance of auditory target detection tasks, decreases in activation were observed bilaterally along the intraparietal sulcus and superior parietal cortex, in the Rolandic sulcus, and the posterior cingulate; these decreases may reflect an attentional shift away from areas involved in the fixation task during the performance of a difficult auditory task. These results demonstrate that focusing more closely on basic neural processing differences (such as temporal integration rates) may lead to a better understanding of the specific neural processes that underlie complex phonological tasks.

Functional dissociations within the inferior parietal cortex in verbal working memory

Neuroimaging studies of working memory have revealed two sites in the left supramarginal gyrus that may support the short-term storage of phonological information. Activation in the left dorsal aspect of the inferior parietal cortex (DIPC) has been observed in contrasts of working memory load, whereas activation in the ventral aspect of the inferior parietal cortex (VIPC) has been found primarily in contrast of information type (verbal vs. nonverbal). Our goal was to determine whether these two areas are functionally distinct or if instead they are part of a homogeneous region with large variations in the focus of peak activity. Toward this end, we used fMRI to assess the neural response in two working memory tasks (N-back and item recognition) in which we also manipulated memory load and the type of information to be recalled (verbal vs. nonverbal). We found both DIPC and VIPC activation in the same group of subjects and further demonstrated that they have differential sensitivity to our experimental factors. Only the DIPC showed robust load effects, whereas only the VIPC showed reliable effects of information type. These results help to account for the differences observed in between-subject comparisons, and they indicate that the two regions are functionally dissociable. In contrast to the DIPC, activity of the VIPC was also recruited in the fixation and low-load conditions, a surprising result that has not been fully explored in prior studies. Despite their distinctive patterns of performance, neither of these regions displayed a pattern of activity that entirely corresponds to common assumptions of a dedicated phonological short-term store (STS). Instead, we hypothesize that the DIPC may support domain-general executive processes, while the VIPC may support phonological encoding-recoding processes central to a variety of language tasks.