Joseph T. Devlin

The myth of the visual word form area

Recent functional imaging studies have referred to a posterior region of the left midfusiform gyrus as the visual word form area (VWFA). We review the evidence for this claim and argue that neither the neuropsychological nor neuroimaging data are consistent with a cortical region specialized for visual word form representations. Specifically, there are no reported cases of pure alexia who have deficits limited to visual word form processing and damage limited to the left midfusiform. In addition, we present functional imaging data to demonstrate that the so-called VWFA is activated by normal subjects during tasks that do not engage visual word form processing such as naming colors, naming pictures, reading Braille, repeating auditory words, and making manual action responses to pictures of meaningless objects. If the midfusiform region has a single function that underlies all these tasks, then it does not correspond to visual word form processing. On the other hand, if the region participates in several functions as defined by its interactions with other cortical areas, then identifying the neural system sustaining visual word form representations requires identification of the set of regions involved. We conclude that there is no evidence that visual word form representations are subtended by a single patch of neuronal cortex and it is misleading to label the left midfusiform region as the visual word form area.

Semantic Processing in the Left Inferior Prefrontal Cortex: A Combined Functional Magnetic Resonance Imaging and Transcranial Magnetic Stimulation Study

The involvement of the left inferior prefrontal cortex (LIPC) in phonological processing is well established from both lesion-deficit studies with neurological patients and functional neuroimaging studies of normals. Its involvement in semantic processing, on the other hand, is less clear. Although many imaging studies have demonstrated LIPC activation during semantic tasks, this may be due to implicit phonological processing. This article presents two experiments investigating semantic functions in the LIPC. Results from a functional magnetic resonance imaging experiment demonstrated that both semantic and phonological processing activated a common set of areas within this region. In addition, there was a reliable increase in activation for semantic relative to phonological decisions in the anterior LIPC while the opposite comparison (phonological vs. semantic decisions) revealed an area of enhanced activation within the posterior LIPC. A second experiment used transcranial magnetic stimulation (TMS) to temporarily interfere with neural information processing in the anterior portion of the LIPC to determine whether this region was essential for normal semantic performance. Both repetitive and single pulse TMS significantly slowed subjects reactions for the semantic but not for the perceptual control task. Our results clarify the functional anatomy of the LIPC by demonstrating that anterior and posterior regions contribute to both semantic and phonological processing, albeit to different extents. In addition, the findings go beyond simply establishing a correlation between semantic processing and activation in the LIPC and demonstrate that a transient disruption of processing selectively interfered with semantic processing.

The left parietal and premotor cortices: motor attention and selection.

It is well established that the premotor cortex has a central role in the selection of movements. The role of parts of the parietal cortex in movement control has proved more difficult to describe but appears to be related to the preparation and the redirection of movements and movement intentions. We have referred to some of these processes as motor attention. It has been known since the time of William James that covert motor attention can be directed to an upcoming movement just as visuospatial attention can be directed to a location in space. While some parietal regions, particularly in the right hemisphere, are concerned with covert orienting and the redirecting of covert orienting it may be useful to consider other parietal regions, in the anterior inferior parietal lobule and in the posterior superior parietal lobule, particularly in the left hemisphere, as contributing to motor attention. Such parts of the parietal lobe are activated in neuroimaging experiments when subjects covertly prepare movements or switch intended movements. Lesions or transcranial magnetic stimulation (TMS) affect the redirecting of motor attention. The difficulties apraxic patients experience when sequencing movements may partly be due to an inability to redirect motor attention from one movement to another. The role of the premotor cortex in selecting movements is also lateralized to the left hemisphere. Damage to left hemisphere movement selection mechanisms may also contribute to apraxia. If, however, it remains intact after a stroke then the premotor cortex may contribute to the recovery of arm movements. A group of patients with unilateral left hemisphere lesions and impaired movements in the contralateral right hand was studied. Functional magnetic resonance imaging showed that in some cases the premotor cortex in the intact hemisphere was more active when the stroke-affected hand was used. TMS in the same area in the same patients had the most disruptive effect on movements. In summary, patterns of motor impairment and recovery seen after strokes can partly be explained with reference to the roles of the parietal and premotor cortices in motor attention and selection.

Interactions between decision making and performance monitoring within prefrontal cortex.

Our ability to judge the consequences of our actions is central to rational decision making. A large body of evidence implicates primate prefrontal regions in the regulation of this ability. It has proven extremely difficult, however, to separate functional areas in the frontal lobes. Using functional magnetic resonance imaging, we demonstrate complementary and reciprocal roles for the human orbitofrontal (OFC) and dorsal anterior cingulate cortices (ACd) in monitoring the outcome of behavior. Activation levels in these regions were negatively correlated, with activation increasing in the ACd and decreasing in the OFC when the selected response was the result of the participants own decision. The pattern was reversed when the selected response was guided by the experimenter rather than the participant. These results indicate that the neural mechanisms underlying the way we assess the consequences of choices differ depending on whether we are told what to do or are able to exercise our volition.

Language Control in the Bilingual Brain

How does the bilingual brain distinguish and control which language is in use? Previous functional imaging experiments have not been able to answer this question because proficient bilinguals activate the same brain regions irrespective of the language being tested. Here, we reveal that neuronal responses within the left caudate are sensitive to changes in the language or the meaning of words. By demonstrating this effect in populations of German-English and Japanese-English bilinguals, we suggest that the left caudate plays a universal role in monitoring and controlling the language in use.

The Role of the Posterior Fusiform Gyrus in Reading

Studies of skilled reading [Price, C. J., & Mechelli, A. Reading and reading disturbance. Current Opinion in Neurobiology, 15, 231238, 2005], its acquisition in children [Shaywitz, B. A., Shaywitz, S. E., Pugh, K. R., Mencl, W. E., Fulbright, R. K., Skudlarski, P., et al. Disruption of posterior brain systems for reading in children with developmental dyslexia. Biological Psychiatry, 52, 101110, 2002; Turkeltaub, P. E., Gareau, L., Flowers, D. L., Zeffiro, T. A., & Eden, G. F. Development of neural mechanisms for reading. Nature Neuroscience, 6, 767773, 2003], and its impairment in patients with pure alexia [Leff, A. P., Crewes, H., Plant, G. T., Scott, S. K., Kennard, C., & Wise, R. J. The functional anatomy of single word reading in patients with hemianopic and pure alexia. Brain, 124, 510521, 2001] all highlight the importance of the left posterior fusiform cortex in visual word recognition. We used visual masked priming and functional magnetic resonance imaging to elucidate the specific functional contribution of this region to reading and found that (1) unlike words, repetition of pseudowords (solst-solst) did not produce a neural priming effect in this region, (2) orthographically related words such as corner-corn did produce a neural priming effect, but (3) this orthographic priming effect was reduced when prime-target pairs were semantically related (teacher-teach). These findings conflict with the notion of stored visual word forms and instead suggest that this region acts as an interface between visual form information and higher order stimulus properties such as its associated sound and meaning. More importantly, this function is not specific to reading but is also engaged when processing any meaningful visual stimulus.

Anatomic constraints on cognitive theories of category specificity.

Many cognitive theories of semantic organization stem from reports of patients with selective, category-specific deficits for particular classes of objects (e.g., fruit). The anatomical assumptions underlying the competing claims can be evaluated with functional neuroimaging but the findings to date have been inconsistent and insignificant when standard statistical criteria are adopted. We hypothesized that category differences in functional brain responses might be small and task dependent. To test this hypothesis, we entered data from seven PET studies into a single multifactorial design which crossed category (living vs man-made) with a range of tasks. Reliable category-specific effects were observed but only for word retrieval and semantic decision tasks. Living things activated medial aspects of the anterior temporal poles bilaterally while tools activated a left posterior middle temporal region. These category-by-task interactions provide robust evidence for an anatomical double dissociation according to category and place strong constraints on cognitive theories of the semantic system. Furthermore they reconcile some of the apparent inconsistencies between lesion studies and functional neuroimaging data.

In praise of tedious anatomy

Functional neuroimaging is fundamentally a tool for mapping function to structure, and its success consequently requires neuroanatomical precision and accuracy. Here we review the various means by which functional activation can be localised to neuroanatomy and suggest that the gold standard should be localisation to the individuals or groups own anatomy through the use of neuroanatomical knowledge and atlases of neuroanatomy. While automated means of localisation may be useful, they cannot provide the necessary accuracy, given variability between individuals. We also suggest that the field of functional neuroimaging needs to converge on a common set of methods for reporting functional localisation including a common standard space and criteria for what constitutes sufficient evidence to report activation in terms of Brodmanns areas.

Meta-analyses of object naming: Effect of baseline

The neural systems sustaining object naming were examined using the activation likelihood estimation (ALE) meta‐analysis approach on the results of 16 previously published studies. The activation task in each study required subjects to name pictures of objects or animals, but the baseline tasks varied. Separate meta‐analyses were carried out on studies that used: (1) high‐level baselines to control for speech processing and visual input; and (2) low‐level baselines that did not control for speech or complex visual processing. The results of the two meta‐analyses were then compared directly, revealing a double dissociation in the activation pattern for studies using high and low baselines. To interpret the differential activations, we report two new functional imaging experiments. The aim of the first was to characterize activation differences associated with visual stimuli that are typically used in baseline conditions (complex visual features, simple structures, or fixation). The aim of the second was to classify object‐naming regions in terms of whether they were engaged preferentially by semantic or phonological processes. The results reveal a remarkably precise correspondence between the areas identified by the meta‐analyses as affected differentially by baseline and the areas that are affected differentially by non‐object structure, semantics or phonology. As expected, high‐level baselines reduced object‐naming activation in areas associated with the processing of complex visual features and speech production. In addition, high‐level baselines increased sensitivity to activation in areas associated with semantic processing, visual‐speech integration and response selection. For example, activation in the anterior temporal areas that neuropsychological studies have associated with semantic processing was more strongly activated in the context of high‐level baselines. These results therefore have implications for understanding the convergence of functional imaging and neuropsychological findings. Hum Brain Mapp 25:70–82, 2005.

Directing spatial attention in mental representations: Interactions between attentional orienting and working-memory load.

Orienting spatial attention to locations in the extrapersonal world has been intensively investigated during the past decades. Recently, it was demonstrated that it is also possible to shift attention to locations within mental representations held in working memory. This is an important issue, since the allocation of our attention is not only guided by external stimuli, but also by their internal representations and the expectations we build upon them. The present experiment used behavioural measures and event-related functional magnetic resonance imaging to investigate whether spatial orienting to mental representations can modulate the search and retrieval of information from working memory, and to identify the neural systems involved, respectively. Participants viewed an array of coloured crosses. Seconds after its disappearance, they were cued to locations in the array with valid or neutral cues. Subsequently, they decided whether a probe stimulus was presented in the array. The behavioural results indicated that orienting of spatial attention within working memory attenuates the well-known effect of decreasing performance when memory load is increased. So internal spatial orienting seems to highlight information or facilitate search within working memory, which leads to advantages in retrieval. Imaging enabled the separation of brain areas supporting spatial orienting functions from those sensitive to working-memory load. Orienting of spatial attention to the contents of working memory activated posterior parietal cortex bilaterally, the insula, and lateral and medial frontal cortices.