Left inferior parietal cortex integrates time and space during collision judgments

Left inferior parietal lobe lesions can cause perturbation of the space-time plans underlying skilled actions. But does the perceptual integration of spatiotemporal information use the same neural substrate or is the role of the left inferior parietal cortex restricted to visuomotor transformations? We use fMRI and a collision judgment paradigm to examine whether the left inferior parietal cortex integrates temporal and spatial variables in situations in which no complex action and no visuomotor transformation is required. We used a perceptual task in which healthy subjects indicated by simple button presses whether two moving objects (of the same or different size) would or would not collide with each other. This task of interest was contrasted with a control task that employed the same stimuli and identical motor responses but in which the size of the two moving objects had to be compared. To assess putative differential eye-movement effects both tasks were performed with and without central fixation. Analysis of the fMRI data (employing a random-effects model and SPM99) showed that collision judgments (relative to size judgments) provoked a significant increase in neural activity in the left inferior parietal cortex (supramarginal gyrus) only. These results show that left inferior parietal cortex is involved in the integration of perceptual spatiotemporal information and thus provide a neural correlate for the use of space-time plans (whose perturbation can lead to apraxia as originally hypothesized by Liepmann). Furthermore, the data suggest that the left supramarginal gyrus combines temporal and spatial variables more widely than previously supposed.     

Neural Correlates of Naming Actions and of Naming Spatial Relations

Ina [¹⁵O] water PET experiment, 10 normal subjects retrieved words denoting actions (performed with or without an implement), and another 10 normal subjects retrieved words denoting the spatial relations between objects. Our objective was to test the following hypothesis: that the salient neural activity associated with naming actions and spatial relations occurs in left frontal operculum and left parietal association cortices, but not in the left inferotemporal cortices (IT) or in the right parietal association cortices. There were two control tasks, one requiring a decision on the orientation of unknown faces (a standard control task in our laboratory) and another requiring the retrieval of words denoting the concrete entities used in the action and spatial relations tasks. In accordance with the hypothesis, both naming actions and spatial relations (using the face orientation task as control activated the left frontal operculum; naming actions also activated the left parietal lobe. However, sectors of the left posterior IT were also engaged in both naming actions and spatial relations. When the naming of concrete entities was subtracted from the naming of actions performed with such entities, area MT in the posterior temporo-occipital region was activated bilaterally. On the other hand, when naming of the concrete entities was subtracted from the naming of spatial relations, left parietal activation was found, and when two tasks of naming spatial relations were contrasted to each other bilateral parietal activation was seen, right when abstract stimuli were used and left when concrete objects were used. The activity in posterior IT is thought to be related to object processing and possibly name retrieval at a subconscious level.     

Representation of manipulable man-made objects in the dorsal stream

We used fMRI to examine the neural response in frontal and parietal cortices associated with viewing and naming pictures of different categories of objects. Because tools are commonly associated with specific hand movements, we predicted that pictures of tools, but not other categories of objects, would elicit activity in regions of the brain that store information about motor-based properties. We found that viewing and naming pictures of tools selectively activated the left ventral premotor cortex (BA 6). Single-unit recording studies in monkeys have shown that neurons in the rostral part of the ventral premotor cortex (canonical F5 neurons) respond to the visual presentation of graspable objects, even in the absence of any subsequent motor activity. Thus, the left ventral premotor region that responded selectively to tools in the current study may be the human homolog of the monkey canonical F5 area. Viewing and naming tools also selectively activated the left posterior parietal cortex (BA 40). This response is similar to the firing of monkey anterior intraparietal neurons to the visual presentation of graspable objects. In humans and monkeys, there appears to be a close link between manipulable objects and information about the actions associated with their use. The selective activation of the left posterior parietal and left ventral premotor cortices by pictures of tools suggests that the ability to recognize and identify at least one category of objects (tools) may depend on activity in specific sites of the ventral and dorsal visual processing streams.     

Perceiving and naming actions and objects

Neuropsychological studies have suggested differences in the cortical representations of verbs and nouns. Assessment of word-class specific deficits often relies on picture naming with different sets of images used for action and object naming. Such a setup may be problematic in neuroimaging studies, as the perception of the image and the actual differences in retrieving verbs or nouns become intertwined. To address this issue, we investigated how different sets of images affect the pattern of activation in action and object naming. In the present fMRI experiment, healthy volunteers silently performed both action and object naming from action images, and object naming from object-only images. A similar network of cortical areas was activated in all three conditions, including bilateral occipitotemporal and parietal regions, and left frontal cortex. With action images, noun retrieval enhanced activation in bilateral parietal and right frontal cortex, areas previously associated with visual search and attention. Increased activation in the left posterior parietal cortex during this condition also suggests that naming an object in the context of action emphasizes motor-based properties of objects. Action images, regardless of whether verbs or nouns were named, evoked stronger activation than object-only images in the posterior middle temporal cortex bilaterally, the left temporo-parietal junction, and the left frontal cortex, a network previously identified in processing of action knowledge. The strong influence of perceptual input on neural activation associated with noun vs. verb naming can in part explain discrepancies in previous lesion and functional neuroimaging studies on the processing of nouns and verbs.     

Premotor Cortex Activation during Observation and Naming of Familiar Tools

Positron emission tomography was used to investigate whether observation of real objects (tools of common use) activates premotor areas in the absence of any overt motor demand. Silent naming of the presented tools and silent naming of their use were also studied. Right-handed normal subjects were employed. Tool observation strongly activated the left dorsal premotor cortex. In contrast, silent tool naming activated Broca's area without additional activity in the dorsal premotor cortex. Silent tool-use naming, in addition to activating Broca's area, increased the activity in the left dorsal premotor cortex and recruited the left ventral premotor cortex and the left supplementary motor area. These data indicate that, even in the absence of any subsequent movement, the left premotor cortex processes objects that, like tools, have a motor valence. This dorsal premotor activation, which further augments when the subject names the tool use, should reflect the neural activity related to motor schemata for object use. The presence of an activation of both dorsal premotor cortex and ventral premotor cortex during tool-use naming suggests a role for these two areas in understanding object semantics.     

The role of the dorsal stream for gesture production

Skilled gestures require the integrity of the neural networks involved in storage, retrieval, and execution of motor programs. Premotor cortex and/or parietal cortex lesions frequently produce deficits during performance of gestures, transitive more than intransitive. The dorsal stream links object information with object action, suggesting that mechanical knowledge of tool use is stored focally in the brain. Using event-related fMRI, we explored activity during instructed-delay transitive and intransitive hand gestures. The comparison between planning-preparation and execution of gestures demonstrated a temporal rostral to caudal gradient of activation in the ventral premotor cortex (PMv) and inferior to superior gradient of activation in the posterior parietal cortex (PPc). Comparison between transitive and intransitive gestures established a functional specificity within the dorsal stream for mechanical knowledge. Results demonstrate that not only PPc but also the PMv acts in the processing of sensorimotor information during gestures. This might be the substrate underlying selective deficits in ideomotor apraxia patients.     

Naming actions and objects: cortical dynamics in healthy adults and in an anomic patient with a dissociation in action/object naming

Neuropsychological studies have demonstrated that the production of nouns and verbs can be dissociated in aphasia. These reports have been taken as evidence for separate representations of nouns and verbs in the human brain. We used whole-head magnetoencephalography to record cortical dynamics of action and object naming in 10 healthy adults and in 1 anomic patient with superior naming of verbs compared with nouns due to a left posterior parietal lesion. A single set of 100 line drawings was used for both action and object naming. In normal subjects, the activation sequences in action and object naming were essentially identical, advancing from the occipital to posterior temporoparietal and further to the left frontal cortex, without consistent involvement of the classical left inferior frontal (Broca) and temporal (Wernicke) language areas. In the anomic patient, pronounced differences between action and object naming emerged in the left hemisphere. The activation sequence was disrupted at the level of the damaged parietal cortex and did not reach the left frontal cortex even in the relatively easier action naming. The more severely impaired object naming was associated with exceptionally strong and early activation of the left inferior frontal cortex (Broca) and subsequent pronounced activation of the left middle temporal cortex, silent in action naming. Verb and noun retrieval thus utilized a spatiotemporally similar neuronal network in healthy individuals. A clear dissociation in cortical correlates of verb and noun retrieval only became evident in our anomic patient, in whom damage to the language network has resulted in disproportionately worse performance in object than action naming.     

A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study

Previous studies of somatosensory object discrimination have been focused on the primary and secondary sensorimotor cortices. However, we expected the prefrontal cortex to also become involved in sequential tactile discrimination on the basis of its role in working memory and stimulus discrimination as established in other domains. To investigate the contributions of the different cerebral structures to tactile discrimination of sequentially presented objects, we obtained event-related functional magnetic resonance images from seven healthy volunteers. Our results show that right hand object exploration involved left sensorimotor cortices, bilateral premotor, parietal and temporal cortex, putamen, thalamus, and cerebellum. Tactile exploration of parallelepipeds for subsequent object discrimination activated further areas in the dorsal and ventral portions of the premotor cortex, as well as parietal, midtemporal, and occipital areas of both cerebral hemispheres. Discriminating a parallelepiped from the preceding one involved a bilateral prefrontal-anterior cingulate-superior temporal-posterior parietal circuit. While the prefrontal cortex was active with right hemisphere dominance during discrimination, there was left hemispheric prefrontal activation during the delay period between object presentations. Delay related activity was further seen in the anterior intraparietal area and the fusiform gyrus. The results reveal a prominent role of the human prefrontal cortex for somatosensory object discrimination in correspondence with recent models on stimulus discrimination and working memory.     

Neural systems underlying spatial language in American Sign Language

A [(15)O]water PET experiment was conducted to investigate the neural regions engaged in processing constructions unique to signed languages: classifier predicates in which the position of the hands in signing space schematically represents spatial relations among objects. Ten deaf native signers viewed line drawings depicting a spatial relation between two objects (e.g., a cup on a table) and were asked either to produce a classifier construction or an American Sign Language (ASL) preposition that described the spatial relation or to name the figure object (colored red). Compared to naming objects, describing spatial relationships with classifier constructions engaged the supramarginal gyrus (SMG) within both hemispheres. Compared to naming objects, naming spatial relations with ASL prepositions engaged only the right SMG. Previous research indicates that retrieval of English prepositions engages both right and left SMG, but more inferiorly than for ASL classifier constructions. Compared to ASL prepositions, naming spatial relations with classifier constructions engaged left inferior temporal (IT) cortex, a region activated when naming concrete objects in either ASL or English. Left IT may be engaged because the handshapes in classifier constructions encode information about object type (e.g., flat surface). Overall, the results suggest more right hemisphere involvement when expressing spatial relations in ASL, perhaps because signing space is used to encode the spatial relationship between objects.     

Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp?

Neuroimaging investigations reliably describe a left-lateralized network of areas as underlying the representations of knowledge about familiar tools. Among the critical 'nodes' of the network, an area centered within the left intraparietal sulcus (IPS) is thought to be related to the motoric representations associated with familiar tools and their usage. This area is in the vicinity of an area implicated in the control of object-directed grasping actions: the anterior intraparietal area, AIP. The current study aimed to evaluate whether this tool-related intraparietal activity could be accounted for by the graspable nature of tools or whether it was due to additional factors such as the functionality of tools. First, we found that during a naming task activation within a discrete region of the left anterior intraparietal cortex was higher for tools than for graspable objects, but did not differ between graspable and non-graspable objects. In addition, the peak activity associated with tool naming was found to be largely distinct and consistently posterior to that associated with real object grasping. A separate region, anterior to the tool-selective focus and possibly overlapping with AIP, demonstrated weak selectivity for both tools and graspable objects relative to non-graspable objects. These findings indicate that this tool-selective area at the anterior end of the left IPS is both separable from the grasp-related intraparietal activity and, consistently, it does not simply reflect the processing of grasping affordances. Taken together, these results suggest that object graspability alone cannot account for the left intraparietal activity driven by the naming of tools. Instead, this activity may relate to learned motor representations associated with the skillful use of familiar tools.     

Neural representations of pantomimed and actual tool use: evidence from an event-related fMRI study

Pantomime of tool use is a highly sensitive test to detect apraxia. The relationship to real-life performance is however unclear since apraxic patients frequently improve substantially when allowed to actually use tools. In the present study, the neural correlates of pantomimed and actual tool use were directly compared in healthy subjects using an event-related functional magnetic resonance imaging (fMRI) paradigm. Subjects were requested to demonstrate the use of various tools either as pantomimes or with the tool in hand. Movement and pre-movement events were evaluated. The comparison of all conditions versus rest revealed a widespread activation including parietal, posterior temporal, frontal, and subcortical areas with some characteristic activation for the different events. The direct comparison between pantomime and actual use conditions revealed no or only minor differential activations for pre-movement events. During the movement event, actual tool use induced the expected additional activation in sensory and motor areas, but also representations presumably related to tool-use knowledge at parietal, posterior temporal, and frontal sites. The opposite contrast of pantomimed versus actual tool use revealed differential activation only in the left intraparietal sulcus in a corresponding region-of-interest analysis. We conclude that planning and preparing of either pantomimed or actual tool use share large parts of a common network. Characteristic differences in the kinematics and dynamics of both movement conditions may be defined just before or during the initiation of the movement when sensory cues about the tool and environment are available in the actual use condition. Sensory and cognitive cues may provide apraxic patients the capacity to evoke a correct action program despite impaired pantomime.     

The neural correlates of spatial language in English and American Sign Language: a PET study with hearing bilinguals

Rather than specifying spatial relations with a closed-class set of prepositions, American Sign Language (ASL) encodes spatial relations using space itself via classifier constructions. In these constructions, handshape morphemes specify object type, and the position of the hands in signing space schematically represents the spatial relation between objects. A [15O]water PET study was conducted to investigate the neural regions engaged during the production of English prepositions and ASL locative classifier constructions in hearing subjects with deaf parents (ASL-English bilinguals). Ten subjects viewed line drawings depicting a spatial relation between two objects and were asked to produce either an ASL locative classifier construction or an English preposition that described the spatial relation. The comparison task was to name the figure object (colored red) in either ASL or in English. Describing spatial relations in either ASL or English engaged parietal cortex bilaterally. However, an interaction analysis revealed that right superior parietal cortex was engaged to a greater extent for ASL than for English. We propose that right parietal cortex is involved in the visual-motoric transformation required for ASL. The production of both English prepositions and ASL nouns engaged Broca's area to a greater extent than ASL classifier constructions. We suggest that Broca's area is not engaged because these constructions do not involve retrieval of the name of an object or the name of a spatial relation. Finally, under the same task conditions, only left parietal activation was observed for monolingual English speakers producing spatial prepositions (H. Damasio et al., 2001, NeuroImage, 13). We conclude that the right hemisphere activation observed for ASL-English bilinguals was due to their life-long experience with spatial language in ASL.     

Language switching and language representation in Spanish-English bilinguals: an fMRI study

The current experiment was designed to investigate the nature of cognitive control in within- and between-language switching in bilingual participants. To examine the neural substrate of language switching we used functional magnetic resonance imaging (fMRI) as subjects named pictures in one language only or switched between languages. Participants were also asked to name (only in English) a separate set of pictures as either the actions or the objects depicted or to switch between these two types of responses on each subsequent picture. Picture naming compared to rest revealed activation in the dorsolateral prefrontal cortex, which extended down into Broca's area in the left hemisphere. There were no differences in the activation pattern for each language. English and Spanish both activated overlapping areas of the brain. Similarly, there was no difference in activation for naming actions or objects in English. However, there was increased intensity of activation in the dorsolateral prefrontal cortex for switching between languages relative to no-switching, an effect which was not observed for naming of actions or objects in English. We suggest that the dorsolateral prefrontal cortex serves to attenuate interference that results from having to actively enhance and suppress two languages in alternation. These results are consistent with the view that switching between languages involves increased general executive processing. Finally, our results are consistent with the view that different languages are represented in overlapping areas of the brain in early bilinguals.     

Pantomime of object use: a challenge to cerebral localization of cognitive function

The paper illustrates difficulties and insecurities of localizing cognitive functions with the example of pantomime of object use. Numerous studies have established a particular sensitivity of this task to left brain damage (LBD), but there is no agreement as to how components of its cognitive architecture are related to the laterality and intrahemispheric location of responsible lesions. Apraxia and asymbolia have been suspected to be crucial for explaining the vulnerability of pantomime to LBD, but analysis of correlations between impairments of pantomime, imitation of gestures, drawing from memory, and language in patients with LBD and aphasia suggests that neither of these putative deficits can adequately account for the data. It rather appears that pantomime taps a central aspect of left hemisphere function which affects performance on a great number of otherwise widely different tasks and which is not bound to any particular location within the hemisphere. I discuss ways to resolve apparent conflicts between this interpretation and the findings of double dissociations between pantomime and imitation in clinical case studies and of circumscribed left parietal activation during pantomime in functional neuroimaging.     

Objects and their actions: evidence for a neurally distributed semantic system

An influential model of conceptual knowledge claims that objects are represented in a distributed network of cortical areas that store information about different types of attributes, such as form, colour, and motion (A. Martin et al., 2000, in: The Cognitive Neurosciences, 2nd ed., MIT Press, Cambridge). Two specific claims of this account are that (a) the motions and actions associated with objects (along with other attributes) are automatically activated whenever the object concept is evoked and (b) topographically distinct neural regions are responsible for motion/action attributes pertaining to objects in the categories of tools and animals. We used fMRI to examine the neural activation associated with conceptual processing of nouns referring to animals and tools and for verbs referring to tool-associated actions (e.g., drilling, painting) and biological actions (e.g., walking, jumping). We found that object names and their associated actions activated the same set of neural regions (left fusiform gyrus, superior and middle temporal cortex) consistent with the claim that word tool and animal concepts implicitly activate the actions associated with them. However, there was no evidence of category specificity for either objects or actions, with essentially the same activations for the form and motion attributes of both living and nonliving categories.     

What vs. where in touch: an fMRI study

Two streams have been identified in cortical visual processing: a ventral stream for form, color, and features, and a dorsal stream for spatial characteristics and motion. We investigated whether similar "what" and "where" dissociations of function exist for human somatosensory processing. Using identical stimuli and hand movements, subjects either performed tactile object recognition (TOR) and ignored location or performed tactile object localization (LOC) and ignored identity. A matched-movement control task separated activation associated with sensorimotor input from higher-level cognitive contributions. Results confirmed separate processing streams for TOR and LOC. TOR activated the frontal pole as well as bilateral inferior parietal and left prefrontal regions involved in tactile feature integration and naming. LOC activated bilateral superior parietal areas involved in spatial processing. The dissociation of object and spatial processing streams appears to be a modality general organizational principle in the brain.     

Three distinct ventral occipitotemporal regions for reading and object naming.

This study investigates word and object processing during naming and viewing tasks and identifies three distinct regions in the left ventral occipitotemporal cortex. Irrespective of task, words and objects (relative to meaningless visual controls) activated the medial surface of the left anterior fusiform gyrus, a region that has previously been associated with semantic knowledge. A more lateral region was differentially active for naming words and objects relative to viewing the same stimuli and a more posterior region was differentially active for objects relative to words irrespective of task. In addition, we found that word processing resulted in greater activation than object processing on the dorsal surface of the left superior temporal gyrus and the left supramarginal gyrus. These regions appear to be important for converting orthography into phonology; their response to words irrespective of task is consistent with established psychological evidence that implicit phonological processing is stronger for words than objects.     

Hemispheric asymmetry emerges at distinct parts of the occipitotemporal cortex for objects, logograms and phonograms: a functional MRI study

Behavioral and neuropsychological studies have suggested that the right hemisphere has a special advantage in the visual recognition of logograms. While this long-standing 'right hemisphere hypothesis' has never been investigated systematically by previous neuroimaging studies, a candidate neural substrate of such asymmetry might be found within the occipitotemporal cortex that is known to exhibit lateralized response to a certain class of stimuli, such as letters and faces. The present study examined the hemispheric specialization of brain activation during naming of objects, logograms and phonograms using functional magnetic resonance imaging. The three types of stimuli overall produced left-predominant activation of the perisylvian and inferior parietal regions relative to the resting baseline. This inter-hemispheric difference was significant irrespective of the stimuli type. In the occipitotemporal cortex, six subregions showing lateralized response were identified. That is, the three stimuli commonly produced left-lateralized response in the posterior fusiform and superior temporal gyri and right-lateralized response in the extrastriate cortex. Only logograms and objects produced a distinct cluster showing right-lateralized activation in the medial anterior fusiform gyrus associated with semantic knowledge, whereas only phonograms produced a left-lateralized activation in the posterior middle temporal cortex close to the site associated with visual perception of alphabetical letters. These findings suggest that while these stimuli similarly recruit the left perisylvian language area as a common neural component for naming, processing of objects and logograms becomes left-lateralized only in the downstream of the occipitotemporal cortex. By contrast, visual processing of phonograms is specialized to the left hemisphere in earlier stages of the area. The present data provide further evidence suggesting that both the left-right and anterior-posterior axes of the occipitotemporal cortex are differentially tuned according to the specific features of visual stimuli.     

Neural representation of observed actions in the parietal and premotor cortex

We investigated the neural representation of observed actions in the human parietal and premotor cortex, which comprise the action observation network or the mirror neuron system for action recognition. Participants observed object-directed hand actions, in which action as well as other properties were independently manipulated: action (grasp or touch), object (cup or bottle), perspective (1st or 3rd person), hand (right or left), and image size (large or small). We then used multi-voxel pattern analysis to determine whether each feature could be correctly decoded from regional activities. The early visual area showed significant above-chance classification accuracy, particularly high in perspective, hand, and size, consistent with pixel-wise dissimilarity of stimuli. In contrast, the highest decoding accuracy for action was observed in the anterior intraparietal sulcus (aIPS) and the ventral premotor cortex (PMv). Moreover, the decoder for action could be correctly generalized for images with high dissimilarity in the parietal and premotor region, but not in the visual area. Our study indicates that the parietal and premotor regions encode observed actions independent of retinal variations, which may subserve our capacity for invariant action recognition of others.