Passive reading and motor imagery about hand actions and tool-use actions: an fMRI study

Recent studies have shown that motor activations in action verb comprehension can be modulated by task demands (e.g., motor imagery vs. passive reading) and the specificity of action verb meaning. However, how the two factors work together to influence the involvement of the motor system during action verb comprehension is still unclear. To address the issue, the current study investigated the brain activations in motor imagery and passive reading of verbs about hand actions and tool-use actions. Three types of Chinese verbs were used, including hand-action verbs and two types of tool-use verbs emphasizing either the hand or tools information. Results indicated that all three types of verbs elicited common activations in hand motor areas during passive reading and motor imagery. Contrast analyses showed that in the hand verbs and the tool verbs where the hand information was emphasized, motor imagery elicited stronger effects than passive reading in the superior frontal gyrus, supplemental motor area and cingulate cortex that are related to motor control and regulation. For tool-use verbs emphasizing tools information, the motor imagery task elicited stronger activity than passive reading in occipital regions related to visual imagery. These results suggest that motor activations during action verb comprehension can be modulated by task demands and semantic features of action verbs. The sensorimotor simulation during language comprehension is flexible and determined by the interactions between linguistic and extralinguistic contexts.     

Observation of static gestures influences speech production

Research investigating ‘mirror neurons’ has demonstrated the presence of an observation–execution matching system in humans. One hypothesized role for this system might be to aid in action understanding by encoding the underlying intentions of the actor. To investigate this hypothesis, we asked participants to observe photographs of an actor making orofacial gestures (implying verbal or non-verbal acts), and to produce syllables that were compatible or incompatible with the gesture they observed. We predicted that if mirror neurons encode the intentions of an actor, then the pictures implying verbal gestures would affect speech production, whereas the non-verbal gestures would not. Our results showed that the observation of compatible verbal gestures facilitated verbal responses, while incompatible verbal gestures caused interference. Although this compatibility effect did not reach statistical significance when the photographs implied a non-verbal act, responses were faster on average when the gesture implied the use of similar articulators as those involved with the production of the target syllable. Altogether, these behavioral findings compliment previous neuroimaging studies indicating that static pictures portraying gestures activate brain regions associated with an observation–execution matching system.     

Brain activation during encoding and recognition of verbal and figural information in older adults

Positron emission tomography (PET) patterns of cerebral blood flow associated with verbal and figural memory are described in relation to their value as functional probes for studying longitudinal changes that occur in the aging brain. Relative to a matching control task, verbal and figural encoding increase blood flow in prefrontal cortex (PFC), anterior cingulate, insular, lateral and medial temporal, occipital cortex and the cerebellum. Additionally, medial temporal regions exhibited greater activity during figural encoding relative to verbal encoding. During recognition, blood flow increases in prefrontal, cingulate, insular, and lateral temporal and Broca's areas. Analysis of hemispheric asymmetry reveals that the prefrontal cortex exhibits regionally dependent results. Prefrontal region BA 10 demonstrates more bilateral activation during encoding and retrieval, whereas BA 46 shows right greater than left activation during both encoding and retrieval. Overall, the two tasks activate diverse regions within the frontal, temporal and occipital lobes of the brain, including areas that show age-related structural changes, proving their usefulness in the longitudinal assessment of brain function in the elderly.     

Sensory-motor interference abolishes repetition priming for observed actions,but not for action-related verbs

Several studies on humans have shown a recruitment of the sensory-motor system in the perception of action-related visual and verbal material, suggesting that actions are represented through sensory-motor processes. To date, these studies have not disentangled whether such a recruitment is epiphenomenal or necessary to action representation. Here we took advantage of repetition priming as a tool to investigate the cognitive representation of actions, and systematically looked whether a concurrent motor or verbal task had a detrimental effect on this representation. In a first experiment participants discriminated images depicting meaningless and meaningful actions, while performing either a concurrent sensory-motor or an articulatory suppression task. Images were classified as depicting a repeated or a new action, relative to the previous image in the trial series. We found a facilitation by repetition priming, that was unaffected by the articulatory task but was completely abolished by the sensory-motor task. In a second experiment, we investigated whether the sensory-motor system is also causally involved in processing action-related verbs. In this experiment actions were presented as written infinitive verbs rather than as images. The facilitation by repetition priming was again unaffected by the concurrent articulatory task, while the sensory-motor concurrent task, although reducing the facilitation, did not abolish it. Our data provide evidence that the sensory-motor system is differentially involved during visual processing of actions and during processing of action-related verbs. Results are discussed within the theoretical frame of embodied cognition.     

THE NOUN/VERB DISSOCIATION IN LANGUAGE PRODUCTION: VARIETIES OF CAUSES

Abstract

We report the performance of two patients who presented with complementary deficits in naming nouns relative to verbs: EA performed far worse with nouns than verbs, while MR performed worse with verbs than nouns. The two patients' grammatical category-specific deficits could not easily be explained in terms of damage to specific types of semantic knowledge prototypically associated with nouns (visual properties) and verbs (action features). One of the two patients, MR, also presented with a selective deficit in processing verbal as opposed to nominal morphology, in line with her impairment in naming verbs. The other patient, EA, showed no impairment in producing nominal and regular verbal morphology. The contrasting patterns of grammatical category-specific deficits in naming and morphological processing, along with other recently reported patterns, are interpreted as providing support for the claim that semantic and grammatical properties independently contribute to the organisation of lexical processes in the brain.     

The noun/verb dissociation in language production: varieties of causes

We report the performance of two patients who presented with complementary deficits in naming nouns relative to verbs: EA performed far worse with nouns than verbs, while MR performed worse with verbs than nouns. The two patients' grammatical category-specific deficits could not easily be explained in terms of damage to specific types of semantic knowledge prototypically associated with nouns (visual properties) and verbs (action features). One of the two patients, MR, also presented with a selective deficit in processing verbal as opposed to nominal morphology, in line with her impairment in naming verbs. The other patient, EA, showed no impairment in producing nominal and regular verbal morphology. The contrasting patterns of grammatical category-specific deficits in naming and morphological processing, along with other recently reported patterns, are interpreted as providing support for the claim that semantic and grammatical properties independently contribute to the organisation of lexical processes in the brain.     

Verbal paired-associate learning by APOE genotype in non-demented older adults: fMRI evidence of a right hemispheric compensatory response

Previous studies of episodic memory report a greater extent of blood-oxygenation-level-dependent (BOLD) response in non-demented older adults with the apolipoprotein E epsilon-4 (APOE epsilon4) allele than in those without the allele. We conducted a functional MRI study to investigate whether APOE genotype is related to brain response to verbal paired-associate encoding and consolidation, particularly in the right hemisphere, among non-demented older adults. Structurally segmented volumes and BOLD response were measured in 13 non-epsilon4 and 12 epsilon4 subjects. The epsilon4 group displayed greater activation than the non-epsilon4 group in multiple right hemisphere regions for previously encoded word pairs relative to fixation. Activation within manually outlined hippocampal regions of interest also displayed genotype-specific dissociations consistent with whole brain analyses. Furthermore, this differential BOLD response occurred in the presence of equivalent behavioral and neuropsychological performances as well as comparable hippocampal and overall structural segmentation volumes between groups. Results implicate a widely distributed and interconnected network of right hemisphere brain regions that may be involved in compensating for APOE epsilon4-related deficiencies associated with verbal episodic memory encoding and consolidation.     

Mirror neurons and intention understanding: Dissociating the contribution of object type and intention to mirror responses using electromyography

Since their discovery in the monkey and human brain, mirror neurons have been claimed to play a key role in understanding others' intentions. For example, “action‐constrained” mirror neurons in inferior parietal lobule fire when the monkey observes a grasping movement that is followed by an eating action, but not when it is followed by a placing action. It is claimed these responses enable the monkey to predict the intentions of the actor. These findings have been replicated in human observers by recording electromyography responses of the mouth‐opening mylohyoid muscle during action observation. Mylohyoid muscle activity was greater during the observation of actions performed with the intention to eat than of actions performed with the intention to place, again suggesting an ability to predict the actor's intentions. However, in previous studies, intention was confounded with object type (food for eating actions, nonfood for placing actions). We therefore used electromyography to measure mylohyoid activity in participants observing eating and placing actions. Unlike previous studies, we used a design in which each object (food, nonfood) could be both eaten and placed, and thus participants could not predict the actor's intention at the onset of the action. Greater mylohyoid activity was found for the observation of actions performed on food objects, irrespective of intention, indicating that the object type, not the actor's intention, drives the mirror response. This result suggests that observers' motor responses during action observation reflect the presence of a particular object, rather than the actor's underlying intentions.     

Neural basis for the processes that underlie visually guided and internally guided force control in humans

Despite an intricate understanding of the neural mechanisms underlying visual and motor systems, it is not completely understood in which brain regions humans transfer visual information into motor commands. Furthermore, in the absence of visual information, the retrieval process for motor memory information remains unclear. We report an investigation where visuomotor and motor memory processes were separated from only visual and only motor activation. Subjects produced precision grip force during a functional MRI (fMRI) study that included four conditions: rest, grip force with visual feedback, grip force without visual feedback, and visual feedback only. Statistical and subtractive logic analyses segregated the functional process maps. There were three important observations. First, along with the well-established parietal and premotor cortical network, the anterior prefrontal cortex, putamen, ventral thalamus, lateral cerebellum, intermediate cerebellum, and the dentate nucleus were directly involved in the visuomotor transformation process. This activation occurred despite controlling for the visual input and motor output. Second, a detailed topographic orientation of visuomotor to motor/sensory activity was mapped for the premotor cortex, parietal cortex, and the cerebellum. Third, the retrieval of motor memory information was isolated in the dorsolateral prefrontal cortex, ventral prefrontal cortex, and anterior cingulate. The motor memory process did not extend to the supplementary motor area (SMA) and the basal ganglia. These findings provide evidence in humans for a model where a distributed network extends over cortical and subcortical regions to control the visuomotor transformation process used during visually guided tasks. In contrast, a localized network in the prefrontal cortex retrieves force output from memory during internally guided actions.     

Involvement of the Motor System in Comprehension of Non-Literal Action Language: A Meta-Analysis Study

Although numerous studies have shown that the sensory-motor system is involved in semantic processing of language stimuli, it is still unclear whether comprehension of abstract concepts is embodied, and whether the involvement of the sensory-motor system is context-dependent. Investigation of how the motor system is activated during comprehension of non-literal action languages can help address these issues. So far several studies have reported brain activations during non-literal action language comprehension, but the findings are highly inconsistent because of different types of non-literal action language stimuli. To clarify how the motor system is involved in comprehension of different types of non-literal languages, the current study conducted quantitative meta-analyses on fMRI findings about comprehension of sentences describing fictive motions, metaphoric actions, and idiomatic actions. Results showed that fictive motion sentences elicited activation in the right parahippocampal gyrus, an area important for spatial processing. For metaphoric actions, the left precentral gyrus (BA 6) was strongly activated, suggesting a link between metaphoric and literal meanings. For idiomatic actions, activity was found in the left inferior frontal gyrus (BA 44/45), highlighting semantic selection and inhibition. No premotor or motor activity was found in idiom condition. These results together suggest that the involvement of the sensory-motor system in abstract concepts processing is flexible, depending on semantic features of the language stimuli and links between abstract and literal meanings.     

Cerebellar involvement in verb generation: an fMRI study

A possible role of the human cerebellum in the generation of verbs corresponding to presented nouns has been suggested. Previous functional brain imaging studies have compared generation of verbs with the reading of nouns as a measure of verb generation. In the present fMRI study involving healthy human subjects, the effects of speech articulation and motor imagery associated with verb production were investigated in greater detail. Generation of verbs to visually presented nouns was compared to a condition in which subjects read those same verbs that had been individually generated by each subject. Activation in lobule HVI/Crus I of the right cerebellar hemisphere was found as a measure of verb generation. In contrast, reading of verbs as a measure of speech articulation evoked cerebellar activations in both left and right paravermal lobule VI. These results suggest an involvement of the right lateral cerebellar hemisphere in linguistic functions during verb generation. Alternatively, effects of inner speech could also possibly explain the results.     

Neural regions essential for writing verbs

Functional imaging data collected during cognitive tasks show which brain regions are active during those tasks, but do not necessarily indicate which regions are essential for those tasks. Here, in a study of two cases of selectively impaired written naming of verbs after focal brain ischemia, we combined imaging and behavioral testing to unambiguously identify brain regions that are crucial for a specific cognitive process. We used magnetic resonance perfusion imaging to show that the selective impairment in each case was due to hypoperfusion (low blood flow) in left posterior inferior frontal gyrus (PIFG) and precentral gyrus (PrG); the impairment was immediately reversed when blood flow was restored to these regions, indicating that parts of the left frontal lobe are crucial for representing and processing verbs.     

The effects of a recency task on the left and right hand tapping performance

The intrahemispheric overflow hypothesis was examined by the cognitive-motor interference method. Subjects were 12 right handed male adults. As the concurrent cognitive task the present study employed Milner's recent-memory (verbal and nonverbal) task which was assumed by the author to be related to the frontal lobe function. The motor task was a single finger repetitive tapping, which control is thought to involve the motor area in the anterior regions of the hemispheres. In verbal material, general interference occurred during both encoding and decoding periods. In nonverbal material, however, recency task interfered with the left hand during decoding period only when the load effect was maximum. The result indicated that even if there were no functional overlap, interference could occur by neural overflow.     

(Don't) Mind the effort: Effects of contextual interference on ERP indicators of motor preparation

Motor learning is associated with a decrease in frontal control‐related brain activity and increase of central and parietal motor‐related activity. Contextual interference (CI), manipulated typically by blocked versus randomized training schedules, affects motor learning, resulting in inferior performance during training but in superior performance during retention and transfer. The CI effect is often explained by increased processing demands under high CI training. Consistently, in the motor preparation phase, the activity of control‐ and attention‐related brain areas is increased under high CI. Here, we investigated the effect of CI on learning‐related changes in ERPs during motor preparation. Participants learned throwing at virtual targets and were tested for retention in the target condition 1 week later. The frontal P3 component decreased with learning during the first session and across sessions. In addition, there was a trend for a stronger reduction of P3 during retention after high CI training. Both initial and late contingent negative variation (iCNV and lCNV) amplitudes decreased with learning and showed a significantly stronger reduction under high CI. We conclude that CI modulates the interplay of cognitive and motor processes in the preparatory phase of motor learning and that a stronger involvement of cognitive processes during high CI training accounts for differential effects of CI on ERP indicators of motor preparation during retention.     

Neuronal substrates of haptic shape encoding and matching: a functional magnetic resonance imaging study

We used functional magnetic resonance imaging to differentiate cerebral areas involved in two different dimensions of haptic shape perception: encoding and matching. For this purpose, healthy right-handed subjects were asked to compare pairs of complex 2D geometrical tactile shapes presented in a sequential two-alternative forced-choice task. Shape encoding involved a large sensorimotor network including the primary (SI) and secondary (SII) somatosensory cortex, the anterior part of the intraparietal sulcus (IPA) and of the supramarginal gyrus (SMG), regions previously associated with somatosensory shape perception. Activations were also observed in posterior parietal regions (aSPL), motor and premotor regions (primary motor cortex (MI), ventral premotor cortex, dorsal premotor cortex, supplementary motor area), as well as prefrontal areas (aPFC, VLPFC), parietal-occipital cortex (POC) and cerebellum. We propose that this distributed network reflects construction and maintenance of sensorimotor traces of exploration hand movements during complex shape encoding, and subsequent transformation of these traces into a more abstract shape representation using kinesthetic imagery. Moreover, haptic shape encoding was found to activate the left lateral occipital complex (LOC), thus corroborating the implication of this extrastriate visual area in multisensory shape representation, besides its contribution to visual imagery. Furthermore, left hemisphere predominance was shown during encoding, whereas right hemisphere predominance was associated with the matching process. Activations of SI, MI, PMd and aSPL, which were predominant in the left hemisphere during the encoding, were shifted to the right hemisphere during the matching. In addition, new activations emerged (right dorsolateral pre-frontal cortex, bilateral inferior parietal lobe, right SII) suggesting their specific involvement during 2D geometrical shape matching.     

Functional connectivity reveals load dependent neural systems underlying encoding and maintenance in verbal working memory

One of the main challenges in working memory research has been to understand the degree of separation and overlap between the neural systems involved in encoding and maintenance. In the current study we used a variable load version of the Sternberg item recognition test (two, four, six, or eight letters) and a functional connectivity method based on constrained principal component analysis to extract load-dependent neural systems underlying encoding and maintenance, and to characterize their anatomical overlap and functional interaction. Based on the pattern of functional connectivity, constrained principal component analysis identified a load-dependent encoding system comprising bilateral occipital (Brodmann's area (BA) 17, 18), bilateral superior parietal (BA 7), bilateral dorsolateral prefrontal (BA 46), and dorsal anterior cingulate (BA 24, 32) regions. For maintenance, in contrast, constrained principal component analysis identified a system that was characterized by both load-dependent increases and decreases in activation. The structures in this system jointly activated by maintenance load involved left posterior parietal (BA 40), left inferior prefrontal (BA 44), left premotor and supplementary motor areas (BA 6), and dorsal cingulate regions (BA 24, 32), while the regions displaying maintenance-load-dependent activity decreases involved bilateral occipital (BA 17, 18), posterior cingulate (BA 23) and rostral anterior cingulate/orbitofrontal (BA 10, 11, 32) regions. The correlation between the encoding and maintenance systems was strong and negative (Pearson's r = -.55), indicting that some regions important for visual processing during encoding displayed reduced activity during maintenance, while subvocal rehearsal and phonological storage regions important for maintenance showed a reduction in activity during encoding. In summary, our analyses suggest that separable and complementary subsystems underlie encoding and maintenance in verbal working memory, and they demonstrate how constrained principal component analysis can be employed to characterize neuronal systems and their functional contributions to higher-level cognition.     

Imitation of novel and well-known actions

Four experiments were carried out using the action span paradigm. In experiment 1 we found that well-learnt, meaningful (MF) actions were imitated better than novel, meaningless (ML) actions. In experiments 2 and 3, during the encoding of MF and ML actions, participants were required to carry out different suppression tasks. In experiment 2 we replicated the advantage of MF actions over ML actions and also found that the motor suppression shortened the action span more than the other forms of suppressions (spatial and articulatory). Action encoding and motor suppression tapping the same subsystem, temporarily holding the motor information, could explain the reduced motor span obtained in experiment 2. Two alternative explanations that could have accounted for this effect were ruled out in experiments 3 and 4. In experiment 3 we verified whether the reduction of the action span was produced by the different combination of the articulatory suppression with motor suppression or with the spatial suppression. In experiment 4, we demonstrated that the reduction was not due to the motor suppression being more difficult than the other types of suppression. The critical finding that the spans of well-learnt, MF actions are longer than those of novel, ML actions observed in experiments 1 and 2 was interpreted in terms of different processing routes engaged in the imitation of these two types of actions. MF actions can be imitated along both a semantic, indirect route and a direct route leading from the visual analysis of the action to the motor system. In contrast, the imitation of ML actions is accomplished along the direct route only.     

Ongoing theta oscillations predict encoding of subjective memory type

Recent human electro-encephalography (EEG) studies show that ongoing brain states support successful encoding of human memory, including recognition. However it is not known whether ongoing cortical activity qualitatively determines different memory types at encoding. In this study, using a remember/know procedure, we measured the EEG oscillations that emerge before and during the encoding of abstract visual stimuli in episodic and non-episodic memory, focusing on the theta (2–8 Hz) and alpha (9–12 Hz) oscillation range. We found that enhanced prestimulus theta oscillations precede episodic memory encoding, compared to non-episodic encoding. The prestimulus difference appeared at frontal and temporal sites. Furthermore, the theta enhancement reappeared after stimulus onset. Enhanced upper alpha oscillations suggested increased working memory processing in the case of episodic memory. Finally, the pre- and post-stimulus theta and alpha amplitudes showed different correlation patterns for episodic and non-episodic encoding. Our results are the first to suggest that encoding of episodic memory depends on preparatory processing in the form of frontal and temporal theta oscillations.