J.C. Mizelle

Neural activation for conceptual identification of correct versus incorrect tool–object pairs

Appropriate tool-object pairing is a natural part of our lives. When preparing to clean our teeth, we know that a toothbrush is useful, but not a screwdriver. The neural correlates of this pairing process remain unclear. We recorded 64-channel electroencephalography to determine neural correlates of identification of tool-object matches and mismatches. Subjects were shown a target tool (e.g. spoon) later paired with an object that was either a conceptual match (e.g. bowl) or mismatch (e.g. wood). To verify that activity was not related to general concept of match-mismatch, in a second condition subjects saw non-tool environmental items (e.g. bird) later paired with a conceptual match (e.g. nest) or mismatch (e.g. spider web). Analysis was focused on time bins after each picture, using standardized low-resolution brain electromagnetic tomography (sLORETA). Tool-object match versus mismatch revealed significant differences in the posterior cingulate, precuneus, left insula and superior temporal gyrus. These patterns were not present for environmental match versus mismatch. This work suggests a specific network in comprehending tool-based pairings, but not extensive to other pairings. The posterior cingulate, precuneus, insula and superior temporal gyrus preferentially differentiates tool-object matching and mismatching, identifying a potential locus related to impairments in comprehending appropriate and inappropriate tool-object relationships that arise after neural injury.

Electroencephalographic reactivity to unimodal and bimodal visual and proprioceptive demands in sensorimotor integration

We used electroencephalography to see how the brain deals with altered sensory processing demands in lower extremity movements. In unimodal conditions, sensory processing demands were altered with subjects performing movement to a small or large visual target, or with a small or large weight to modify proprioception. In bimodal conditions, both weight and targets needed to be met. We assessed activity over primary sensorimotor, premotor and parietal areas before and during knee movements. In unimodal conditions, the primary sensorimotor area showed the least sensitivity to the maximally increased sensory demand in both vision and proprioception, while the premotor region was most sensitive to proprioceptive demands, and the parietal region showed greatest sensitivity to visual demands. In bimodal conditions, intermediate levels of sensory processing demand maximally increased activation at premotor and parietal regions. However, when visual and proprioceptive demands were both maximal, activation decreased and was similar to that seen with the lowest level of sensory processing demand. As behavior was consistent across conditions while activation at these regions decreased, we suggest that additional brain areas, possibly high order cognitive and attentional regions, may be required to augment the function of the traditional sensorimotor network in lower extremity movements with increasingly difficult sensory processing demands.

The Neuroscience of Storing and Molding Tool Action Concepts: How “Plastic” is Grounded Cognition?

Choosing how to use tools to accomplish a task is a natural and seemingly trivial aspect of our lives, yet engages complex neural mechanisms. Recently, work in healthy populations has led to the idea that tool knowledge is grounded to allow for appropriate recall based on some level of personal history. This grounding has presumed neural loci for tool use, centered on parieto-temporo-frontal areas to fuse perception and action representations into one dynamic system. A challenge for this idea is related to one of its great benefits. For such a system to exist, it must be very plastic, to allow for the introduction of novel tools or concepts of tool use and modification of existing ones. Thus, learning new tool usage (familiar tools in new situations and new tools in familiar situations) must involve mapping into this grounded network while maintaining existing rules for tool usage. This plasticity may present a challenging breadth of encoding that needs to be optimally stored and accessed. The aim of this work is to explore the challenges of plasticity related to changing or incorporating representations of tool action within the theory of grounded cognition and propose a modular model of tool–object goal related accomplishment. While considering the neuroscience evidence for this approach, we will focus on the requisite plasticity for this system. Further, we will highlight challenges for flexibility and organization of already grounded tool actions and provide thoughts on future research to better evaluate mechanisms of encoding in the theory of grounded cognition.

Why is that Hammer in My Coffee? A Multimodal Imaging Investigation of Contextually Based Tool Understanding.

Appropriate tool–object pairing is a natural part of our lives. When preparing to stir coffee, we know that a hammer is useful for some tasks but that it is not appropriate in this behavioral context. The neural correlates of this context–tool pairing process remain unclear. In the current work, we used event-related electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) to determine neural correlates for differentiating contextually correct and incorrect tool use. Subjects were shown images depicting correct (e.g., spoon used to stir coffee) or incorrect (e.g., hammer used to stir coffee) tool use. We identified distinct regional and temporal activations for identifying incorrect versus correct tool use. The posterior cingulate, insula, and superior temporal gyrus preferentially differentiated incorrect tool–object usage, while occipital, parietal, and frontal areas were active in identifying correct tool use. Source localized EEG analysis confirmed the fMRI data and showed phases of activation, where incorrect tool-use activation (0–200 ms) preceded occipitotemporal activation for correct tool use (300–400 ms). This work extends our previous findings to better identify the neural substrate for contextual evaluation of tool use, and may contribute to our understanding of neurological disorders resulting in tool-use deficits.

Testing perceptual limits of functional units: Are there “automatic” tendencies to associate tools and objects?

Prior work has demonstrated a unique network involving the insula, temporal cortex, and precuneus in evaluating appropriate relationships between tool-object pairings under instruction [20]. However, are there automatic tendencies to evaluate appropriate tool-object pairings? Using electroencephalography (EEG), we emulated our prior work to identify neural mechanisms that, in the absence of task-related consciousness, differentiate functionally matching from mismatching tool-object pairs. This was compared to any activation consistent with this using environmental image pairs. In addition, based on the paradigm we were able to discern any naïve processes that distinguish tools from non-tool environmental images. Results show that without task-related consciousness, the left occipitotemporal gyrus is preferentially active for tools compared to environmental images. Tool-object match and mismatch each versus control images show differences relative to a control image over the left temporal cortex, extending into the insula, yet there was no difference between tool-object match and mismatch. This suggests that there is no clear neural mechanism for continual evaluation of tool matching from mismatching, though there is for broad picture classifications. Taken together with our previous results, this creates a discussion for the role of intention when determining such relationships.

Distinctive laterality of neural networks supporting action understanding in left- and right-handed individuals: An EEG coherence study

Prior work has demonstrated that perspective and handedness of observed actions can affect action understanding differently in right and left-handed persons, suggesting potential differences in the neural networks underlying action understanding between right and left-handed individuals. We sought to evaluate potential differences in these neural networks using electroencephalography (EEG). Right- and left-handed participants observed images of tool-use actions from egocentric and allocentric perspectives, with right- and left-handed actors performing the actions. Participants judged the outcome of the observed actions, and response accuracy and latency were recorded. Behaviorally, the highest accuracy and shortest latency was found in the egocentric perspective for right- and left-handed observers. Handedness of subject showed an effect on accuracy and latency also, where right-handed observers were faster to respond than left-handed observers, but on average were less accurate. Mu band (8-10 Hz) cortico-cortical coherence analysis indicated that right-handed observers have coherence in the motor dominant left parietal-premotor networks when looking at an egocentric right or allocentric left hands. When looking in an egocentric perspective at a left hand or allocentric right hand, coherence was lateralized to right parietal-premotor areas. In left-handed observers, bilateral parietal-premotor coherence patterns were observed regardless of actor handedness. These findings suggest that the cortical networks involved in understanding action outcomes are dependent on hand dominance, and notably right handed participants seem to utilize motor systems based on the limb seen performing the action. The decreased accuracy for right-handed participants on allocentric images could be due to asymmetrical lateralization of encoding action and motoric dominance, which may interfere with translating allocentric limb action outcomes. Further neurophysiological studies will determine the specific processes of how left- and right-handed participants understand actions.

Theta frequency band activity and attentional mechanisms in visual and proprioceptive demand

In a companion manuscript we reported reduced electroencephalographic (EEG) activation at traditional sensorimotor areas in knee movements with high levels of task difficulty modulated by varying visual and proprioceptive sensory demands. Given that reduced cortical activity with more complex tasks is counter-intuitive, we suggested that high order cognitive-motor areas may show increased EEG activation to compensate for the observed decrease in sensorimotor regions. To test this hypothesis, we evaluated theta band activation at anterior frontal regions in a secondary analysis of our previous data. Unlike activation at sensorimotor areas, anterior frontal responses increased with each level of task difficulty as modulated by precision of visual targeting and/or proprioceptive demands from adding masses to the leg. Activity was increased as both unimodal visual and proprioceptive requirements became more demanding, but showed greater sensitivity to visual over proprioceptive processing requirements. Each level of bimodal task demands showed increasing activation, which was consistently greater when modulated through visual demands. These results are consistent with our hypothesis of increased contribution of anterior frontal regions for motor control in lower extremity movements with increasing sensory demands and further support different mechanisms for internally and externally guided movement.

Remodeling of cortical activity for motor control following upper limb loss.

OBJECTIVE Upper extremity loss presents immediate and lasting challenges for motor control. While sensory and motor representations of the amputated limb undergo plasticity to adjacent areas of the sensorimotor homunculus, it remains unclear whether laterality of motor-related activity is affected by neural reorganization following amputation. METHODS Using electroencephalography, we evaluated neural activation patterns of formerly right hand dominant persons with upper limb loss (amputees) performing a motor task with their residual right limb, then their sound left limb. We compared activation patterns with left- and right-handed persons performing the same task. RESULTS Amputees have involvement of contralateral motor areas when using their sound limb and atypically increased activation of posterior parietal regions when using the affected limb. When using the non-amputated left arm, patterns of activation remains similar to right handed persons using their left arm. CONCLUSIONS A remodeling of activations from traditional contralateral motor areas into posterior parietal areas occurs for motor planning and execution when using the amputated limb. This may reflect an amputation-specific adaptation of heightened visuospatial feedback for motor control involving the amputated limb. SIGNIFICANCE These results identify a neuroplastic mechanism for motor control in amputees, which may have great relevance to development of motor rehabilitation paradigms and prosthesis adaptation.

Reliability of Visual and Somatosensory Feedback in Skilled Movement: The Role of the Cerebellum

The integration of vision and somatosensation is required to allow for accurate motor behavior. While both sensory systems contribute to an understanding of the state of the body through continuous updating and estimation, how the brain processes unreliable sensory information remains to be fully understood in the context of complex action. Using functional brain imaging, we sought to understand the role of the cerebellum in weighting visual and somatosensory feedback by selectively reducing the reliability of each sense individually during a tool use task. We broadly hypothesized upregulated activation of the sensorimotor and cerebellar areas during movement with reduced visual reliability, and upregulated activation of occipital brain areas during movement with reduced somatosensory reliability. As specifically compared to reduced somatosensory reliability, we expected greater activations of ipsilateral sensorimotor cerebellum for intact visual and somatosensory reliability. Further, we expected that ipsilateral posterior cognitive cerebellum would be affected with reduced visual reliability. We observed that reduced visual reliability results in a trend towards the relative consolidation of sensorimotor activation and an expansion of cerebellar activation. In contrast, reduced somatosensory reliability was characterized by the absence of cerebellar activations and a trend towards the increase of right frontal, left parietofrontal activation, and temporo-occipital areas. Our findings highlight the role of the cerebellum for specific aspects of skillful motor performance. This has relevance to understanding basic aspects of brain functions underlying sensorimotor integration, and provides a greater understanding of cerebellar function in tool use motor control.

How can we improve our understanding of skillful motor control and apraxia? Insights from theories of “affordances”

A recent opinion article published in Frontiers in Human Neuroscience (Osiurak, 2013) points out several challenges of the study of “affordances” related to investigations of apraxia. In 2010, we published in Frontiers a review and theoretical proposal that addresses our concerns about affordances and grounded cognition (Mizelle and Wheaton, 2010b). Central to our premise was the argument that, for tool use, action goals were the grounded invariant elements as opposed to the action representations of the tools themselves. Further, parameters of the behavior(s) undertaken to achieve the action goal (tool used to accomplish the task, usage context of the tool, and the motor variables to accomplish the task) are affording to the goal, inherently variable, but are driven by the fixed action goal itself. Our model (Modular Selection for Action Goals, MSAG) incorporates the idea that stored representational knowledge of tools can be broadly adapted by usage context so that action goals can be achieved, emphasizing the adaptability of tool contextual and usage representations and the fixedness of the overall action goal. In commentary to our MSAG model, Pellicano et al. (2011) considered an alternative view where affordances (stable and variable) function to align tools to action goals. The core difference is that Pellicano and colleagues proposed that potentiation of tool-action goal alignment is mediated by affordances (certain properties of tools). We proposed that the fulfillment of the action goal defines affording properties of any possible combination of tools and motor variables, where some combinations are more or less affording to the action goal than others. At any rate, we certainly agree that further studies need to be considered to appreciate and refine specifics of any models, whether ours or those of Pellicano and colleagues. While Osiurak emphasized the alternative commentary (Pellicano et al., 2011), we feel it is worth noting that many of the ideas presented by Osiurak (2013) reflect core concepts of our 2010 MSAG theory. For example, in Figure 2 of the MSAG proposal paper (Mizelle and Wheaton, 2010b), selection of alternative tools when the canonical tool is not available (we use the example of tools within a reasonable workspace) is not necessarily driven by a broad range of stable affordances (the adaptive grounded view). Rather, an alternative tool is selected based on the properties which best allow for the accomplishment of the action goal based on known mechanical/functional properties of tools. This embodies the first two assumptions of Osiurak (2013). Under MSAG, interconnected modules are triggered by an action goal that afford semantic flexibility of tools; tool (selection), usage context (refinement, as tools have multiple uses), and neurobiomechanics (motor specifics). Further, our contention has been that the elements that best fulfill the action goal become the relevant affordances for tool selection and motor performance, not necessarily the “grounded” or stable affording properties of tools. This embodies the third assumption presented by Osiurak. The action goal defines the cooperatively determined usage context of the tool. Chiefly, this allows for creativity and adaptability in how action goals are accomplished, especially when canonical tools—those with grounded action representations coincident with the action goal—are not available. Work in our lab has sought to understand how people “connect” tools and objects for action goals. Using electroencephalography (EEG), we have suggested that erroneous tool-object pairings generates ventral activation, which seems to precede parietofrontal activation typical of tool-object encoding for action (Mizelle and Wheaton, 2010a,c). Further, in a multimodal neuroimaging study, we used EEG and functional MRI (fMRI) to propose that contextual understanding of incorrect/impossible actions (via ventral pathways) precedes the activity of correct/possible actions (via parietofrontal pathways) that may suggest how both conceptual and ideomotor type apraxias could occur (Mizelle and Wheaton, 2010d). Indeed, this was reflected in MSAG as we proposed that ventral damage could corrupt the ability to align a tool with the action goal and the canonical usage context of that tool. In this case, a failure to deselect inappropriate tools would result, but the inappropriate tool would be used in motor-relevant ways in an attempt to achieve the desired behavior. It is our proposal that such ventral pathway damage could help distinguish clinico-anatomical correlates of motor versus conceptual apraxias. Core to the goals of this Research Topic (“Bridging the theories of offordances and limb apraxia”), what does MSAG have to do with apraxia? We have had interest in focusing MSAG on the conceptual level, to better understand neural circuits that could be vulnerable in persons with conceptual apraxias. We have recently refined the MSAG proposal, suggesting that the dorsal parietofrontal areas encode possible “functional affordance,” where qualities of seen (or desired) actions of tools are encoded based on relevance to behaviors for achievement of an action plan (Mizelle et al., 2013). In this work, we chose tool-object pairs that were always correct/possible to fulfill an action goal, but modified the functional affordance by changing how the tool interacted with the object. When functional affordance is high (correct tool-object pairs are used correctly) parietofrontal activation is dominant. Yet, when functional affordance is low (correct tool-object pairs used incorrectly), ventral brain areas show significant activations. Thus, functional affordance may be similarly driven, at least in part, by the mechanical/physical alignment (Mizelle et al., 2013) and contextualization (Mizelle and Wheaton, 2010a,d) of tool-object pairs. This helps to underscore a common problem in conceptual apraxia, where tool selection for a task is impacted. If ventral networks are largely affected, conceptual errors can become predominant, yet the MSAG model does not stop there. As MSAG predicts, successful fulfillment of the action goal is paramount and a certain amount of inherent flexibility exists to accomplish the goal. As we proposed in MSAG, accomplishing the goal without ending in a fault is of primary concern. MSAG proposes a preliminary framework of how both conceptual and motor “faults” may occur, which would reflect conceptual and ideomotor apraxias. While many of our studies have focused on the conceptual errors, we are continuing work on expansion into the motoric domain, and the interactions between conceptual and motor properties of action. We anticipate that such refinement will be a pivotal step in being able to better detail the neural systems involved in apraxia. We are continuing to study how we encode and understand action goals, which is core to shaping MSAG and highly relevant to the opinion article by Ousirak. In the context of goal-based tool use, our own work suggests that affordances are complex, possibly dynamic entities. We propose that research should focus on the varied properties of affordance and how these varied properties might interact. A good place to start would be seeking to align the various proposals of affordance, and their relevance to apraxia, through collaborative research efforts.