Arguments about the nature of concepts: #symbodiment and beyond

(This post is an edited and abridged version of the opening article to the #symbodiment special issue of the Psychonomic Bulletin & Review authored by Bradford Z. Mahon and Gregory Hickok. The full article can be found here.)

The question of how word, object, event and action meanings are represented and organized in the brain has a rich and dynamic history.

A number of neuropsychological phenomena were critical in laying the basis for the modern understanding of the neural systems that support conceptual knowledge. First, it was observed that patients could present with disproportionate deficits to a category or domain of knowledge: category-specific semantic deficits. Category-specific semantic deficits are conceptual impairments that are selective or disproportionate for living animate entities (animals), living inanimate entities (fruit/vegetables), conspecifics (knowledge of people), or nonliving things.

At the same time as that early formative work was underway on category-specific deficits, Goodale and Milner and colleagues described the consequences of a focal lesion to what came to be termed the ventral object processing pathway: bilateral lesions to lateral occipital-temporal cortex could lead to impairments for visually recognizing objects but no difficulty performing grasping and reaching movements to the same objects.

Other patients presented with the reverse behavioral dissociation after lesions to posterior parietal cortex: impaired object directed reaching or grasping despite intact object identification.

Those and other data formed the basis for a new understanding of functionally and anatomically dissociable channels of visual processing, what has come to be referred to as the two visual (or ventral/dorsal) systems model. Around the same time it was also established that neurodegerative diseases, such as Semantic Dementia, could lead to broad deterioration of semantic knowledge, sometimes with category-specific dissociations. Another key piece of neuropsychological evidence was the observation that the ability to produce nouns (typically objects) or verbs (typically actions) was doubly dissociable, and in some cases attributable to a semantic level dissociation while in other cases attributable to a lexical and/or syntactic level dissociation.

Thus, when the first functional neuroimaging studies on conceptual processing in the human brain were being reported, there were established efforts well underway to understand a) how conceptual knowledge could be organized in the brain such that it could dissociate after brain damage along (seemingly) categorical lines, b) how different channels within the cortical visual processing network differentially contributed to visual object identification and object directed action and spatial processing, and c) how object and action knowledge, and nouns and verbs, might be dissociably represented by distinct neural systems.

The first neuroimaging studies to look at the neural organization of concepts seemed to largely substantiate the idea that semantic category or domain was an organizing principle in the brain: Martin and colleagues observed that subregions of the ventral object processing pathway exhibited differential activation for animals and tools, and Kanwisher and colleagues reported neural specificity for faces.

Subsequent investigations documented stimulus specificity for placesbody parts, and written words in the ventral visual pathway.

More recently, it has been discovered that many regional biases by category or stimulus type, while present in what are principally ‘visual’ or ‘visually responsive’ regions of the brain, are nonetheless also present in individuals without any visual experience, and in remarkably high anatomical correspondence with sighted individuals; the data from congenitally blind participants suggest that while vision clearly plays a critical role in shaping neural responses in high-level visual areas, the broad scaffolding of the visual system by ‘semantic domain’ originates in constraints that operate independent of visual experience.

Those constraints may be hardwired anatomical connectivity between regions of the ‘visual system’ and other regions of the brain that process nonvisual information about the same classes of stimuli. The idea that connectivity-based constraints drive category-specificity in high-level visual areas has been gaining momentum.

Hearty discussion ensued, and continues, about the constraints and principles of neural organization that give rise to category-specificity, where ‘category’ in this context is understood broadly, to capture objects, actions, nouns, verbs, faces, places, body parts, and so on.

In the last decade, multivariate techniques for analyzing distributed patterns of neural activity have grown in prominence as a means to understand how object concepts are coded in cortex. The widespread adoption of multivoxel pattern classification approaches has led to a shift in emphasis from ‘which regions’ of the brain support which ‘types’ or ‘classes’ of concepts, to studying the representational space within those regions.

Another important and recent development has been an emphasis on using functional and anatomical connectivity to probe the network structure of anatomically distinct regions that exhibit congruent category-preferences.

Along with reporting the first comprehensively described cases of category-specificity, Warrington and her collaborators also articulated a proposal that has dramatically shaped theoretical approaches for understanding the organization and representation of concepts in the brain. The Sensory/Functional Theory refers to the idea that dissociations among different classes or categories of information arise because of damage to modality-specific brain systems, and that there are high correlations between certain categories and certain modality-specific systems.

Largely in parallel to research investigating the granularity of neural specificity for different categories, the broad discovery was made that the sensorimotor systems are engaged during conceptual processing. The reckoning that sensorimotor systems are engaged during conceptual processing led to a resurgence of interest in the idea that conceptual content is distributed in the sensorimotor systems—the embodied cognition hypothesis (also referred to as ‘grounded cognition’, ‘situated cognition’; herein we refer to this class of proposals as ‘embodied cognition’).

While prior theories of concept representation had emphasized the organization of conceptual content (where conceptual content refers to what concepts are about, as in a concept is about the color red, or about dogs, or about peace), the embodied framework emphasized the format in which conceptual information was represented (i.e., in a modality-specific or sensorimotor format, a multisensory format, as opposed to in an amodal format). Allport, one of the pioneers of this perspective put it thus:

The essential idea is that the same neural elements that are involved in coding the sensory attributes of a (possibly unknown) object presented to eye or hand or ear also make up the elements of the auto-associated activity-patterns that represent familiar object-concepts in “semantic memory.” This model is, of course, in radical opposition to the view, apparently held by many psychologists, that “semantic memory” is represented in some abstract, modality-independent, “conceptual” domain remote from the mechanisms of perception and motor organization.

The ‘embodied’ theory of semantic representation has been enormously influential over the last decade, particularly in the context of investigations of the neural underpinnings of conceptual knowledge. In a now classic theoretical treatment of this issue, Barsalou laid out what is perhaps the most complete framework to date. Within the ‘Perceptual Symbol System’ framework, conceptual processing is embodied or grounded because conceptual content is, at least in part, re-accessed sensorimotor information – concepts are not an additional level of representation that is abstracted away from sensorimotor systems, and represented in a stand-alone manner from those sensorimotor systems.

Barsalou was diligent in his framing of the theory to argue how key phenomena of human conceptual processing (e.g., compositionality, productivity) could arise from the quasi-symbolic operation of perceptual symbols.

Another important discovery that has shaped the climate in which recent theoretical accounts of meaning representation have been developed is that of so-called ‘mirror neurons’: neurons (and neural regions) in or adjacent to the motor system that are activated when observing others’ actions. The discovery of mirror neurons reinvigorated interest in motor theories of the perception and recognition of actions. The basic idea of motor theories of action recognition is that in order to recognize and identify an action it is necessary to covertly simulate the motor movements that would be required in order to produce that action. In relatively recent times, this theory was most prominently proposed in the domain of speech perception by Liberman and colleagues, and has since been extended into many other domains on the basis of the putative mirror properties of motor responses. An active discussion ensued, and continues, about what ‘mirror’ neuron (and neural) activity is really telling us about action perception and recognition.

It should be noted that while there is no necessary relation between embodied theories of meaning representation and motor theories of action perception, the two accounts have nonetheless become intertwined in many discussions because they are proposals in the same spirit. One’s concept ‘kick’ is constituted (at least in some important ways) by information stored in a motor format in that individual’s motor system and which pertains to that individual’s foot; and similarly, one’s ability to recognize the action of ‘kicking’ depends on covert simulation (by that individual’s motor system) of kicking (with that individual’s actual foot-motor representation). Thus, the representation of ‘kicking’ by one’s motor system serves both to support action recognition and constitutes, in part, the concept ‘kick.’

One obvious test of ‘mirror neuron’ and ‘embodied accounts’ is to ask what happens to action recognition and concept representation when a brain lesion has disrupted sensorimotor information.

The general finding that has emerged is that despite lesions that cause sensorimotor impairments, and presumably high levels of redaction of sensorimotor information, patients can exhibit little to no impairment for conceptual processing. Those neuropsychological data seem to be influencing the theoretical discussion more and more. As Barsalou emphasizes in the #symbodiment special issue, a key issue is the degree to which a given concept may be distributed over multiple modality-specific systems: for instance, damaging the motor system may not affect the concept ‘kick’ if that concept can change the ‘posture’ of its reliance on modality-specific information to lean more heavily on representations in the visual system. In this regard, the patient data have formed an important part of the motivation for ‘hybrid’ accounts: on these accounts, while conceptual processing reaches into the sensorimotor systems, the center of gravity of conceptual processing is abstracted away from specific sensorimotor information, and distributed across many systems.

Even with this brief look back over the recent history of the empirical study of concepts, it is clear that real progress has been made along two dimensions: we have a deep understanding of the organization of conceptual content, and much is also known about the representational format of concepts. Perhaps most importantly, and as highlighted in this special issue of Psychonomic Bulletin & Review, the field has advanced in the sophistication with which key theoretical questions are framed and approached empirically. But it is equally clear that the questions themselves that are now at the forefront of the field are the direct descendants of questions that were at the forefront of the field in its modern initiation.

What is new about current discussions of content and format in conceptual representation is that we now have (many) methods that probe in vivo neural activity during conceptual processing. Continued progress will be spurred by keeping two questions front and center with respect to any given theoretical proposal: First: Is it an hypothesis about the nature of conceptual content or about the nature of conceptual format? Second: Given the answer to the first question, what would an alternative hypothesis look like? These two questions can serve to set in relief the bridging assumptions that connect theories of the organization and representation of concepts to the empirical phenomena, and thus serve to reappraise the substantive issues that need to be adjudicated.

This post is an abridged and edited version of the introductory article to the special issue of the Psychonomic Bulletin & Review on “Arguments about the Nature of Concepts: Symbols, embodiment, and beyond”.

The full article can be accessed here.

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