We have organized this review around theoretical explanations of category specificity in the human brain. One theme that emerges is the historical progression from theories based on a single principle of organization to theories that integrate multiple dimensions of organization. This progression is due to the broad recognition in the field that a single dimension will not be sufficient to explain all aspects of the organization of object knowledge in the brain. However, not every dimension or principle of organization is of equal importance because not all dimensions have the same explanatory scope. A relative hierarchy of principles is therefore necessary to determine which of the many known facts are theoretically important and which are of only marginal significance.
Two broad findings emerge from cognitive neuropsychological research. First, patients have been reported with disproportionate impairments for a modality or type of knowledge (e.g., visual/perceptual knowledge, ; manipulation knowledge, ). Second, category-specific semantic deficits are associated with impairments for all types of knowledge about the impaired category (). Analogues to those two facts are also found in functional neuroimaging. First, the attributes of some categories of objects (e.g., tools) are differentially represented in modality-specific systems (i.e., motor systems). Second, within a given modality-specific system (e.g., ventral visual pathway), there is functional organization by semantic category (e.g., living animate versus nonliving) (see for an overview). Thus, across both neuropsychological studies and functional imaging studies, the broad empirical generalization emerges that there are two, orthogonal, constraints on the organization of object knowledge: object domain and sensory/motor modality. This empirical generalization is neutral with respect to how one explains the causes of category-specific effects in both functional neuroimaging and neuropsychology.
Many theoretical proposals of the causes of category specificity articulate dimensions along which semantic categories differ (e.g., Cree & McRae 2003
, Devlin et al. 1998
, Gauthier et al. 2000
, Haxby et al. 2001
, Humphreys & Forde 2001
, Laws & Gale 2002
, Levy et al. 2001
, Mechelli et al. 2006
, Op de Beeck et al. 2008
, Rogers et al. 2004
, Sartori & Lombardi 2004
, Simmons & Barsalou 2003
, Tranel et al. 1997
, Tyler & Moss 2001
, Warrington & Shallice 1984
, Zannino et al. 2006
). Understanding the role that such dimensions play in the genesis of category specificity in a particular part of the brain, or a particular component of a cognitive model, will be central to characterizing the functioning of that component of the system. However, progress in understanding the causes of category specificity in one region of the brain, or one functional component of a cognitive model, will require an understanding of how category specificity is realized throughout the whole brain and throughout the whole cognitive model.
All current theories of the organization of conceptual knowledge assume that a concept is composed of distinct types of information. This shared assumption permits an explanation of how thinking about a single concept (e.g., hammer) can engage different regions of the brain that process distinct types of information (e.g., sensory versus motor). It also allows for an account of how patients may present with impairments for a type or modality of knowledge (e.g., know what a hammer looks like but not know how to use it). However, that assumption begs the question of how the different types of information that constitute a given concept are functionally unified. A central theoretical issue to be addressed by the field is to understand the nature of the mechanisms that unify different types of knowledge about the same entity in the world and that give rise to a functionally unitary concept of that entity.
Our own view—the distributed domain-specific hypothesis—assumes that the first-order principle of organization is object domain. Within any given domain of knowledge, there will be functional and neural specialization according to types or modalities of knowledge. For instance, visual motion properties of living animate things are represented in a different region/system than are visual form properties of living animate things. In addition, affective properties of living animate things may be represented by other, functionally and neuroanatomically, distinct systems. However, all of those types of information constitute the domain “living animate.” For that reason, it is critical to specify the nature of the functional connectivity that relates processing across distinct subsystems specialized for different types of information. The basic expectation of the distributed domain-specific hypothesis is that the functional connectivity that relates processing across distinct types of information (e.g., emotional value versus visual form) will be concentrated around those domains that have had evolutionarily important histories. The strong prediction that follows from that view is that such neural circuits are the same circuits that are damaged in patients with category-specific semantic deficits.
Independently of whether the distributed domain-specific hypothesis is empirically confirmed, it serves to highlight two key aspects of human conceptual processing. First, humans do not have systems that support rich conceptual knowledge of objects in order to carry out only explicit knowledge tasks, such as object naming or similarity judgments. We have those systems because they serve action and ultimately have been in the service of survival. An understanding of the architecture of the conceptual system must therefore be situated in the context of the real-world computational problems that the conceptual system is structured to support. Second, human behavior arises due to the integration of multiple cognitive processes that individually operate over distinct types of knowledge. In contrast to the view that domain specificity implies modularity, we have emphasized the distributed nature of domain-specific neural circuits. On the distributed domain-specific hypothesis, the distinct (and potentially modular) processes within the sensory, motor, and affective systems are components of broader structures within the mind/brain. This framework thus emphasizes the need to understand how different types of cognitive processes, operating over different types of information, work in concert to orchestrate behavior.
In the more than 25 years since Warrington and colleagues’ first detailed reports of patients with category-specific semantic deficits, new fields of investigation have emerged around the study of the organization and representation of conceptual knowledge. Despite that progress, the theoretical questions that currently occupy researchers are the same as those that were initially framed and debated two decades ago: What are the principles of neural organization that give rise to effects of category specificity? Are different types of information involved in processing different semantic categories and, if so, what distinguishes those different types of information? Future research will undoubtedly build upon the currently available theories as well as redeploy their individual assumptions within new theoretical frameworks.
- To what degree do sensory and motor processes participate in higher cognitive function? The available evidence from neuropsychology places a clear upper limit on the degree to which conceptual knowledge can be assumed to be “embodied.” However, equally compelling findings from functional neuroimaging demonstrate that the sensory and motor systems are automatically engaged during conceptual processing. It will be important to develop articulated models of the dynamics of activation flow among concepts and the sensory and motor systems in order to test hypotheses about the causes of sensory and motor activation during conceptual processing.
- Are different domains of knowledge represented differently in males and females? Some researchers have highlighted the fact that patients with disproportionate semantic impairments for fruit/vegetables are male. This pattern remains even after controlling for gender-specific familiarity among items from different categories. Those data raise the question of whether early (and culturally influenced) differences in experience can qualitatively shape the functional architecture of the conceptual system.
- How does damage to one region of the brain affect processing in other regions of the brain? Little is currently known about how damage to distinct regions within a network affects processing in other regions of the network. Detailed cognitive and anatomical studies of patients with semantic deficits will aide in understanding the dynamics of brain damage and the implications for cognitive models of conceptual processing.