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Where do you know what you know? The representation of semantic knowledge in the human brain

Key Points

  • Semantic memory corresponds to people's general conceptual knowledge about objects and events, including knowledge about their characteristic properties and behaviours, as well as knowledge about the words we use to name and describe objects and events in speech.

  • Whereas episodic memory encompasses memory for specific episodes or situations in one's life, semantic memory encompasses factual knowledge divorced from any specific situational context: “a scallop is an edible sea creature” (semantic) as opposed to “I ate scallops for supper last night” (episodic).

  • Essentially all theories agree that a widely distributed brain network is responsible for our semantic knowledge of modality-specific features (for example, what a scallop looks or tastes like); but the theories differ on whether this network is sufficient for all of the functions of semantic memory.

  • The theory highlighted in this review proposes that conceptual knowledge requires an amodal hub, which itself contains no semantic features but rather represents the semantic similarity among concepts — for example, the semantic similarity between scallops and prawns, despite their differences in virtually every modality-specific attribute.

  • This theory predicts that a lesion of the specific brain region supporting the amodal hub should disrupt all abilities requiring central conceptual knowledge, independent of the modality of input (such as objects, words or sounds) or output (such as speaking, drawing or using objects) and independent of the type of concept (living things, man-made objects and abstract ideas, for example).

  • Patients with semantic dementia, a neurodegenerative syndrome resulting from focal atrophy of the anterior temporal lobes (ATL) bilaterally, show precisely this pattern of semantic degradation across all modalities and all types of conceptual knowledge; therefore, semantic dementia suggests that the ATL supports an amodal hub.

  • Functional neuroimaging studies of semantic processing only sometimes reveal activation in the ATL. The likelihood of activation in this region, however, can be predicted by a combination of the specific imaging techniques employed and the specificity of semantic processing required by the imaging task.

  • Simulations of semantic memory in connectionist models suggest one reason why the semantic network might require a hub: without such an architecture, it is not clear how the system can learn representations that capture semantic similarity relations.

Abstract

Mr M, a patient with semantic dementia — a neurodegenerative disease that is characterized by the gradual deterioration of semantic memory — was being driven through the countryside to visit a friend and was able to remind his wife where to turn along the not-recently-travelled route. Then, pointing at the sheep in the field, he asked her “What are those things?” Prior to the onset of symptoms in his late 40s, this man had normal semantic memory. What has gone wrong in his brain to produce this dramatic and selective erosion of conceptual knowledge?

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Figure 1: Two theoretical positions regarding the neuroanatomical distribution of the cortical semantic network and schematic models based on these views.
Figure 2: Examples of impaired performance on semantic tasks in patients with semantic dementia.
Figure 3: Differences between semantic dementia and Alzheimer's disease in measures of brain function and semantic memory.
Figure 4: ATL activation in functional imaging studies of semantic processing.

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Acknowledgements

We gratefully acknowledge help from E. Copper-Pye in preparation of the manuscript.

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Correspondence to Karalyn Patterson or Timothy T. Rogers.

Glossary

Expressive vocabulary

The set of words that an individual knows and can retrieve for referring to objects and other concepts in speech or writing.

Receptive vocabulary

The set of words that an individual can comprehend when hearing or reading them.

Aphasia

Impaired language abilities resulting from brain disease or injury.

Cross-modal

The term that is applied to representations or processes that operate across different kinds of sensory, motor and linguistic representations. For instance, representations and processes that receive input from and/or direct output to both visual and auditory representations would be considered cross-modal.

Anomia

The failure to name objects, concepts and people, whether in response to stimulus presentation or in spontaneous speech.

Volumetric MRI

A method that uses finely cut brain slices (usually less than 2 mm thick) to measure the volume of brain structures.

Voxel-by-voxel analysis

A method of whole-brain image analysis in which the brain scans of different individuals are fitted to a standard template (to minimize inter-individual differences in brain shape) so that brain regions can be compared systematically across subjects.

Lesion-overlap study

A method that seeks to define a common area of brain damage relevant to a given behavioural deficit by overlaying the scan-defined lesions of multiple subjects with the behavioural deficit in question.

PET activation paradigm

An experimental paradigm that uses PET to measure changes in cerebral perfusion in response to a stimulus.

Magnetoencephalography

(MEG). A method of measuring physiological activity across the cortex by detecting pertubations in the magnetic field that is generated by the electrical activity of neuronal populations.

Voxel-based morphometry

A voxel-by-voxel analysis of structural-image data, most commonly the grey-matter segments extracted from T1-weighted MRI.

Conjunction analysis

A statistical method used in functional brain imaging research for identifying brain regions that are significantly activated in two or more separate experimental conditions.

Connectionist model

A form of computational model used to understand cognitive processes by simulating the flow of activation among simple, neuron-like processing units through weighted, synapse-like connections.

Normative property-listing studies

Studies in which participants are given the name of a category or item (for example, 'bird' or 'robin') and asked to list as many properties as they can think of that characterize it. The proportion of participants that list any particular property serves as an index of the property's importance to the concept.

Drawing-to-name

A non-verbal method of investigating a person's knowledge of objects in which the participant is given a concept name (for example, 'camel') and asked to draw the corresponding object.

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Patterson, K., Nestor, P. & Rogers, T. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 8, 976–987 (2007). https://doi.org/10.1038/nrn2277

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