Noun imageability and the temporal lobes

Abstract

We used positron emission tomography to investigate brain activity in response to hearing or reading nouns of varying imageability. Three experiments were performed. Activity increased with noun imageability in the left mid-fusiform gyrus, the lateral parahippocampal area in humans, and in the rostral medial temporal lobes close to or within perirhinal cortex. The left mid-fusiform activation has been observed in previous imaging studies of single word processing. Its functional significance was variously attributed to semantic processing, visual imagery, encoding episodic memories, or the integration of lexical inputs from different sensory modalities. These hypotheses are not mutually exclusive. The more rostral medial lobe response to noun imageability has not been observed previously. However, lesions in perirhinal cortex impair knowledge about objects in non-human primates, and bilateral rostral ventromedial temporal lobe potentials in response to object nouns were observed with human intracranial recordings. Imageable (object) nouns are learnt with reference to sensory experiences of living and non-living objects, whereas acquisition of the meaning of low imageable (abstract) nouns is more dependent on their context within sentences. Parahippocampal and perirhinal cortices are reciprocally connected with, respectively, second and third order sensory association cortices. We conclude that access to the representations of word meaning is dependent on heteromodal temporal lobe cortex, and that during the acquisition of object nouns one route is established through ventromedial temporal cortical regions that have reciprocal connections with all sensory association cortices.

Introduction

Long-term explicit memories result from interactions between neocortex and medial temporal lobe structures [12], [16]. Within the medial temporal lobe, the parahippocampal and perirhinal cortices have strong reciprocal connections with second-order and third-order association cortices, respectively, and their output is to entorhinal cortex, the hippocampus and the amygdala [7], [19], [35]. Knowledge about the material world, one form of explicit memory, is acquired predominantly through our senses. Therefore, it seems plausible that during brain development and the acquisition of language, one route to long-term knowledge about the meaning of nouns that refer to objects and their attributes is through heteromodal medial temporal cortex with close anatomical connections to sensory association cortices. However, many nouns do not refer to objects. Low imageable nouns, which refer to abstract concepts, are acquired later in life [3], [18]. Knowledge about their meaning, in the absence of direct sensory correlates, is more reliant on their context within sentences [33]. Throughout our lives we remain more proficient with concrete nouns [23], [31] — most of us find it easier to define the differences between rhinoceros and hippopotamus than between charity and altruism. The ‘concreteness’ effect may be exaggerated by disease. Aphasic stroke patients, with damage over the lateral surface of the left hemisphere, commonly show relative preservation of object noun retrieval and comprehension [13], [20]. The reverse dissociation has been observed infrequently (e.g. [2], [34], [38], [39]), and in many of the patients the pathology was usually diffuse and bilateral (degenerative disease or necrosis following herpes simplex encephalitis). Nevertheless, the evidence from the lesion literature is that access to knowledge about object and abstract words is not evenly distributed within temporal lobe cortex.

The experiments described here systematically investigated the relationship between the imageability of nouns (a psychological rating scale along which nouns vary parametrically between concrete and abstract) and regional cerebral blood flow (an indirect physiological measure of net synaptic activity). Imageability is not apparent in a noun’s phonetic/orthographic or lexical structure, and so any regional physiological difference results from access to knowledge about object and abstract words. Measurements were made using positron emission tomography (PET) and radiolabelled water (H₂¹⁵O) as tracer.