Neuropsychological studies of patients with acquired semantic impairments have yielded two distinct and contrasting patterns of performance in a spoken-word/picture matching task (Warrington & Cipolotti, 1996). Patients labeled "access/refractory" are strongly influenced by presentation rate, semantic relatedness of distractors, and repetition, yet they seem relatively unaffected by lexical frequency. "Degraded-store" patients, on the other hand, are strongly affected by lexical frequency but not by presentation rate, semantic relatedness, or repetition.

In our theoretical account of this pattern of data, language processes maintain and integrate semantic information over time, thereby compensating for the natural tendency of cortical neurons to habituate. Damage to parts of the language system responsible for semantic maintenance/integration has the effect of leaving semantic representations vulnerable to cortical habituation - producing the "access/refractory" pattern. Damage to semantic representations themselves leaves the compensation spared, producing the "degraded-store" pattern.

Warrington (1975) documented patients with temporal lobe atrophy sparing medial structures ("semantic dementia") who exhibited selective semantic deficits. Comprehension performance was better for objects with high-frequency names.

Warrington & Shallice (1979) documented a patient whose reading performance was highly inconsistent and unaffected by frequency, yet the patient could access some semantic information about words he couldn't read. They proposed criteria to distinguish between patients with impaired semantic access processes and patients with degraded representations.

Warrington & McCarthy (1983; 1987) studied globally aphasic patients who seemed to fit with the "access" pattern: Their performance on a spoken-word/picture matching task was poor under conditions of fast presentation rate, multiple repetitions of trials and semantically close distractors.

Rapp & Caramazza (1993) criticized the empirical validity of the "access/degraded-store" distinction, pointing out that no patient had been tested with all of the criteria and that a number of "mixed" patterns had also been observed. They argued that the distinction would be of little use until more specific theoretical claims were made about the nature of representations and access procedures.

Warrington & Cipolotti (1996) responded to the criticism of poor empirical validity, showing that two sets of patients do indeed present with a contrasting pattern of impairment.

Patients:

Two globally aphasics (A1, A2) with wide-spread damage of the left hemisphere (more frontal in A1, more posterior in A2), largely sparing temporal cortex.

Four "semantic dementia" patients (S1-S4), all with focal atrophy of the left temporal lobe.

Task:

Spoken-word/picture matching (point to a picture in an array of 4 that matches the word spoken by the experimenter).

Design:

Response-Stimulus Interval (1 sec vs. 15 secs), Semantic Relatedness (Close vs. Distant), and Lexical Frequency (High vs. Low) were completely crossed, and each condition was tested in a blocked fashion. A block consisted of 3 repetitions of all 4 pictures in an array, probed in pseudorandom order.

Language processing requires the maintenance and integration of semantic information over time. Given numerous observations that neurons in the brain habituate (i.e. show a response decrement) under conditions of repeated stimulation, sustaining semantic information should be particularly difficult.

In order to effectively perform language comprehension and production, we propose that neurons in temporal cortex which participate in coding semantic information compensate for habituation by learning to use interactions with other cortical areas (perhaps frontal and posterior parietal areas).

We suggest that the "access/refractory" patients have damage to areas which help to sustain and integrate semantic information over time, unmasking the normal compensation of semantic habituation. For these patients, word/picture matching performance should be most impaired in the conditions expected to maximize habituation of semantic information (e.g. fast rate, semantically close distractors, and multiple repetitions). Frequency should have a relatively small effect because the factors driving poor performance are less related to frequency (how many neurons are shared across semantically similar representations).

We would claim that "degraded-store" patients, on the other hand, have damage to semantic representations themselves. They shouldn't be affected as much by rate of presentation and repetition because the cortical areas compensating for semantic habituation are largely spared. Frequency should matter more because the neurons coding semantic information provide top-down support for earlier levels of processing (e.g. phonology). Damage may weaken the support to the extent that correct performance is affected. Low frequency words will be most affected because the inputs are particularly weak. Semantic relatedness might also be expected to matter for these patients, although if damage is severe enough, a within-category manipulation might have no effect.

Decremented responses of motor neurons in Aplysia following repeated stimulation of the sensory neurons at different ISI's (Panel A: Byrne, 1982). The data are modeled (Panel B) with transmitter depletion and inactivation of Ca++ channels.

Recordings from neurons in inferior temporal cortex of anesthetized macaque monkeys during the repeated presentation of common objects at different ISI's.

Recordings from anesthetized and awake monkeys performing a passive viewing task.

Rather than modeling spoken-word/picture matching, per se, we modeled only the auditory word comprehension aspects of the task. This is partially motivated by the observation that "access/refractory" patients on record tend to perform at ceiling on picture/picture matching.

Short-term bias added to the netinput of each unit in the network:

stbias_j(t) = -c * a_j(t-1) + lambda * stbias_j(t-1)

where c is the "buildup parameter, lambda is the "decay" parameter, and a_j(t-1) is the activation of unit j at time t-1. The values of c and lambda were constrained to be the same for all units in the network. (See Staddon & Higa, 1996, for a similar modeling approach.)

Input Patterns:

a "word" is a temporal sequence of 2 phonological patterns or "phonemes"

8 unique phonemes (4/12 units on for each) 32 total words were constructed from the 8 phonemes.

Target Patterns:

32 semantic patterns (5/20 units on for each) forming 2 non-overlapping categories (16 members each)

In each category, 8 patterns are "closely" related (on average, share 3.875 "on" units with category prototype), and 8 are "distantly" related (share 2.375 "on" units with category prototype).

Each semantic pattern is paired at random with an input "word".

The network was trained with a continuous, temporal version of backpropagation discussed in Pearlmutter (1989).

Half of the 32 training patterns were assigned to be high frequency (presented twice as often during training) and half low frequency.

Time Course of a Single Training Pattern:

RSI's were biased to be short if members from the same category followed each other.

Results:

After approximately 30,000 passes through the training set, the network performed at 91% correct (on best-match criterion described in "Testing Procedure").

"Access/refractory" damage:

randomly removed connections between cleanup and semantics

"Degraded-Store" damage:

randomly removed semantic units

Damage was sampled to produce a comparable level of performance to that of the patients and matched performance for the two types of damage. Each lesion severity explored was repeated 20 times to insure a stable estimate of performance.

Each lesioned network was presented with 4 types of arrays of 4 words each, as in Warrington & Cipolotti (1996): Close/HF, Close/LF, Distant/HF, Distant/LF.

In each testing block, all 4 words in one of the arrays were probed 3 times in a pseudorandom order and at a fixed RSI (either 2 or 30 time units).

Each array was presented at both a fast rate and a slow rate.

The pattern of semantic activity generated by an input word was compared with the target semantic patterns of all the words in the array. The best match was taken to be the network's response (chance performance = 25% correct).

A connectionist model which is trained to maintain and integrate semantic information and which incorporates the principle of neural habituation is capable of accounting for the basic pattern of data associated with the "access/ degraded-store" distinction. While the model is capturing all of the relevant effects, some of the effects are not sufficiently strong in magnitude (e.g. the frequency effect, under "degraded-store" damage). Current modeling efforts are aimed at providing a better fit to the data.

Because the theorizing relies on neural habituation as a principle of the normal cognitive system, it may be possible to tie together seemingly unrelated phenomena in experiments with normal subjects, as well as other effects in brain-injured populations. We are currently attempting to extend this account to the phenomena of semantic satiation, verbal transformation, and priming (semantic and repetition) in normal subjects, and perseverative naming errors in aphasic patients. If successful, the theory should be able to make testable predictions in neuroimaging experiments, as well as in behavioral studies.

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