Elsevier

Neuropsychologia

Volume 35, Issue 4, 28 February 1997, Pages 559-566
Neuropsychologia

The functional anatomy of verbal initiation and suppression using the Hayling Test

https://doi.org/10.1016/S0028-3932(96)00104-2Get rights and content

Abstract

This study utilised positron emission tomography (PET) to identify the cortical areas involved in verbal initiation and suppression in normal subjects whilst performing a sentence completion test (the Hayling Test). In the first condition (response initiation) subjects were required to complete a sentence from which the last word was omitted, whereas in the second condition (response suppression) subjects were asked to complete a sentence with a word which made no sense in the context of the sentence. Subjects were also required to perform a control task in which they had to read out the last word of given sentences. Compared to the control task, response initiation was associated with left-sided activation of the frontal operculum, inferior frontal gyrus, middle temporal gyrus and the right anterior cingulate gyrus, whereas response suppression was associated with left frontal operculum, inferior frontal gyrus and right anterior cingulate gyrus activation. The difference in activation between the two conditions of the Hayling Test lay in the increased activation of the left middle temporal gyrus and the left inferior frontal gyrus during response initiation. ©1997 Elsevier Science Ltd. All rights reserved.

Introduction

Verbal initiation and suppression are two of the many cognitive skills which are believed to be subserved by the frontal lobes. Evidence in support of the anatomical areas attributed to these skills stems from clinical studies which have reported patients with frontal lesions to have deficits on tasks calling on these abilities 3, 16, 17. These studies all reported that patients with left frontal lesions produced far fewer words on the Verbal Fluency Test (VFT) than patients with lesions elsewhere in the brain. Problems of this sort can be described as problems with response initiation. However this interpretation is by no means certain as Perret [23]has argued that the VFT calls on similar cognitive processing demands to the Stroop task despite their differing formats (VFT requires the generation of words within a specific category whereas the Stroop Test requires inhibition of competing responses). Perret's study of 118 patients with circumscribed lesions showed that patients with left frontal lesions were impaired on word fluency as well as a modified version of the Stroop Test. More importantly however, he found correlations of performance on the two tests to be highest in the left frontal group. Perret explained this finding by arguing that when patients perform a word search according to an initial letter, they are being asked to “suppress the habit of using words according to meaning”. In fluency tasks subjects are asked to generate words (or whatever) in a particular category. Such a task necessarily has two components; activating words within the category and suppressing words outside the category. As Perrett points out, generating words by an initial letter requires the suppression of the stronger semantic associations. However, even when generating words in a semantic category, some semantic associations may have to be suppressed. For example, the word HORSE may activate the word CART, but this word would not be appropriate for the category of living things. This analysis emphasises the close relationship between initiation and suppression in fluency tasks.

Some studies have shown that when suppression skills are tapped more specifically, patients with frontal lesions are impaired. Drewe [6]found that patients with frontal lesions were impaired on a `go, no–go' task where the subject is required to withhold responses to one or two stimuli. However she found no difference between left and right frontal lesion patients. Verfaillie and Heilman [29]in a case study of two patients with differing medial frontal lesions observed that, in a task where they had to respond with the opposite hand to the one touched, the patient with the left frontal lesion performed normally whereas the right frontal patient did not. This was also the case during a response preparation task where the patient with the left frontal lesion like the controls benefited from preparatory information whereas the right frontal patient did not.

Clearly studies have shown that frontal lesions can cause impairments on tests of response initiation and suppression and, depending on the specific features of the test (verbal or spatial), both left and right sites have been implicated. Some of the functional implications of these lesion studies have been supported and extended with the advent of functional imaging. For example the studies of both Pardo et al. [21]and Bench et al. [2]using positron emission tomography (PET) with normal subjects have identified frontal regions, in particular the anterior cingulate, which was activated during performance of the Stroop Test. Similarly Frith et al. [14]using a verbal fluency task have observed regional activation including both the anterior cingulate and left dorsal lateral prefrontal cortex (DLPFC), with a reciprocal deactivation of activity in the superior temporal gyrus when compared with a control task involving word repetition.

It is possible that both initiation and suppression are related skills, subserved by similar but overlapping subsystems and functional regions. The problem of comparing these cognitive skills is that the usual tests which examine these, (e.g. verbal fluency, Stroop tasks) differ widely in their characteristics. Recently Burgess and Shallice [5], have devised a task which examines initiation and suppression with minimal changes in the characteristics of the two components of the task. In this test sentences are presented with the last word omitted. In the first condition the subject has to provide an ending to the sentence which makes sense in the context (initiation). In the second condition the subject must provide a word which makes no sense in the context of the sentence. In this condition the obvious response must be suppressed or inhibited (suppression). Both parts of the test are performed poorly by patients with frontal lesions (both left and right), but not by patients with lesions elsewhere [5]. Schizophrenic patients have also been shown to perform poorly on this test [18].

Posner and Snyder [25]have suggested that there are two distinct processes underlying retrieval of items from long-term memory and there is much experimental work supporting this position In relation to single word processing [19]. The two processes are `spreading activation' which is automatically elicited by stimuli and strategic, conscious attention, similar to Shallice's supervisory attentional system [20]which can be facilitatory or inhibitory. The production of a response in the various tasks we have discussed will depend on both these two processes. In the first part of the Hayling Test, appropriate words are likely to be retrieved through the automatic association process caused by the presentation of the sentence and there is relatively little need for strategic processes. However, in the second part of the test where an inappropriate word has to be found there will be a major role for strategic processes.

In addition to verbal fluency, a number of word generation tasks have been studied with PET 3, 27, 30, which involve similar processes to the Hayling task. For example in the Warburton et al. study [30]the subject was required to produce verbs for given nouns (e.g. cake–eat). However, although the results have differed from study to study due largely to design factors, there is some convergence for activations of lateral frontal regions, although there are differences over the precise locations. Involvement of the left temporal lobe has also been demonstrated, where both increases and decreases in rCBF have been observed. The precise role of this region is however unclear and seems to depend on the nature of the task. In the Warburton et al. study [30]they identified this region, in particular the posterior part of the left temporal lobe as being involved in the lexical and semantic components of analysis needed to perform this task. It therefore seems reasonable to suppose that any task that makes similar demands will also produce activation of this region. If Perret's [23]suggestion that both the Stroop and verbal fluency tests have similar processing demands are correct, there should be some convergence of regions of activation in the Hayling Test with those observed in previous functional imaging studies where the verbal fluency and Stroop tests have been used as it encompasses the features of both. In particular, activation of the anterior cingulate should be observed on both parts of the test due to its proposed role in tasks calling on the supervisory attentional system [20]as should the left temporal region since word retrieval is required in this task.

Section snippets

Subjects

Six normal male volunteers were recruited for this study. The ages ranged between 19 and 36 years of age. All were right-handed as assessed by the Annett handedness questionnaire [1]and none had any significant medical or psychiatric history. All gave informed consent. The procedure for administering radioactivity was approved by the local ethics committee and approval to administer radioisotope was granted by the Administration of Radioactive Substances Advisory Committee (ARSAC) U.K.

Activation task

The main

Results

All experimental conditions were firstly compared to the rest condition (see Table 1). Both parts of the Hayling Test showed significant activation of the occipital cortex, left frontal operculum and the inferior frontal gyrus. Significant activation was also seen in the left middle temporal gyrus during part A of the Hayling Test and in the precentral gyrus during part B. Relative to the reading condition, Part A produced activation in the left frontal operculum, left inferior frontal gyrus,

Discussion

The results of this study show that when compared with a control reading task, both forms of the Hayling Test are associated with activation in 3 areas, the left frontal Operculum, the left inferior frontal gyrus and the right anterior cingulate. The difference in activation patterns between parts A and B of the Hayling Test (initiation and suppression) were restricted to the increase in activity in the middle temporal gyrus and the left inferior frontal gyrus (Brodmann's area 44/6) during

Acknowledgements

The authors wish to thank the six subjects for their much appreciated participation in this study. We would also like to thank the radiographers Graham Lewington and Andy Blyth for their help and the MRC Cyclotron Unit for the use of their facilities. Thanks also to Drs Richard Wise and Paul Burgess and Professors Richard Frackowiak and Tim Shallice for their discussions and comments on the manuscript. Finally, our thanks to Professor Maria Ron for her continued support. C. D. Frith and P.

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