Brain Vol. 128 No. 1 © Guarantors of Brain 2005; all rights reserved
From the Archives
‘Utilization behaviour’ and its relation to lesions of the frontal lobes. by F. Lhermitte (From the Clinique de Neurologie et de Neuropsychologie, Hôpital de la Salpê.trière, 47, Boulevard de l'Hôpital, 75013, Paris, France.) Brain 1983; 106: 237–255.Lhermitte takes as his starting point the contralateral grasp reflex resulting from frontal lobe lesions, tracing its history from Wilson and Walshe (1914) and Adie and Critchley (1927)—see above—to Derek Denny Brown's concept of ‘magnetic apraxia’ in which unilateral frontal release of parietal function leads to crossed grasping in response to tactile and visual stimuli (N C Med J 1956; 17: 295–303 and J Nerv Mental Dis 1958; 36: 35–117). But Lhermitte went further, carrying forward the simple notion of an irrepressible motor response routed through the corticospinal pathways to a more general concept in which ‘manual grasping behaviour’ occurs in the context of uni- or bilateral frontal lobe lesions: ‘the presentation of everyday objects within the reach of the hands or field of vision impels the patient to grasp and use them. We suggest calling this utilization behaviour’. From a series of >40 cases observed between 1963 and 1982, Lhermitte described in detail five cases with utilization behaviour. A patient with right frontal damage from subarachnoid haemorrhage showed transient bilateral grabbing of food and households objects; bilateral frontal and anterior callosal lesions were demonstrated at autopsy. A left frontal arteriovenous malformation was followed by transient postoperative aphasia and utilization behaviour for food and household items. Surgery for a tumour in the anterior part of the third ventricle led to a right frontal lesion with transient contralateral neglect but bilateral utilization behaviour for household items. A right frontal occlusive stroke was followed by dense left hemiplegia, but the right arm showed irrepressible handling of available objects. Abnormal behaviour drew attention to a right frontal glioma with contralateral neglect and utilization behaviour such that the patient placed three pairs of glasses on his nose. Challenged on the purpose of these behaviours, the patients replied: ‘you held out objects to me: I thought I had to use them’.
Lhermitte had already established that normal Parisians, assessed under similar circumstances to the patients, are not tempted to manipulate food, cutlery and cigarettes but respond politely and courteously to the somewhat silly opportunities presented. Questioned about the stimuli, they rationalized the situation thus: ‘you examined the sensitivity of my skin; you were probably looking for something but I don't know what’. A member of the audience at the Société Française de Neurologie, where the syndrome was first presented in 1981, behaved with impeccable motor restraint. So, this was a sign of neurological disease in which patients instinctively grasp, with puzzlement, the first object and then use the second (related) item to perform the behaviour: pen and paper lead to uncontrollable writing; knife and apple to peeled fruit and eating; cigarette and lighter to a smoke. The actions are without internal motivation, subjects eating and drinking immediately after lunch, and writing without wishing to convey meaning. But there are inhibitions. These patients rarely responded ‘to the offer of a urinal’.
In reaching a position on utilization behaviour, Lhermitte drew on evidence for comparable responses following cortical stimulation of the anterior cingulate, but manifesting rather restricted manual and buccal responses unlike the utilization of one or more objects in a complex (and under other circumstances appropriate) behaviour. The activity is not compulsive since the pace of response is slow and measured. The limited pathological opportunities prevented precise clinico-anatomical localization, but utilization behaviour is only associated with lesions of the frontal lobes, or, more precisely, the anterior pole and orbital surface. Why the behaviours in Lhermite's series were transient in patients with fixed structural lesions remained unexplained.
Lhermitte did not favour the connectionist model of Denny Brown who had reduced magnetic apraxia to the disruption of circuits involving prefrontal–parietal–motor cortex pathways, since utilization behaviour was bilateral, complex and utilitarian, combining grasp and use, and not associated with the more primitive sucking movements that characterized Denny Brown's experimental and clinical examples. Whilst sympathetic to the ‘charming’ metaphor of magnetism, Lhermitte did not really consider his patients to be apractic. Rather ‘all the information coming from the body and from the outside world is received in areas of the sensory cortex which surround the parietal lobe; systems develop in the parietal area which unite these unending sequences of stimuli. These systems activate other unknown patterns and prepare the response of the patient. The result is that the normal activity of the parietal lobe tends to create links of dependence between the subject and stimuli from the environment while some of the functions of the frontal lobe allow the subject to remain aloof from the outside world and to ensure his independence by modulating and inhibiting the activities of the parietal cortex. Perhaps it is not such a large step from the mesial frontal localization of lesions responsible for grasping and utilization behaviour to the anatomy of ‘normal’ and ‘abnormal’ collecting in humans.
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