A neural basis for collecting behaviour in humans

Abstract

Collecting behaviour is commonplace in the normal population, but there has been little investigation of its neural basis in humans. The observation that collecting behaviour can assume pathological proportions in patients with certain patterns of brain damage led us to hypothesize that dysfunction in a system encompassing mesial prefrontal cortices accounts for abnormal collecting and may guide normal collecting. We tested the hypothesis in 86 subjects with focal lesions of the telencephalon, by relating the neuroanatomical placement of the lesions to the presence of repetitive and indiscriminate acquisition behaviour and impaired discard behaviour. The subjects had no history of psychiatric disease or abnormal collecting behaviour prior to lesion onset. Lesions were analysed with high-resolution three-dimensional MRI. Collecting behaviour was evaluated with a standardized questionnaire completed by a close relative of each subject. Thirteen subjects exhibited abnormal collecting, characterized by massive and disruptive accumulation of useless objects. In all cases, the abnormality of collecting behaviour was severe and persisted despite attempted interventions and obvious negative consequences. There were no differences between pathological collectors and non-collectors on tests of executive functions or anterograde memory. All subjects with pathological collecting behaviour had damage to the mesial frontal region (including the right polar sector and the anterior cingulate), but there was no damage to most of the subcortical structures that, in species such as rodents, are known to drive the acquisition and retention of objects. The evidence suggests that damage to the mesial frontal region disrupts a mechanism which normally modulates subcortically driven predispositions to acquire and collect, and adjusts these predispositions to environmental context.