Positive and negative factors in movement control:: A current review of Denny-Brown's hypothesis

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Abstract

In his extensive writings, Denny-Brown hypothesized that two competitive 'tropisms,' one positive (exploratory) and one negative (withdrawal) act to coordinate normal movements at all levels of the neuraxis. Lesions in particular areas of the central nervous system result in disequilibrium between these tropisms, leading to disorders of posture and movement, including involuntary movements. The tactile manifestations of unbalanced exploratory tropisms are grasping responses, whereas the complementary withdrawal tropisms are avoiding responses. In Denny-Brown's view, at the level of the cerebral cortex, grasping responses result from frontal lobe injury whereas avoiding responses result from parietal lobe lesions. In this report we review Denny-Brown's conceptions of positive and negative tropisms, their anatomical loci, and whether his hypothesis has merit in a contemporary approach to brain function. We find that Denny-Brown's view on the anatomical loci associated with these behaviors is incomplete, but that the idea of conflicting behavioral tendencies is valuable for understanding and managing some neurological and perhaps also psychiatric disorders. For example, his hypothesis offers an important perspective in understanding the paradoxical success of stereotaxic surgery to alleviate the symptoms of Parkinson's disease.

Introduction

Derek E. Denny-Brown, one of the foremost neurologists of this century, brought to clinical neurology a physiologist's perspective of both the normal functioning of the nervous system and the responses of the nervous system to injury (Denny-Brown, 1952). The conceptual framework of his work included an overall scheme of motor system organization that included positive (exploratory) and negative (withdrawal) 'tropisms' (Denny-Brown, 1956, Denny-Brown, 1966, Denny-Brown and Chambers, 1958, Langworthy, 1970) that he believed were analogous to the conflict between excitation and inhibition at the cellular level (Chambers, personal communication). Denny-Brown hypothesized that a balance between the positive and negative tropisms is required for smoothly constituted movement. Further, he thought the generation of purposive movement required reflex function as a component of the response to refined stimuli (Denny-Brown, 1956, Denny-Brown, 1966, Langworthy, 1970).

Denny-Brown suggested that central nervous system (CNS) lesions lead to disequilibrium between the residual portions of the tropisms, and this disequilibrium is manifested in 'release' of abnormal movements (reflexes and automatisms) that are associated with the newly dominant tropism at that level (Denny-Brown, 1950). At the cortical level, positive tropisms, typified by grasping behaviors, were thought to appear (be 'released') after frontal lobe lesions whereas negative or withdrawal tropisms, typified by avoiding behaviors, were released after parietal lobe lesions. Denny-Brown viewed higher level exploratory functions as organized and controlled by the parietal lobe, and withdrawal behaviors as organized and controlled by the frontal lobe. Denny-Brown's ideas on the anatomical regions controlling these behaviors were based on observations in patients with neurological disorders and his extensive ablation studies in non-human primates (Denny-Brown and Chambers, 1958, Denny-Brown and Botterell, 1948, Rushworth and Denny-Brown, 1959).

In this paper we review Denny-Brown's conceptions of the different types of exploratory and avoiding responses that may result from imbalances in positive and negative tropisms at various levels of the neuraxis. We also review the literature pertaining to grasping and avoiding behaviors in patients to show that Denny-Brown's ideas on the anatomical loci for grasping and avoiding behaviors in humans need to be modified because of recent data. It appears that grasping and perhaps also avoiding behaviors can be released by both focal and diffuse lesions in many different CNS regions. Although Denny-Brown's ideas on the functional localization of positive and negative factors should be updated and modified, his hypothesis that motor behavior is organized around competitive but balanced reflex responses continues to have merit, explaining some puzzling clinical findings, such as the success of stereotaxic surgery for Parkinsonism.

Section snippets

Definitions

With each of Denny-Brown's definitions we also present a figure taken from the patient films in the Denny-Brown collection of research materials (Vilensky et al., 1994). In some cases we used enlargements of the same frames of film used by Denny-Brown in his original papers on grasping and avoiding.

Available data

Table 1 summarizes the available data on grasping responses beginning with the report by Seyffarth and Denny-Brown (1948)(consult that paper for earlier reports), including information on the methods used to identify lesion loci. The data suggest that grasping and/or utilization phenomena are often associated with contralateral or ipsilateral frontal lobe (especially medial frontal lobe) lesions, but also may be associated with retrolandic, temporal lobe, subcortical or thalamic lesions.

Positive and negative tropisms

Although Denny-Brown's views on the anatomical loci associated with grasping and avoiding behaviors were probably incomplete, the idea that there are competitive (i.e. positive and negative) motor behavioral tendencies that can result from lesions at many levels of the neuraxis continues to be useful for understanding the behavior of patients.

Yakolev (1954)considered the terminal flexion posture of the trunk and upper and lower limbs that is seen in the final phases of severe disorders (e.g.

Motor recovery after stereotaxic lesions for Parkinson's disease

A resurgence of interest in stereotaxic surgery to improve the symptoms of Parkinsonism has occurred recently. This interest has been triggered by: (1) the progressive disability that occurs over time; (2) the limited effects of levo-dopa in the late stages of disease; (3) the development of techniques that allow precise lesion localization; and (4) better understanding of basal ganglia physiology (Wichman and DeLong, 1993, Olanow, 1996). Although improved comprehension of basal ganglia

Conclusions

Grasping and avoiding behaviors are abnormal responses to environmental stimuli that occur in the mature nervous system subsequent to brain injury. These responses can be observed after both focal and diffuse lesions in various brain regions. Although the different variants of these behaviors are associated with lesions of specific neuroanatomical loci, qualitatively identical behaviors have been observed after injury to different regions.

Denny-Brown's use of positive and negative tropisms to

Acknowledgements

This work was supported, in part, by the National Institute of Neurological Disorders and Stroke (PHS NS33782).

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