The effect of cingulate lesions on social behaviour and emotion

Abstract

Functional and structural neuroimaging of the human cingulate cortex has identified this region with emotion and social cognition and suggested that cingulate pathology may be associated with emotional and social behavioural disturbances. The importance of the cingulate cortex for emotion and social behaviour, however, has not been clear from lesion studies. Bilateral lesions in the cingulate cortex were made in three macaques and their social interactions were compared with those of controls. Subsequently, cingulate lesions were made in the three controls and their behaviour was compared before and after surgery. Cingulate lesions were associated with decreases in social interactions, time spent in proximity with other individuals, and vocalisations but an increase in manipulation of an inanimate object. The results are consistent with a cingulate role in social behaviour and emotion.

Introduction

It is widely held that the cingulate cortex processes emotional and social information. For this reason when changes in cingulate blood flow or neuroanatomy have been identified in patients with depression [49] or autism [1] the findings have been thought important for understanding the nature and origins of these illnesses. There is, however, some uncertainty about the role of the cingulate cortex in normal social behaviour and emotion [18], [19], [28], [40], [45], [56], [61], [68]. The ready identification of cingulate cortex with emotion is partly a consequence of its historical association with Papez’s circuit [50] and its anatomical connexions with the amygdala (85) which has a clearly established role in emotion [2], [3], [7], [8], [9], [33], [34], [43]. Direct evidence that the cingulate cortex itself is concerned with emotion and social behaviour is more difficult to evaluate.

Several studies have recorded changes in blood flow and blood oxygenation level (BOLD) signal (“activations”) in the cingulate cortex when subjects view emotionally arousing images and pictures of angry faces [13], [36] or when subjects participate in some other emotionally arousing condition, such as anxiety induction [54]. Activations are also recorded in cingulate and paracingulate areas when subjects are required to make attributions about the thoughts and beliefs of others in “theory of mind” tasks [25], [27]. These studies, however, can sometimes be difficult to interpret. First, the cingulate cortex is often just part of a wider network of activated areas and the activation changes in the cingulate may be much smaller and less reliable than those recorded in other non-limbic areas of the brain, such as the visual cortex [11]. Second, even when it has been concluded that the cingulate cortex is playing a role in some aspect of emotion it has been pointed out that the activation changes in this region are difficult to interpret because of its high level of resting baseline activity [61]. Third, because cingulate and other medial frontal activations are common in many different tasks their interpretation is not transparent [35], [52], [53].

It is difficult to make definitive conclusions about the role of the cingulate in emotion and social behaviour by studying human patients. It is clear that many patients with emotional and social behavioural disturbances have lesions that include the cingulate cortex [12], [58], [62]. When cerebrovascular accidents in the territory of the anterior cerebral artery damage the cingulate cortex, however, they also tend to damage the orbitofrontal cortex [19]. Any changes in emotion or social behaviour are often attributed to orbitofrontal damage because it is clear from studies of lesions in monkeys that this region is important in emotion and social behaviour [34] and in reinforcement processing [10], [26]. Cingulate lesions have been made in patients with severe psychiatric illnesses and it is reported that in some cases these have lead to amelioration of emotional pathology [19]. The unusual pre-surgical behaviour in such cases, however, can make interpretation of the lesion effect difficult.

In the case of other brain structures linked with emotion, such as the amygdala, similar issues have been addressed by the making of lesions in non-human primates [3], [8], [22]. In the case of the cingulate cortex, however, the literature concerning the effects of lesions in the monkey brain is older and more confusing. Reviews of early studies have found evidence that cingulate lesions led to social and emotional impairments but have also highlighted some reports where no deficits were found [18], [66]. It is clear, however, that the naming conventions used to describe cingulate areas, particular anterior and ventral areas, has varied over time and between researchers. The extent to which the more anterior and ventral cingulate divisions are included within lesions has varied considerably. Neuroimaging results, however, consistently emphasise the importance of just such cingulate regions for emotion [14]. In addition, the testing procedures that have been used in earlier studies have been very varied and are sometimes merely anecdotal.

In the present investigation, we have addressed the role of the cingulate cortex in social behaviour and emotion by attempting to make more complete lesions of the anterior cingulate gyrus in cynomologus macaques. We took care to include the cingulate regions rostral and ventral to the corpus callosum that can be difficult to access. We have assessed any impairments using procedures based on those used by other investigators to identify the social and emotional role of the amygdala in lesion studies [7], [9], [23]. In the first experiment, we looked at the behaviour of pairs of monkeys with cingulate lesions and compared it to the behaviour of pairs of control monkeys. We recorded vocalisations, gestures, interactions, time spent with a novel object and time spent in proximity to one another. In the first experiment, both animals were able to move freely throughout the testing area (Fig. 1a). In experiment 2, we attempted to confirm the measurements of time spent in proximity when one animal was constrained to a sub-section of the apparatus and only the second monkey was free to move throughout the apparatus (Fig. 1b). Experiment 3 used a similar procedure to experiment 1 but in this case a comparison was made between the pre- and post-operative performances of the same animals.