Effects of orbital frontal lesions on aversive and aggressive behaviors in rhesus monkeys.

Abstract

Rhesus monkeys were tested for emotional reactions to human observers and to animal-like objects (doll and snake) before and after removal of orbital frontal (OF) or portions of temporal neocortex (T). The OF lesions, but not T lesions, initially produced hyporeactivity and anorexia, followed by hyperreactivity to environmental stimulation and heightened oral tendencies. The OF monkeys, unlike those with T lesions, showed increased frequencies of certain aversive reactions to the doll initially following surgery and reduced frequencies of aggressive reactions in all test situations as late as 10 mo. following surgery. The critical focus for producing deficits in aggression appears to be the posteromedial sector of OF cortex. This decrease in aggression is situationally dependent and may reflect an impairment in the modulation of arousal mechanisms.In the course of testing monkeys with orbital frontal (OF) ablations in an instrumental learning situation (Butter, Mishkin, & Rosvold, 1963), the present authors observed abnormalities in emotional behavior, abnormalities not seen following resections of other neocortical areas. These emotional alterations appeared, at least to casual observation, to be striking and long lasting. For this reason, and because the particular role of frontal cortex in the control of emotionality is unclear (Brutkowski, 1965), a systematic investigation of these alterations was undertaken. In an initial experiment, monkeys with OF lesions, along with operated and unoperated controls, were tested for aversive and aggressive responses to human observers, whose presence tends to elicit strong emotional reactions from rhesus monkeys. Compared to their controls, the OF monkeys showed more frequent aversive reactions and, to a smaller extent, less frequent aggressive reauthors express their thanks to Kirsten McEnaney for her assistance in testing the animals and data analysis and to Raymond Jaeger for histological analyses.

Positron Emission Tomography of Regional Brain Metabolic Responses to a Serotonergic Challenge in Major Depressive Disorder with and without Borderline Personality Disorder

“…We did not find a difference in the orbitofrontal cortical area between depressed patients with BPD and MDD without BPD in contrast to findings from both lesion (Butter et al, 1970;Grafman et al, 1996;Heinrichs, 1989;Raleigh et al, 1979) and neuroimaging studies (De La Fuente et al, 1997;Goyer et al, 1994;New et al, 2002New et al, , 2004Siever et al, 1999) that suggest a role for the orbitofrontal cortex in impulsive aggression. Our sample of depressed women with BPD did not differ significantly in terms of clinical measures of aggression and impulsivity from the depressed women without BPD (see Table 1).…”

“…Lesion studies suggest that control of aggression may be mediated by the anterior cingulate gyrus and orbitofrontal region (Butter et al, 1970;Grafman et al, 1996;Heinrichs, 1989;Raleigh et al, 1979). Functional neuroimaging studies of brain glucose metabolism in borderline and other aggressive and impulsive patients have also implicated the anterior cingulate area.…”

Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys

“…Our results contrast with previous reports (Butter et al, 1970;Butter and Snyder, 1972) in which monkeys with PFo damage were reported to show a decrease in aggression and an increase in avoidance behavior in response to human observers. These different results could be related to differences in the degree of familiarity of human observers or low interrater reliability for behavioral scoring (Butter et al, 1968(Butter et al, , 1970.…”

“…This set of findings is seemingly at odds with the evidence for functional interactions of the amygdala and the PFo in other settings (Baxter et al, 2000;Schoenbaum et al, 2003). To further complicate matters, yet other studies (Butter et al, 1970;Butter and Snyder, 1972) report an overall reduction in aggressive behaviors in monkeys with PFo lesions in the presence of a human observer and somewhat less of a reduction in aggression in response to a doll or snake.…”

“…Another commonly used tool relies on monkeys responses to an unfamiliar human observer. Early investigations by Butter et al (1968Butter et al ( , 1970 found evidence of increased defensive behaviors in monkeys with PFo lesions in response to a human observer and a doll but not in response to a fake snake. In contrast, Kalin et al (2001) found that monkeys with bilateral amygdala lesions displayed fewer defensive behaviors in the presence of a snake but not in response to a human observer.…”