Emotional responses toward humans in monkeys with selective frontal lesions

Butter, Charles M.; Mishkin, Mortimer; Mirsky, Allan F.

doi:10.1016/0031-9384(68)90087-5

Cited by 45 publications

(26 citation statements)

References 8 publications

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“…The frequency of tooth grinding recorded after surgery also correlated negatively with the amount of damage to areas 11 and 13. These deficits are consistent with several previous experiments in monkeys with large ventral frontal lobe lesions that examined reactivity to a human intruder (Butter et al, 1968; 1970; Butter and Snyder, 1972), although these studies did not specifically report tooth grinding. Our results are also consistent with human functional neuroimaging studies demonstrating heightened orbital frontal activity to angry facial expressions (an unambiguous indicator of threat, similar to direct eye contact for macaques) relative to expressions of sadness (Blair et al, 1999).…”

Section: Discussionsupporting

confidence: 91%

“…This finding is consistent with a recent report by Kalin and colleagues (2007) that also tested animals before and after surgery. Other similar studies (Butter et al, 1968; Izquierdo et al, 2005) measured emotional reactivity only after surgery and did not find freezing deficits for monkeys with orbital frontal lesions. It is possible that freezing deficits in the current study and in the experiment by Kalin and colleagues (2007) were significantly influenced by unintended damage to the agranular insular area (Carmichael and Price, 1994).…”

Section: Discussionmentioning

confidence: 75%

“…Nonhuman primate studies have also linked the amygdala (Aggleton and Passingham, 1981; Zola-Morgan et al, 1991; Meunier et al, 1999; Kalin et al, 2001; Prather et al, 2001; Stefanacci et al, 2003; Izquierdo and Murray, 2004; Kalin et al, 2004; Mason et al, 2006; Antoniadis et al, 2007), hippocampus (Chudasama et al, 2008) and orbital frontal cortex (Butter et al, 1968; Butter et al, 1970; Butter and Snyder, 1972; Izquierdo et al, 2005; Kalin et al, 2007) to normal emotional reactivity, especially towards potential predators or a staring human. We also found that bilateral amygdala or orbital frontal lesions in monkeys altered behavioral responses to threatening social signals (Machado and Bachevalier, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Behavioral and hormonal reactivity to threat: Effects of selective amygdala, hippocampal or orbital frontal lesions in monkeys

Machado

Bachevalier

2008

Psychoneuroendocrinology

100

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SummaryWe compared the effects of bilateral amygdala, hippocampal or orbital frontal cortex lesions on emotional and hormonal reactivity in rhesus monkeys (Macaca mulatta). Experiment 1 measured behavioral reactivity to an unfamiliar human intruder before and after surgery. Animals with amygdala lesions demonstrated decreases in one passive defensive behavior (freezing), whereas animals with hippocampal lesions showed decreases in a more stimulus-directed defensive behavior (tooth grinding). Orbital frontal cortex lesions also reduced these two defensive behaviors, as well as decreased cage-shaking dominance displays. Animals with amygdala, hippocampal or sham lesions also demonstrated increased tension-related behaviors after surgery, but those with orbital frontal lesions did not. Finally, all three lesions diminished the operated animals' ability to modulate tension-related behaviors depending on the magnitude of threat posed by the human intruder. Experiment 2 measured circulating levels of cortisol and testosterone when a subset of these same animals were at rest and following physical restraint, temporary isolation, exposure to threatening objects and social interactions with an unfamiliar conspecific. None of the lesions impacted on testosterone levels in any condition. Amygdala or orbital frontal lesions blunted cortisol reactivity during isolation from peers, but not during any other condition. Hippocampal lesions did not alter circulating levels of cortisol under any conditions. These results indicate that the amygdala, hippocampus and orbital frontal cortex play distinct, yet complimentary roles in coordinating emotional and hormonal reactivity to threat.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 75%

Section: Introductionmentioning

confidence: 99%

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Behavioral and hormonal reactivity to threat: Effects of selective amygdala, hippocampal or orbital frontal lesions in monkeys

Machado

Bachevalier

2008

Psychoneuroendocrinology

100

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“…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. Regardless, the present study is the first to show different effects of PFo and amygdala damage on responses to social stimuli.…”

Section: Responses To a Human Intrudermentioning

confidence: 59%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Izquierdo¹,

Suda²,

Murray³

2005

J. Neurosci.

178

203

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The present study examines the effects of bilateral orbital prefrontal cortex (PFo) lesions on monkeys' emotional responses in two different contexts: in the presence of a rubber snake and in the presence of a human intruder. For comparison, we also assessed the responses of rhesus monkeys with selective amygdala lesions on these same tasks. Monkeys with PFo lesions, like those with amygdala lesions, displayed blunted emotional responses to the fake snake. Unlike monkeys with amygdala lesions, however, monkeys with PFo lesions displayed more mild aggression than controls in the presence of a human intruder. The findings support the idea that the PFo helps integrate sensory signals in the service of choosing among competing responses. In addition, they point to a divergence of the roles of the PFo and amygdala in responding to a social stimulus, the human intruder.

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EVidence for dorsolateral and orbital prefrontal cortical involvement in the expression of aggressive behavior

Giancola¹

1995

Aggr. Behav.

136

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Numerous studies have implicated the role of the prefrontal cortex in the expression of aggressive behavior. However, the nature of this relationship remains poorly understood. As such, the purpose of this article is to review both the animal and human literature pertaining to prefrontal cortical functioning and aggression in an attempt to help clarify this relationship. Particular attention is paid to differentiating the functions of the dorsolateral and the orbital regions of the prefrontal cortex in the expression of aggression. Evidence was garnered from four different types of studies: 1) those examining aggressive behavior in animals following ablations to the prefrontal cortex; 2) those examining aggressive behavior in humans following surgical and accidental lesions to the prefrontal cortex; 3) those examining prefrontal cortical functioning in individuals with psychiatric disorders characterized by aggression; and 4) those relating prefrontal cortical functioning to human aggressive behavior in laboratory situations. The general conclusion of this article is that the dorsolateral region of the prefrontal cortex is more likely to be involved in the expression of physical aggression whereas the orbital region is more likely to be involved in the expression of what is termed herein “disinhibited‐nonaggressive” behavior. © 1995 Wiley‐Liss, Inc.

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Emotional responses toward humans in monkeys with selective frontal lesions

Cited by 45 publications

References 8 publications

Behavioral and hormonal reactivity to threat: Effects of selective amygdala, hippocampal or orbital frontal lesions in monkeys

Behavioral and hormonal reactivity to threat: Effects of selective amygdala, hippocampal or orbital frontal lesions in monkeys

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

EVidence for dorsolateral and orbital prefrontal cortical involvement in the expression of aggressive behavior

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