Mapping the contribution of single muscles to facial movements in the rhesus macaque
Introduction
The rhesus macaque (Macaca mulatta) is the primary species used in clinical research to model different aspects of human neuropsychiatric disorders. Social communication with facial expression is shared by humans and non-human primates and is profoundly altered in many human disorders, such as Parkinson's disease, schizophrenia, autism, and various manifestations of pain. Monkeys with MPTP-induced parkinsonism, for example, appear to have similarly inexpressive faces as human patients [1], [2], [3], [4] and the efficacy of treatments that improve the clinical symptoms (e.g., deep brain stimulation) can be reflected in improvement in facial muscle tone and expressivity [5]. Thus, comparison between rhesus models and human patients could be highly useful in assessing treatment and progression of the disease. While global facial expressivity has been compared successfully between species (e.g. oro-facial dyskinesia [6]) in a similar manner to other motor symptoms of neuropsychiatric disease (levodopa-induced dyskinesia [7]; bradykinesis [8]; akinesia [9]), we do not have a system in macaques that allows us an objective description of facial movements in the normal or pathological case. Assessing facial expression in terms of homologous component muscle movements is necessary in order to understand the similarities between the human and macaque facial movement systems and to quantify deficits in facial movement in relation to its neuromuscular basis. In order to conduct such studies, it is essential to verify whether similar rhesus macaque and human facial movements share the same underlying muscle contractions.
The literature on the neuromuscular mechanisms that give rise to facial expressions in rhesus macaques is sparse. Early studies (e.g. [10]) claimed that rhesus macaques have less complex and more undifferentiated facial musculature than humans. Recent dissections of facial muscles, however, have found a great degree of similarity between humans and rhesus macaques [11]. These dissections were conducted using a unique method of removing the facial mask from the skull and dissecting this ‘inside-out’ preparation which retains many of the original structures [12]. This method was used successfully to identify the facial muscles in the chimpanzee (Pan troglodytes) and to compare the human and chimpanzee facial architecture with the human face [13]. Based on the known anatomy, the functional similarities were then compared using intramuscular electrical stimulation to document the changes that occur in each muscle [14].
A better understanding of chimpanzee facial movements facilitated the development of a coding system that allows systematic comparative analysis of facial expressions between humans and chimpanzees (Chimpanzee Facial Action Coding System: ChimpFACS [15]). ChimpFACS is an anatomically based system, where each specific muscle contraction is identified as a unit of movement, and is based on FACS (The Facial Action Coding System: [16]), which is the most commonly used objective and standardized coding system in human facial expression research. The development of a similar, objective coding system for the rhesus macaque requires measurements of facial movement in relation to the activation of each anatomically identified muscle. If, as the dissections suggest, rhesus macaques share a similar underlying musculature to both humans and chimpanzees, this technique can be extended to this monkey species to facilitate scientific comparison between facial expressions. Research using monkey models would be greatly aided by the development of a refined, accurate measurement tool for quantifying facial movement and, as this method would offer more detailed and accurate observations, this would also represent an important step in achieving the welfare goals of replacement, reduction and refinement in animal research [17]. Specifically, given that a FACS approach can greatly increase the quality of information gleaned from facial expressions, a small sample of rhesus macaque individuals could yield a rich data set, and animals that are already used in clinical trials could be additionally studied for facial expression deficits.
The objective of the present investigation was to document the facial appearance changes that occur when facial muscles contract in the rhesus macaque. Using intramuscular electrical stimulation techniques, we aimed to 1) record the surface changes during contraction of targeted facial muscles, and 2) compare these contractions to facial movements in humans and chimpanzees using FACS terminology.
Section snippets
Subject
Weak electrical stimulations of individual facial muscles were performed on one anesthetized adult male rhesus macaque aged 7 years. The testing session lasted approximately 1 h. All the procedures and the anesthesia (Ketamine 8 mg/kg for pre-anesthesia and Propofol 200–600 μg/kg/min as a continuous IV drip for anesthesia) were approved by the Institutional Animal Care and Use Committees (IACUC) at the University of Arizona.
Procedures
The subject was positioned supine on a testing table with the head
Results and discussion
The following section combines the results of the current study with comparison to human and chimpanzee facial movements (as documented in [14], FACS [16], and ChimpFACS [15]). Each muscle is first described in terms of gross anatomy [11], followed by a description of how the equivalent muscle moves in humans and chimpanzees. Finally, appearance change on stimulated contraction is described. Movements were classified as AUs if they met the minimum criteria for coding according to the human
Conclusions
The appearance changes associated with each facial muscle movement have been documented and compared to both humans and chimpanzees. The findings have two main implications. First, the facial movements of the rhesus macaque evoked by intramuscular electrical stimulation are highly similar to the base units of movement (AUs) in humans. Thus, the facial muscles we see in humans appear to be a little altered from the format we see in a monkey species, with the exception of the reduction in
Acknowledgements
This research was supported by grant R03MH082282 from NIH (to LAP), NS-39489 from NIH/NINDS (to AJF) and MH070836 (to KMG). We would like to thank Prisca Zimmerman, Robert Gibboni III, and Clayton Mosher (University of Arizona), for help with the experiment, Marc Mehu for providing FACS coding and Paul Waby (University of Portsmouth) for technical assistance. We also thank Tim Smith for producing Fig. 1, and Sarah-Jane Vick for providing FACS coding and extensive and invaluable comments on the
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