Mapping the contribution of single muscles to facial movements in the rhesus macaque

Abstract

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans, chimpanzees and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans and chimpanzees were stimulated successfully in the rhesus macaque and caused similar appearance changes. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from those of a monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.

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.