The Physiological Effect of Human Grooming on the Heart Rate and the Heart Rate Variability of Laboratory Non-Human Primates: A Pilot Study in Male Rhesus Monkeys

Abstract

Grooming is a widespread, essential, and complex behavior with social and affiliative valence in the non-human primate world. Its impact at the autonomous nervous system level has been studied during allogrooming among monkeys living in a semi-naturalistic environment. For the first time, we investigated the effect of human grooming to monkey in a typical experimental situation inside laboratory. We analyzed the autonomic response of male monkeys groomed by a familiar human (experimenter), in terms of the heart rate (HR) and heart rate variability (HRV) at different body parts. We considered the HRV in both the time (SDNN, RMSSD, and RMSSD/SDNN) and the frequency domain (HF, LF, and LF/HF). For this purpose, we recorded the electrocardiogram of two male rhesus monkeys seated in a primate chair while the experimenter groomed their mouth, chest, or arm. We demonstrated that (1) the grooming carried out by a familiar human determined a decrement of the HR and an increment of the HRV; (2) there was a difference in relation to the groomed body part. In particular, during grooming the mouth the HRV was higher than during grooming the arm and the chest. Taken together, the results represent the first evidence that grooming carried out by a familiar human on experimental monkeys has the comparable positive physiological effect of allogrooming between conspecifics. Moreover, since the results underlined the positive modulation of both HR and HRV, the present study could be a starting point to improve the well-being of non-human primates in experimental condition by means of grooming by a familiar person.

Using imaging photoplethysmography for heart rate estimation in non-human primates

“…In our study estimated pulse rates were in the range of 95–125 BPM for monkey Sun, 125–150 BPM for Fla and 160–230 BPM for Mag, which agrees with previously reported values of heart rate (120-250 BPM) for rhesus monkeys sitting in a primate chair [2, 35–37]. Performance of our method for pulse rate estimation (Table 5) was only slightly worse than those reported for humans: mean absolute error obtained in [75] was 2.5 BPM; fraction of epochs with error below 6 BPM (about 8% of average human pulse rate) for the best method considered in [45] was achieved for 87% of epochs; reported values of the Pearson correlation coefficient vary from 0.87 in [45] to 1.00 in [25].…”

Short-term reciprocity in macaque’s social decision-making

“…Future studies should take these observations into consideration, especially when performances in juice reward allocation tasks are taken as a proxy of macaque's social motivation in neuroscience (Azzi et al, 2012;Chang et al, 2011). To overcome these methodological and conceptual challenges and study exchanges of positive acts under experimental condition in primates, the use of grooming by the experimenters (or by a dedicated device) might be considered in further investigations (Grandi and Ishida, 2015;Taira and Rolls, 1996). To conclude, by using both positive and negative outcomes, this study has clarified the apparent dichotomy within the scientific literature of reciprocity in nonhuman primates.…”

A Potential Role for mu-Opioids in Mediating the Positive Effects of Gratitude

“…Allogrooming settles in-group tensions, maintains social bonds, reinforces social hierarchies, and provokes reciprocal prosocial behavior in the form of reciprocal grooming, food sharing, or coalitionary support (de Waal, 1997; Akinyi et al, 2013; Jaeggi and Gurven, 2013; Lutermann et al, 2013; Borgeaud and Bshary, 2015; Garrido et al, 2016; Richard et al, 2016). The parallels between the effects of allogrooming and the effects of gratitude on social behavior are apparent, and a possible link between the social effects of allogrooming and physiology emerges from the observation that when an individual is being groomed, they visibly relax and their heart rate decreases significantly (Grandi and Ishida, 2015). …”