Development of an Assessment Method for Freely Moving Nonhuman Primates' Eating Behavior Using Manual and Deep Learning Analysis

Overview

Journal Heliyon

Specialty Social Sciences

Date 2024 Feb 15

PMID 38356587

Authors

Leslie Jaesun Ha

Meelim Kim

Hyeon-Gu Yeo

Inhyeok Baek

Keonwoo Kim

Miwoo Lee

Youngjeon Lee

Hyung Jin Choi

Affiliations

Soon will be listed here.

Abstract

Purpose: Although eating is imperative for survival, few comprehensive methods have been developed to assess freely moving nonhuman primates' eating behavior. In the current study, we distinguished eating behavior into appetitive and consummatory phases and developed nine indices to study them using manual and deep learning-based (DeepLabCut) techniques.

Method: The indices were utilized to three rhesus macaques by different palatability and hunger levels to validate their utility. To execute the experiment, we designed the eating behavior cage and manufactured the artificial food. The total number of trials was 3, with 1 trial conducted using natural food and 2 trials using artificial food.

Result: As a result, the indices of highest utility for hunger effect were approach frequency and consummatory duration. Appetitive composite score and consummatory duration showed the highest utility for palatability effect. To elucidate the effects of hunger and palatability, we developed 2D visualization plots based on manual indices. These 2D visualization methods could intuitively depict the palatability perception and hunger internal state. Furthermore, the developed deep learning-based analysis proved accurate and comparable with manual analysis. When comparing the time required for analysis, deep learning-based analysis was 24-times faster than manual analysis. Moreover, temporal and spatial dynamics were visualized via manual and deep learning-based analysis. Based on temporal dynamics analysis, the patterns were classified into four categories: early decline, steady decline, mid-peak with early incline, and late decline. Heatmap of spatial dynamics and trajectory-related visualization could elucidate a consumption posture and a higher spatial occupancy of food zone in hunger and with palatable food.

Discussion: Collectively, this study describes a newly developed and validated multi-phase method for assessing freely moving nonhuman primate eating behavior using manual and deep learning-based analyses. These effective tools will prove valuable in food reward (palatability effect) and homeostasis (hunger effect) research.

References

Bala P, Eisenreich B, Yoo S, Hayden B, Park H, Zimmermann J . Automated markerless pose estimation in freely moving macaques with OpenMonkeyStudio. Nat Commun. 2020; 11(1):4560. PMC: 7486906. DOI: 10.1038/s41467-020-18441-5. View

Barra B, Conti S, Perich M, Zhuang K, Schiavone G, Fallegger F . Epidural electrical stimulation of the cervical dorsal roots restores voluntary upper limb control in paralyzed monkeys. Nat Neurosci. 2022; 25(7):924-934. DOI: 10.1038/s41593-022-01106-5. View

Diaz M, Wilson M, Howell L . Effects of long-term high-fat food or methamphetamine intake and serotonin 2C receptors on reversal learning in female rhesus macaques. Neuropsychopharmacology. 2018; 44(3):478-486. PMC: 6333825. DOI: 10.1038/s41386-018-0200-z. View

Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey M, Baker M . The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. J Cereb Blood Flow Metab. 2020; 40(9):1769-1777. PMC: 7430098. DOI: 10.1177/0271678X20943823. View

von Ziegler L, Sturman O, Bohacek J . Big behavior: challenges and opportunities in a new era of deep behavior profiling. Neuropsychopharmacology. 2020; 46(1):33-44. PMC: 7688651. DOI: 10.1038/s41386-020-0751-7. View

Gosztolai A, Gunel S, Lobato-Rios V, Pietro Abrate M, Morales D, Rhodin H . LiftPose3D, a deep learning-based approach for transforming two-dimensional to three-dimensional poses in laboratory animals. Nat Methods. 2021; 18(8):975-981. PMC: 7611544. DOI: 10.1038/s41592-021-01226-z. View

Snyder A, Yu B, Smith M . A Stable Population Code for Attention in Prefrontal Cortex Leads a Dynamic Attention Code in Visual Cortex. J Neurosci. 2021; 41(44):9163-9176. PMC: 8570836. DOI: 10.1523/JNEUROSCI.0608-21.2021. View

Rolls E, Sienkiewicz Z, Yaxley S . Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey. Eur J Neurosci. 1989; 1(1):53-60. DOI: 10.1111/j.1460-9568.1989.tb00774.x. View

Watts A, Kanoski S, Sanchez-Watts G, Langhans W . The physiological control of eating: signals, neurons, and networks. Physiol Rev. 2021; 102(2):689-813. PMC: 8759974. DOI: 10.1152/physrev.00028.2020. View

10.

Otani Y, Sawada A, Hanya G . Short-term separation from groups by male Japanese macaques: costs and benefits in feeding behavior and social interaction. Am J Primatol. 2013; 76(4):374-84. DOI: 10.1002/ajp.22241. View

11.

Baxter M, Murray E . The amygdala and reward. Nat Rev Neurosci. 2002; 3(7):563-73. DOI: 10.1038/nrn875. View

12.

Fukuda M, Ono T . Amygdala-hypothalamic control of feeding behavior in monkey: single cell responses before and after reversible blockade of temporal cortex or amygdala projections. Behav Brain Res. 1993; 55(2):233-41. DOI: 10.1016/0166-4328(93)90119-b. View

13.

Berger M, Agha N, Gail A . Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex. Elife. 2020; 9. PMC: 7228770. DOI: 10.7554/eLife.51322. View

14.

Richter C, Gras P, Hodges K, Ostner J, Schulke O . Feeding behavior and aggression in wild Siberut macaques (Macaca siberu) living under low predation risk. Am J Primatol. 2015; 77(7):741-52. DOI: 10.1002/ajp.22393. View

15.

Huang M, Li D, Cheng X, Pei Q, Xie Z, Gu H . The tectonigral pathway regulates appetitive locomotion in predatory hunting in mice. Nat Commun. 2021; 12(1):4409. PMC: 8292483. DOI: 10.1038/s41467-021-24696-3. View

16.

Parker B, Sturm K, MacIntosh C, Feinle C, Horowitz M, Chapman I . Relation between food intake and visual analogue scale ratings of appetite and other sensations in healthy older and young subjects. Eur J Clin Nutr. 2004; 58(2):212-8. DOI: 10.1038/sj.ejcn.1601768. View

17.

Liu S, Iriate-Diaz J, Hatsopoulos N, Ross C, Takahashi K, Chen Z . Dynamics of motor cortical activity during naturalistic feeding behavior. J Neural Eng. 2019; 16(2):026038. PMC: 7367697. DOI: 10.1088/1741-2552/ab0474. View

18.

Torres N, Chabardes S, Piallat B, Devergnas A, Benabid A . Body fat and body weight reduction following hypothalamic deep brain stimulation in monkeys: an intraventricular approach. Int J Obes (Lond). 2012; 36(12):1537-44. DOI: 10.1038/ijo.2011.271. View

19.

HAMILTON C, Ciaccia P, LEWIS D . Feeding behavior in monkeys with and without lesions of the hypothalamus. Am J Physiol. 1976; 230(3):818-30. DOI: 10.1152/ajplegacy.1976.230.3.818. View

20.

Berthoud H, Munzberg H, Morrison C . Blaming the Brain for Obesity: Integration of Hedonic and Homeostatic Mechanisms. Gastroenterology. 2017; 152(7):1728-1738. PMC: 5406238. DOI: 10.1053/j.gastro.2016.12.050. View