Active vision during prey capture in wild marmoset monkeys

Victoria Ngo, Julia C. Gorman, María Fernanda De la Fuente, Antonio Souto, Nicola Schiel, Cory T. Miller

Current Biology · 2022 · 42 citations · 22 references

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A foundational pressure in the evolution of all animals is the ability to travel through the world, inherently coupling the sensory and motor systems. While this relationship has been explored in several species,1Kleinfeld D. Ahissar E. Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system.Curr. Opin. Neurobiol. 2006; 16: 435-444https://doi.org/10.1016/j.conb.2006.06.009Crossref PubMed Scopus (282) Google Scholar, 2Parker P.R.L. Brown M.A. Smear M.C. Niell C.M. Movement-related signals in sensory areas: roles in natural behavior.Trends Neurosci. 2020; 43: 581-595https://doi.org/10.1016/j.tins.2020.05.005Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 3Wachowiak M. All in a sniff: olfaction as a model for active sensing.Neuron. 2011; 71: 962-973https://doi.org/10.1016/j.neuron.2011.08.030Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar, 4Gibson E.J. The Ecological Approach to Visual Perception. Houghton Mifflin, 1979Google Scholar it has been largely overlooked in primates, which have typically relied on paradigms in which head-restrained subjects view stimuli on screens.5Leopold D.A. Park S.H. Studying the visual brain in its natural rhythm.Neuroimage. 2020; 216: 116790https://doi.org/10.1016/j.neuroimage.2020.116790Crossref PubMed Scopus (19) Google Scholar Natural visual behaviors, by contrast, are typified by locomotion through the environment guided by active sensing as animals explore and interact with the world,4Gibson E.J. The Ecological Approach to Visual Perception. Houghton Mifflin, 1979Google Scholar,6Schroeder C.E. Wilson D.A. Radman T. Scharfman H. Lakatos P. Dynamics of active sensing and perceptual selection.Curr. Opin. Neurobiol. 2010; 20: 172-176https://doi.org/10.1016/j.conb.2010.02.010Crossref PubMed Scopus (355) Google Scholar a relationship well illustrated by prey capture.7Palleroni A. Miller C.T. Hauser M. Marler P. Predation: prey plumage adaptation against falcon attack.Nature. 2005; 434: 973-974https://doi.org/10.1038/434973bCrossref PubMed Scopus (32) Google Scholar, 8Lin H.-T. Leonardo A. Heuristic rules underlying dragonfly prey selection and interception.Curr. Biol. 2017; 27: 1124-1137https://doi.org/10.1016/j.cub.2017.03.010Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 9Mischiati M. Lin H.-T. Herold P. Imler E. Olberg R. Leonardo A. Internal models direct dragonfly interception steering.Nature. 2015; 517: 333-338https://doi.org/10.1038/nature14045Crossref PubMed Scopus (157) Google Scholar, 10Michaiel A.M. Abe E.T. Niell C.M. Dynamics of gaze control during prey capture in freely moving mice.Elife. 2020; 9: e57458https://doi.org/10.7554/elife.57458Crossref PubMed Scopus (0) Google Scholar, 11Wagner H. Kettler L. Orlowski J. Tellers P. Neuroethology of prey capture in the barn owl (Tyto alba L.).J. Physiol. Paris. 2013; 107: 51-61https://doi.org/10.1016/j.jphysparis.2012.03.004Crossref PubMed Scopus (21) Google Scholar, 12Hoy J.L. Yavorska I. Wehr M. Niell C.M. Vision drives accurate approach behavior during prey capture in laboratory mice.Curr. Biol. 2016; 26: 3046-3052https://doi.org/10.1016/j.cub.2016.09.009Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar Here, we characterized prey capture in wild marmoset monkeys as they negotiated their dynamic, arboreal habitat to illustrate the inherent role of vision as an active process in natural nonhuman primate behavior. Not only do marmosets share the core properties of vision that typify the primate Order,13Mitchell J.F. Reynolds J.H. Miller C.T. Active vision in marmosets: a model system for visual neuroscience.J. Neurosci. 2014; 34: 1183-1194https://doi.org/10.1523/jneurosci.3899-13.2014Crossref PubMed Google Scholar, 14Mitchell J.F. Leopold D.A. The marmoset monkey as a model for visual neuroscience.Neurosci. Res. 2015; 93: 20-46https://doi.org/10.1016/j.neures.2015.01.008Crossref PubMed Scopus (118) Google Scholar, 15Mitchell J.F. Priebe N.J. Miller C.T. Motion dependence of smooth pursuit eye movements in the marmoset.J. Neurophysiol. 2015; 113: 3954-3960https://doi.org/10.1152/jn.00197.2015Crossref PubMed Scopus (20) Google Scholar, 16Coop S.H. Yates J.L. Mitchell J.F. Foveal remapping of motion in area MT of the marmoset monkey.J. Vis. 2021; 21: 2638https://doi.org/10.1167/jov.21.9.2638Crossref Google Scholar, 17Hori Y. Cléry J.C. Selvanayagam J. Schaeffer D.J. Johnston K.D. Menon R.S. Everling S. Interspecies activation correlations reveal functional correspondences between marmoset and human brain areas.Proc. Natl. Acad. Sci. USA. 2021; 118 (e2110980118)https://doi.org/10.1073/pnas.2110980118Crossref Scopus (6) Google Scholar, 18Hung C.C. Yen C.C. Ciuchta J.L. Papoti D. Bock N.A. Leopold D.A. Silva A.C. Functional mapping of face-selective regions in the extrastriate visual cortex of the marmoset.J. Neurosci. 2015; 35: 1160-1172https://doi.org/10.1523/jneurosci.2659-14.2015Crossref PubMed Google Scholar but they are prolific hunters that prey on a diverse set of prey animals.19Schiel N. Souto A. Huber L. Bezerra B.M. Hunting strategies in wild common marmosets are prey and age dependent.Am. J. Primatol. 2010; 71: 1-8Google Scholar, 20Schiel N. Souto A. The common marmoset: an overview of its natural history, ecology and behavior.Dev. Neurobiol. 2017; 77: 244-262https://doi.org/10.1002/dneu.22458Crossref PubMed Scopus (53) Google Scholar, 21Digby L. Barreto C.E. Vertebrate predation in common marmosets.Neotrop. Primates. 1998; 6: 124-126Google Scholar, 22Souto A. Bezerra B.M. Schiel N. Huber L. Saltatory search in free-living Callithrix jacchus: environmental and age influences.Int. J. Primatol. 2007; 28: 881-893https://doi.org/10.1007/s10764-007-9165-1Crossref Scopus (22) Google Scholar Marmosets pursued prey using vision in several different contexts, but executed precise visually guided motor control that predominantly involved grasping with hands for successful capture of prey. Applying markerless tracking for the first time in wild primates yielded novel findings that precisely quantified how marmosets track insects prior to initiating an attack and the rapid visually guided corrections of the hands during capture. These findings offer the first detailed insight into the active nature of vision to guide multiple facets of a natural goal-directed behavior in wild primates and can inform future laboratory studies of natural primate visual behaviors and the supporting neural processes.

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