Head-free eye tracking, and efficient receptive field mapping in the marmoset

The marmoset has emerged as a promising primate model system, in particular for visual neuroscience. Many common experimental paradigms rely on head fixation and a sustained period of eye fixation during the presentation of salient visual stimuli. Both of these behavioral requirements can be challenging for marmosets. Here, we present two methodological developments to overcome these difficulties. First, we show that it is possible to use a standard eye tracking system without head fixation to assess visual behavior in the marmoset. Eye tracking quality from head-free animals is sufficient to measure precise psychometric functions from a visual acuity task. Secondly, we introduce a novel method for efficient receptive field mapping that does not rely on moving stimuli but uses fast flashing annuli and wedges. We present data recorded in areas V1 and V6 and show that receptive field locations are readily obtained within a short period of recording time. Thus, the methodological advancements presented in this work will contribute to establish the marmoset as a valuable model in neuroscience.

[1]  J. O’Keefe,et al.  Two Distinct Types of Eye-Head Coupling in Freely Moving Mice , 2020, Current Biology.

[2]  Kazuhiko Seki,et al.  Transgenic Monkey Model of the Polyglutamine Diseases Recapitulating Progressive Neurological Symptoms , 2017, eNeuro.

[3]  Cory T. Miller,et al.  Spatial encoding in primate hippocampus during free navigation , 2019, PLoS biology.

[4]  Diederick C. Niehorster,et al.  What to expect from your remote eye-tracker when participants are unrestrained , 2017, Behavior Research Methods.

[5]  Junichi Ushiba,et al.  Calcium Transient Dynamics of Neural Ensembles in the Primary Motor Cortex of Naturally Behaving Monkeys. , 2018, Cell reports.

[6]  David S. Greenberg,et al.  Rats maintain an overhead binocular field at the expense of constant fusion , 2013, Nature.

[7]  S Treue,et al.  Standardized automated training of rhesus monkeys for neuroscience research in their housing environment. , 2018, Journal of neurophysiology.

[8]  Samuel G. Solomon,et al.  A simpler primate brain: the visual system of the marmoset monkey , 2014, Front. Neural Circuits..

[9]  Alexander C. Huk,et al.  Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context , 2018, Proceedings of the National Academy of Sciences.

[10]  Mario Fiorani,et al.  Automatic mapping of visual cortex receptive fields: A fast and precise algorithm , 2014, Journal of Neuroscience Methods.

[11]  Nicholas G Hatsopoulos,et al.  A platform for semi-automated voluntary training of common marmosets for behavioral neuroscience. , 2020, Journal of neurophysiology.

[12]  Lorenz Pammer,et al.  Comparative approaches to cortical microcircuits , 2016, Current Opinion in Neurobiology.

[13]  Evan D. Remington,et al.  An Operant Conditioning Method for Studying Auditory Behaviors in Marmoset Monkeys , 2012, PloS one.

[14]  Trevor B. Poole,et al.  An ethogram of the common marmoset (Calithrix jacchus jacchus): General behavioural repertoire , 1976, Animal Behaviour.

[15]  John H. Reynolds,et al.  Active Vision in Marmosets: A Model System for Visual Neuroscience , 2014, The Journal of Neuroscience.

[16]  Samuel U. Nummela,et al.  Psychophysical measurement of marmoset acuity and myopia , 2017, Developmental neurobiology.

[17]  Sandra Macedo-Ribeiro,et al.  Structure of mycobacterial maltokinase, the missing link in the essential GlgE-pathway , 2015, Scientific Reports.

[18]  Ruigang Yang,et al.  Model-based head pose tracking with stereovision , 2002, Proceedings of Fifth IEEE International Conference on Automatic Face Gesture Recognition.

[19]  Cory T. Miller,et al.  Optogenetic manipulation of neural circuits in awake marmosets. , 2016, Journal of neurophysiology.

[20]  Diego Vidaurre,et al.  Transient visual pathway critical for normal development of primate grasping behavior , 2018, Proceedings of the National Academy of Sciences.

[21]  Helen Shen,et al.  Precision gene editing paves way for transgenic monkeys , 2013, Nature.

[22]  R. Reid,et al.  Receptive field structure varies with layer in the primary visual cortex , 2005, Nature Neuroscience.

[23]  Kazuhiko Seki,et al.  Generation of transgenic marmosets using a tetracyclin-inducible transgene expression system as a neurodegenerative disease model† , 2017, Biology of Reproduction.

[24]  K. Servick Why are U.S. neuroscientists clamoring for marmosets? , 2018, Science.

[25]  E. J. Tehovnik,et al.  Eye Movements Modulate Visual Receptive Fields of V4 Neurons , 2001, Neuron.

[26]  David A. Leopold,et al.  fMRI in the awake marmoset: Somatosensory-evoked responses, functional connectivity, and comparison with propofol anesthesia , 2013, NeuroImage.

[27]  Brad A. Chadwell,et al.  Effects of support diameter and compliance on common marmoset (Callithrix jacchus) gait kinematics , 2016, Journal of Experimental Biology.

[28]  M. Tovée,et al.  Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. , 1994, Journal of neurophysiology.

[29]  Yunyan Wang,et al.  Distinct Subthreshold Mechanisms Underlying Rate-Coding Principles in Primate Auditory Cortex , 2016, Neuron.

[30]  M. A. MacIver,et al.  Neuroscience Needs Behavior: Correcting a Reductionist Bias , 2017, Neuron.

[31]  Yi Zhou,et al.  Rapid Head Movements in Common Marmoset Monkeys , 2020, iScience.

[32]  A. Gail,et al.  A cage-based training, cognitive testing and enrichment system optimized for rhesus macaques in neuroscience research , 2017, Behavior research methods.

[33]  E. S. Pearson,et al.  THE USE OF CONFIDENCE OR FIDUCIAL LIMITS ILLUSTRATED IN THE CASE OF THE BINOMIAL , 1934 .

[34]  Marisa Carrasco,et al.  Attentional enhancement of spatial resolution: linking behavioural and neurophysiological evidence , 2013, Nature Reviews Neuroscience.

[35]  Y. Okazaki,et al.  A non-human primate model of familial Alzheimer’s disease , 2020, bioRxiv.

[36]  M. Rosa,et al.  A twisted visual field map in the primate cortex predicted by topographic continuity , 2019, bioRxiv.

[37]  Xiaoqin Wang,et al.  Wireless multi-channel single unit recording in freely moving and vocalizing primates , 2012, Journal of Neuroscience Methods.

[38]  Xiaoqin Wang,et al.  Subthreshold Activity Underlying the Diversity and Selectivity of the Primary Auditory Cortex Studied by Intracellular Recordings in Awake Marmosets , 2019, Cerebral cortex.

[39]  B. Graham,et al.  PII: S0042-6989(98)00189-8 , 1998 .

[40]  Ignace T. C. Hooge,et al.  The area-of-interest problem in eyetracking research: A noise-robust solution for face and sparse stimuli , 2016, Behavior research methods.

[41]  Katarzyna Harezlak,et al.  Guidelines for the Eye Tracker Calibration Using Points of Regard , 2014 .

[42]  Sergey L. Gratiy,et al.  Real-time spike sorting platform for high-density extracellular probes with ground-truth validation and drift correction , 2017, bioRxiv.

[43]  Chia-Chun Hung,et al.  Functional Mapping of Face-Selective Regions in the Extrastriate Visual Cortex of the Marmoset , 2015, The Journal of Neuroscience.

[44]  H. Okano,et al.  Common marmoset as a new model animal for neuroscience research and genome editing technology , 2014, Development, growth & differentiation.

[45]  Kazuhiko Seki,et al.  Decoding of muscle activity from the sensorimotor cortex in freely behaving monkeys , 2019, NeuroImage.

[46]  Steven J. Eliades,et al.  Journal of Neuroscience Methods Chronic Multi-electrode Neural Recording in Free-roaming Monkeys , 2022 .

[47]  M. Shadlen,et al.  The effect of stimulus strength on the speed and accuracy of a perceptual decision. , 2005, Journal of vision.

[48]  Edmund T Rolls,et al.  The Receptive Fields of Inferior Temporal Cortex Neurons in Natural Scenes , 2003, The Journal of Neuroscience.

[49]  Kevin M. Cury,et al.  DeepLabCut: markerless pose estimation of user-defined body parts with deep learning , 2018, Nature Neuroscience.

[50]  Tristan A. Chaplin,et al.  Representation of the visual field in the primary visual area of the marmoset monkey: Magnification factors, point‐image size, and proportionality to retinal ganglion cell density , 2013, The Journal of comparative neurology.

[51]  Matthias Bethge,et al.  Using DeepLabCut for 3D markerless pose estimation across species and behaviors , 2018 .

[52]  Teppei Ebina,et al.  Arm movements induced by noninvasive optogenetic stimulation of the motor cortex in the common marmoset , 2019, Proceedings of the National Academy of Sciences.

[53]  S. Dumoulin,et al.  The Relationship between Cortical Magnification Factor and Population Receptive Field Size in Human Visual Cortex: Constancies in Cortical Architecture , 2011, The Journal of Neuroscience.

[54]  Hans-Werner Gellersen,et al.  Pursuit calibration: making gaze calibration less tedious and more flexible , 2013, UIST.

[55]  Joseph S. Gati,et al.  Integrated radiofrequency array and animal holder design for minimizing head motion during awake marmoset functional magnetic resonance imaging , 2019, NeuroImage.

[56]  C. H. Summers,et al.  Putting the “Biology” Back into “Neurobiology”: The Strength of Diversity in Animal Model Systems for Neuroscience Research , 2016, Front. Syst. Neurosci..

[57]  H. Gu,et al.  Large-Scale Brain Networks in the Awake, Truly Resting Marmoset Monkey , 2013, The Journal of Neuroscience.

[58]  Risa Kawai,et al.  A Fully Automated High-Throughput Training System for Rodents , 2013, PloS one.

[59]  Melina E. Hale,et al.  Toward Diversification of Species Models in Neuroscience , 2019, Brain, Behavior and Evolution.

[60]  Judith M Burkart,et al.  Common marmosets show social plasticity and group-level similarity in personality , 2015, Scientific Reports.

[61]  Marcus Nyström,et al.  Eye tracker data quality: what it is and how to measure it , 2012, ETRA.

[62]  Jonathan Winawer,et al.  The HCP 7T Retinotopy Dataset: Description and pRF Analysis , 2018, bioRxiv.

[63]  Michael Breakspear,et al.  Naturalistic Stimuli in Neuroscience: Critically Acclaimed , 2019, Trends in Cognitive Sciences.

[64]  Naoyuki Matsumoto,et al.  Tonically Active Neurons in the Primate Caudate Nucleus and Putamen Differentially Encode Instructed Motivational Outcomes of Action , 2004, The Journal of Neuroscience.

[65]  Jonathan Winawer,et al.  The Human Connectome Project 7 Tesla retinotopy dataset: Description and population receptive field analysis , 2018, Journal of vision.

[66]  H. Okano,et al.  Human-specific ARHGAP11B increases size and folding of primate neocortex in the fetal marmoset , 2020, Science.

[67]  M. Carrasco Visual attention: The past 25 years , 2011, Vision Research.

[68]  Cory T. Miller,et al.  Motion dependence of smooth pursuit eye movements in the marmoset. , 2015, Journal of neurophysiology.

[69]  S. Ferrari Predation Risk and Antipredator Strategies , 2009 .

[70]  L. Populin Monkey Sound Localization: Head-Restrained versus Head-Unrestrained Orienting , 2006, The Journal of Neuroscience.

[71]  Michael M Yartsev,et al.  The emperor’s new wardrobe: Rebalancing diversity of animal models in neuroscience research , 2017, Science.

[72]  David A. Leopold,et al.  Marmosets: A Neuroscientific Model of Human Social Behavior , 2016, Neuron.

[73]  David A. Leopold,et al.  The marmoset monkey as a model for visual neuroscience , 2015, Neuroscience Research.

[74]  Christophe Hurter,et al.  Improving eye-tracking calibration accuracy using symbolic regression , 2019, PloS one.

[75]  Attila Losonczy,et al.  Functional Access to Neuron Subclasses in Rodent and Primate Forebrain , 2019, Cell reports.

[76]  H. Okano,et al.  Generation of transgenic non-human primates with germline transmission , 2009, Nature.

[77]  Ueli Rutishauser,et al.  Simultaneous Eye Tracking and Single-Neuron Recordings in Human Epilepsy Patients. , 2019, Journal of visualized experiments : JoVE.

[78]  Lauren K. Hayrynen,et al.  Functional Localization of the Frontal Eye Fields in the Common Marmoset Using Microstimulation , 2019, The Journal of Neuroscience.

[79]  C. Galletti,et al.  Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex , 2009, The Journal of Neuroscience.

[80]  W. M. Keck,et al.  Highly Selective Receptive Fields in Mouse Visual Cortex , 2008, The Journal of Neuroscience.

[81]  Erika Sasaki,et al.  Generation of transgenic marmosets expressing genetically encoded calcium indicators , 2016, Scientific Reports.

[82]  Stefan Everling,et al.  Methods for chair restraint and training of the common marmoset on oculomotor tasks. , 2018, Journal of neurophysiology.

[83]  D. Ringach Mapping receptive fields in primary visual cortex , 2004, The Journal of physiology.

[84]  Nicholas G. Hatsopoulos,et al.  A platform for semi-automated voluntary training of common marmosets for behavioral neuroscience: Voluntary training of common marmosets , 2019 .