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Neuroscience Research on Human Visual Path Integration: Empirical Overview and Strategic Considerations

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Neuroscience Research on Human Visual Path Integration: Empirical Overview and Strategic Considerations Report No. MAE0820 Neuroscience Research on Human Visual Path Integration: Empirical Overview and Strategic Considerations Jimmy Y. Zhong12 1School of Mechanical and Aerospace Engineering (MAE), Nanyang Technological University, Singapore 639798, Singapore 2 GSU/GT Center for Advanced Brain Imaging (CABI), Georgia Institute of Technology, Atlanta, GA 30318, USA Email: [email protected] Report No. MAE0820 1 Foreword 2 3 This manuscript is based on modifications and extensions of copyrighted writings of the author 4 that were previously unpublished in any book or journal. It is intended as a 5 conceptual/theoretical piece of writing and should not be regarded as a research report or article 6 of any kind. All written opinions and recommendations expressed herein belong solely to the 7 author and do not belong to any other person or organization. If deemed useful, please cite and 8 reference this paper in its original form: 9 10 Zhong, J. Y. (2021, August). (Technical Report No. MAE0820). Neuroscience research on 11 human visual path integration: Empirical overview and strategic considerations. School of 12 Mechanical and Aerospace Engineering, Nanyang Technological University, Singapore. 13 https://doi.org/10.31234/osf.io/h6u3b i Report No. MAE0820 14 Abstract 15 16 Over the past two decades, many neuroimaging studies have attempted to uncover the brain 17 regions and networks involved in path integration and identify the underlying neurocognitive 18 mechanisms. Although these studies made inroads into the neural basis of path integration, they 19 have yet to offer a full disclosure of the functional specialization of the brain regions supporting 20 path integration. In this paper, I reviewed notable neuroscientific studies on visual path 21 integration in humans, identified the commonalities and discrepancies in their findings, and 22 incorporated fresh insights from recent path integration studies. Specifically, this paper presented 23 neuroscientific studies performed with virtual renditions of the triangle/path completion task and 24 addressed whether or not the hippocampus is necessary for human path integration. Based on 25 studies that showed evidence supporting and negating the involvement of the hippocampal 26 formation in path integration, this paper introduces the proposal that the use of different path 27 integration strategies may determine the extent to which the hippocampus and entorhinal cortex 28 are engaged during path integration. To this end, recent studies that investigated the impact of 29 different path integration strategies on behavioral performance and functional brain activity were 30 discussed. Methodological concerns were raised with feasible recommendations for improving 31 the experimental design of future strategy-related path integration studies, which can cover 32 cognitive neuroscience research on age-related differences in the role of the hippocampal 33 formation in path integration and Bayesian modelling of the interaction between landmark and 34 self-motion cues. The practical value of investigating different path integration strategies was 35 also discussed briefly from a biomedical perspective. 36 37 Keywords: path integration, strategy, spatial navigation, hippocampus, entorhinal cortex, 38 cognitive neuroscience ii Report No. MAE0820 39 1. Introduction 40 41 In everyday contexts, whenever we have a destination in mind we want to travel to, we 42 rely on our innate adeptness for navigation, as typified by our cognitive ability to reason in 43 space, plan, and execute a path to our desired location (Gallistel, 1990). Navigation generally 44 occurs in the presence of external cues that present themselves ubiquitously in the form of 45 stationary landmarks in our everyday environments but can also proceed when only internal 46 bodily cues are available (i.e., during non-visual self-locomotion, see, e.g., Klatzky et al., 1990; 47 Loomis et al., 1993). The process of estimating distance and directional changes relative to a 48 starting position and integrating such displacements with self-motion cues to compute and update 49 a homing vector is called path integration (also known as dead reckoning) [see, e.g., Gallistel, 50 1990; Mittelstaedt & Mittelstaedt, 1980, 1982; Müller & Wehner, 1988; for reviews, see Etienne 51 & Jeffery, 2004; Loomis, Klatzky, Golledge, & Philbeck, 1999; Loomis, Klatzky, & Golledge, 52 2001; Srinivasan, 2015]. 53 Path integration was first postulated to apply to humans by Darwin (1873), who recounted 54 the remarkable feat in which the natives of North Siberia were able to chart direct courses of 55 return after meandering through icy plains without relying on any visible cues at sea or in the 56 sky, concluding that: 57 58 “We must bear in mind that neither a compass, nor the north star, nor any other such sign, suffices to 59 guide a man to a particular spot through an intricate country, or through hummocky ice, when many 60 deviations from a straight course are inevitable, unless the deviations are allowed for, or a sort of ‘dead 61 reckoning’ is kept.” 62 Darwin (1873, p. 418) 63 64 Subsequent empirical studies showed that this special “dead reckoning” ability is present 65 in a wide variety of animals, encompassing insects (e.g., honey bees, Saharan desert ants), 66 spiders, birds (e.g., pigeons, geese), and mammals (e.g., golden hamsters, gerbils, dogs, humans) 67 [Gallistel, 1990; Mittelstaedt & Mittelstaedt, 1980, 1982; see Etienne & Jeffery, 2004, 68 Srinivasan, 2015, for reviews of path integration in non-human animals; see Loomis et al., 1999, 69 2001, for reviews of path integration in humans]. In the animal kingdom, the perfect example of 70 the ”path integrator” is perhaps the Saharan desert ant, Cataglyphis fortis, which is capable of - 1 - Report No. MAE0820 71 returning in a straight-line path back to its nest after tracking a tortuous outbound path in a 72 featureless landscape to find food (see, e.g., Müller & Wehner, 1988; Wehner & Srinivasan, 73 2003; Wehner & Wehner, 1990) [Fig. 1]. Based on the ant’s foraging and homing behavior, path 74 integration was proposed to enable the navigating animal to compute its movement changes 75 continuously along each step of its outbound journey and integrate such changes with idiothetic 76 signals (derived from the vestibular and proprioceptive systems) to update a homing vector (i.e., 77 a representation of distance and directional estimates from a point of origin) (Müller & Wehner, 78 1988). 79 To date, research on path integration continues to draw the attention of many researchers 80 in spatial cognition due to the possibilities it offers for a better understanding of the basic 81 neurocognitive processes or mechanisms that are involved in spatial perception and cognitive 82 mapping (Burgess, 2014; Hafting, Fyhn, Molden, Moser, & Moser, 2005; Moser, Kropff, & 83 Moser, 2008). 84 Fig. 1 Path integration in Cataglyphis fortis. An ant’s tortuous outbound path (from N to F) and straight homeward path (from F to N, in bold) recorded in a featureless salt pan. [Source: Fig. 1.1 in Wehner & Srinivasan (2003). Reproduced with permission.] 85 86 1.1 Assessing Path Integration in Humans 87 88 The traditional behavioral paradigm used for studying path integration in humans is the 89 path- or triangle-completion task (see, e.g., Klatzky et al., 1990; Loomis et al., 1993; Fukusima, - 2 - Report No. MAE0820 90 Loomis, & Da Silva, 1997; Philbeck, Klatzky, Behrmann, Loomis, & Goodridge, 2001; Sholl, 91 1989). The path completion task, originally developed by Klatzky et al. (1990), requires a 92 participant, donning blindfolds and headphones, to walk two or more straight segments with one 93 or more turns in between under the guidance of the experimenter, and to walk back (or point 94 back) to the origin on his/her initiative at the end of the outbound journey. Triangle completion 95 (Fig. 2) is the popular derivative of this path completion paradigm and refers to participants’ 96 attempts at returning to the origin (or pointing toward it) after traversing two straight segments 97 with one turn (i.e., the whole trajectory forms a triangle) [Klatzky, Loomis, Beall, Chance, & 98 Golledge, 1998; Loomis et al., 1993; Philbeck et al., 2001; Sholl, 1989]. Importantly, the 99 donning of blindfolds and headphones throughout the task blocked out visual and auditory cues 100 that could facilitate the updating of positional estimates and obliged the participant to attend to 101 idiothetic cues from vestibular and proprioceptive systems (e.g., efferent motor commands, 102 kinesthetic feedback from the musculature, acceleratory signals from the vestibular system) for a 103 moment-to-moment updating of the perceived home or target location. 104 Fig. 2 In a trial of the conventional triangle completion task, the participant traverses an outbound path (shown by dark arrows) and then attempts to walk back to the starting position with visual and auditory cues occluded (the dotted line segment shows the ideal/perfect path of return). Apart from walking responses, pointing or heading responses toward the point of origin have also been applied. 105 106 In the first extensive study that applied the triangle completion task, Loomis et al. (1993) 107 showed that sighted participants who were blindfolded performed as well as their congenitally 108 and adventitiously blind counterparts when walking back to the starting position at the end of 109 outbound travel. No group showed particularly good performance and analyses of the distance
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