Learning to move in the real world

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Comparative research reveals extraordinary animal athleticism—mites lift >1000 times their body weight, mantis shrimp strike their prey with the force of a bullet, and peregrine falcons dive toward prey at 335 mph (539.13 km/hour) ([ 1 ][1]). Even human babies travel the distance of eight football fields per hour during free play ([ 2 ][2]). However, movement in the real world is not about being the strongest, fastest, or most active. Rather, effective action is a moment-to-moment process of matching the current status of the body to features of the environment ([ 3 ][3]). Locomotion—like other actions—must be tailored to local conditions. On page 697 of this issue, Hunt et al. ([ 4 ][4]) provide an elegant demonstration of the creativity of functional movement, showing that wild squirrels tune their leaps to branch bendiness and target distance, even inventing ingenious maneuvers when required.

Matching behavior to local conditions—that is, perceiving “affordances” for action—involves perception-action coupling ([ 5 ][5]). Animals must generate perceptual information about which actions are possible and then select appropriate actions from this set of possibilities ([ 2 ][2], [ 3 ][3]). The arboreal canopy is an ideal natural laboratory for studies of perception-action coupling because support diameters vary from tiny twigs to massive boughs, with more than three orders of magnitude of variation in branch compliance ([ 6 ][6]). Moreover, mistakes can have serious consequences—falling injuries account for most limb-bone fractures in free-ranging primates ([ 7 ][7]). Arboreal animals must avoid errors or quickly correct them.

Hunt et al. created an outdoor obstacle course and trained wild squirrels to jump from cantilevered perches to cross gaps of varying distances. Launch perches varied in compliance, requiring squirrels to negotiate a critical trade-off: Moving toward the end of the perch would shorten leaping distance but compromise stability and force production; staying closer to the base would ensure a secure launching platform but at the cost of increased gap distance. Squirrels launched closer to the base of the perch, which suggests that support compliance is a critical factor in arboreal locomotion ([ 8 ][8]). Notably, squirrels also demonstrated the creativity of functional movement. After learning the leaping task, squirrels encountered new adjustments to launch-perch compliance and gap distance, necessitating moment-to-moment modifications in behavior to ensure gap-crossing success. Squirrels innovated new strategies—parkour-like jumping maneuvers off the back wall of the apparatus when launching impulse was insufficient to cross the gap, and front and back flips to grasp the landing perch when their leaps over- or undershot the target.

Squirrels are not alone in the precision and creativity of their locomotion. Every animal must perceive and exploit affordances for locomotion under variable conditions ([ 3 ][3], [ 5 ][5]). Bats and iguanas alter locomotor forces to compensate for increased body mass associated with feeding and pregnancy ([ 9 ][9], [ 10 ][10]). Running guinea fowl adjust limb postures within a single step to maintain stability after an unexpected drop ([ 11 ][11]). Likewise, human infants gauge affordances with exquisite precision and invent new locomotor strategies on the fly (e.g., sliding down steep slopes or high drop-offs on their bottoms, backward feetfirst, or headfirst like Superman) ([ 2 ][2], [ 3 ][3]).

So how do animals learn to gauge and adjust their movements? Hunt et al. suggest that trial-and-error learning governs affordance perception in the course of a single session. However, adult squirrels have had a lifetime of learning, so development must be a critical factor. During development, new affordances emerge as animals’ bodies, skills, and effective environments change ([ 2 ][2]). Human infants can grow up to 2 cm in a single day ([ 12 ][12]). One week, babies are crawlers; the next, they are walkers ([ 13 ][13])—yesterday, objects on the coffee table were out of sight and beyond reach; today, they are accessible ([ 2 ][2]). Thus, learning occurs in the context of development, and the flux of body growth and motor-skill acquisition ensures that infants do not learn fixed solutions. Indeed, static solutions would be maladaptive in a continually changing ecosystem. Instead, infants “learn to learn.” They learn to detect information for affordances at each moment to determine which actions are possible with their current body and skills in a given environment. Learning amid development results in perception-action coupling that is sufficiently flexible to scale up to the novelty and variability of action in the real world ([ 2 ][2], [ 3 ][3]).

Human perceptual-motor development is an iterative process, where experience moving in a variable environment generates perception of new affordances that, in turn, facilitates new experiences ([ 2 ][2]). Human infants move to learn while they are learning to move. Likely, infant squirrels and other arboreal animals show similar calibration and creativity as they learn to navigate the canopy, particularly because misperceptions can prove fatal. Future work should consider the ontogeny of perception-action coupling in natural habitats.

Just as movement in the real world requires flexibility and creativity, researchers studying natural locomotion must be as ingenious as their animal subjects. The trick is to capture movement in all its complexity while retaining sufficient experimental control and measurement fidelity ([ 2 ][2]). The study of Hunt et al. is a beautiful example. Their unexpected results elucidate what every homeowner knows: Squirrels are clever acrobats when navigating complex environments.

1. [↵][14]1. D. J. Irschick,
2. T. E. Higham

, Animal Athletes: An Ecological and Evolutionary Approach (Oxford Univ. Press, 2016).

2. [↵][15]1. K. E. Adolph

, Hum. Development 63, 180 (2019).

[OpenUrl][16]

3. [↵][17]1. L. S. Liben,
2. U. Mueller

1. K. E. Adolph,
2. S. R. Robinson

, in Cognitive Processes, L. S. Liben, U. Mueller, Eds., vol. 2 of Handbook of Child Psychology and Developmental Science (Wiley, 2015).

4. [↵][18]1. N. H. Hunt,
2. J. Jinn,
3. L. F. Jacobs,
4. R. J. Full

, Science 373, 697 (2021).

[OpenUrl][19][Abstract/FREE Full Text][20]

5. [↵][21]1. J. J. Gibson

, The Ecological Approach to Visual Perception (Houghton Mifflin, 1979).

6. [↵][22]1. N. T. Dunham,
2. A. McNamara,
3. L. Shapiro,
4. T. Hieronymus,
5. J. W. Young

, Am. J. Phys. Anthropol. 167, 569 (2018).

[OpenUrl][23][CrossRef][24]

7. [↵][25]1. N. C. Lovell

, Am. J. Phys. Anthropol. 34, 117 (1991).

[OpenUrl][26]

8. [↵][27]1. J. W. Young,
2. B. M. Stricklen,
3. B. A. Chadwell

, J. Exp. Biol. 219, 2659 (2016).

[OpenUrl][28][Abstract/FREE Full Text][29]

9. [↵][30]1. J. Iriarte-Diaz,
2. D. K. Riskin,
3. K. S. Breuer,
4. S. M. Swartz

, PLOS ONE 7, e36665 (2012).

[OpenUrl][31][CrossRef][32][PubMed][33]

10. [↵][34]1. J. Scales,
2. M. Butler

, Integr. Comp. Biol. 47, 285 (2007).

[OpenUrl][35][CrossRef][36][PubMed][37]

11. [↵][38]1. M. A. Daley,
2. A. A. Biewener

, Proc. Natl. Acad. Sci. U.S.A. 103, 15681 (2006).

[OpenUrl][39][Abstract/FREE Full Text][40]

12. [↵][41]1. M. Lampl,
2. J. D. Veldhuis,
3. M. L. Johnson

, Science 258, 801 (1992).

[OpenUrl][42][Abstract/FREE Full Text][43]

13. [↵][44]1. K. E. Adolph,
2. S. R. Robinson,
3. J. W. Young,
4. F. Gill-Alvarez

, Psychol. Rev. 115, 527 (2008).

[OpenUrl][45][CrossRef][46][PubMed][47][Web of Science][48]

Acknowledgments: K.E.A. was supported by National Institute of Child Health and Human Development grant R01HD033486 and Defense Advanced Research Projects Agency grant N66001-19-2-4035. J.W.Y. was supported by National Science Foundation grant BCS-1921135.

[1]: #ref-1
[2]: #ref-2
[3]: #ref-3
[4]: #ref-4
[5]: #ref-5
[6]: #ref-6
[7]: #ref-7
[8]: #ref-8
[9]: #ref-9
[10]: #ref-10
[11]: #ref-11
[12]: #ref-12
[13]: #ref-13
[14]: #xref-ref-1-1 “View reference 1 in text”
[15]: #xref-ref-2-1 “View reference 2 in text”
[16]: {openurl}?query=rft.jtitle%253DHum.%2BDevelopment%26rft.volume%253D63%26rft.spage%253D180%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[17]: #xref-ref-3-1 “View reference 3 in text”
[18]: #xref-ref-4-1 “View reference 4 in text”
[19]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DHunt%26rft.auinit1%253DN.%2BH.%26rft.volume%253D373%26rft.issue%253D6555%26rft.spage%253D697%26rft.epage%253D700%26rft.atitle%253DAcrobatic%2Bsquirrels%2Blearn%2Bto%2Bleap%2Band%2Bland%2Bon%2Btree%2Bbranches%2Bwithout%2Bfalling%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.abe5753%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[20]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEyOiIzNzMvNjU1NS82OTciO3M6NDoiYXRvbSI7czoyMjoiL3NjaS8zNzMvNjU1NS82MjAuYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9
[21]: #xref-ref-5-1 “View reference 5 in text”
[22]: #xref-ref-6-1 “View reference 6 in text”
[23]: {openurl}?query=rft.jtitle%253DAm.%2BJ.%2BPhys.%2BAnthropol.%26rft.volume%253D167%26rft.spage%253D569%26rft_id%253Dinfo%253Adoi%252F10.1002%252Fajpa.23686%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[24]: /lookup/external-ref?access_num=10.1002/ajpa.23686&link_type=DOI
[25]: #xref-ref-7-1 “View reference 7 in text”
[26]: {openurl}?query=rft.jtitle%253DAm.%2BJ.%2BPhys.%2BAnthropol.%26rft.volume%253D34%26rft.spage%253D117%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[27]: #xref-ref-8-1 “View reference 8 in text”
[28]: {openurl}?query=rft.jtitle%253DJournal%2Bof%2BExperimental%2BBiology%26rft.stitle%253DJ.%2BExp.%2BBiol.%26rft.aulast%253DYoung%26rft.auinit1%253DJ.%2BW.%26rft.volume%253D219%26rft.issue%253D17%26rft.spage%253D2659%26rft.epage%253D2672%26rft.atitle%253DEffects%2Bof%2Bsupport%2Bdiameter%2Band%2Bcompliance%2Bon%2Bcommon%2Bmarmoset%2B%2528Callithrix%2Bjacchus%2529%2Bgait%2Bkinematics%26rft_id%253Dinfo%253Adoi%252F10.1242%252Fjeb.140939%26rft_id%253Dinfo%253Apmid%252F27582562%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
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[30]: #xref-ref-9-1 “View reference 9 in text”
[31]: {openurl}?query=rft.stitle%253DPLoS%2BONE%26rft.aulast%253DIriarte-Diaz%26rft.auinit1%253DJ.%26rft.volume%253D7%26rft.issue%253D5%26rft.spage%253De36665%26rft.epage%253De36665%26rft.atitle%253DKinematic%2Bplasticity%2Bduring%2Bflight%2Bin%2Bfruit%2Bbats%253A%2Bindividual%2Bvariability%2Bin%2Bresponse%2Bto%2Bloading.%26rft_id%253Dinfo%253Adoi%252F10.1371%252Fjournal.pone.0036665%26rft_id%253Dinfo%253Apmid%252F22615790%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[32]: /lookup/external-ref?access_num=10.1371/journal.pone.0036665&link_type=DOI
[33]: /lookup/external-ref?access_num=22615790&link_type=MED&atom=%2Fsci%2F373%2F6555%2F620.atom
[34]: #xref-ref-10-1 “View reference 10 in text”
[35]: {openurl}?query=rft.jtitle%253DIntegr.%2BComp.%2BBiol.%26rft_id%253Dinfo%253Adoi%252F10.1093%252Ficb%252Ficm054%26rft_id%253Dinfo%253Apmid%252F21672838%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[36]: /lookup/external-ref?access_num=10.1093/icb/icm054&link_type=DOI
[37]: /lookup/external-ref?access_num=21672838&link_type=MED&atom=%2Fsci%2F373%2F6555%2F620.atom
[38]: #xref-ref-11-1 “View reference 11 in text”
[39]: {openurl}?query=rft.jtitle%253DProc.%2BNatl.%2BAcad.%2BSci.%2BU.S.A.%26rft_id%253Dinfo%253Adoi%252F10.1073%252Fpnas.0601473103%26rft_id%253Dinfo%253Apmid%252F17032779%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[40]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6NDoicG5hcyI7czo1OiJyZXNpZCI7czoxMjoiMTAzLzQyLzE1NjgxIjtzOjQ6ImF0b20iO3M6MjI6Ii9zY2kvMzczLzY1NTUvNjIwLmF0b20iO31zOjg6ImZyYWdtZW50IjtzOjA6IiI7fQ==
[41]: #xref-ref-12-1 “View reference 12 in text”
[42]: {openurl}?query=rft.jtitle%253DScience%26rft.stitle%253DScience%26rft.aulast%253DLampl%26rft.auinit1%253DM%26rft.volume%253D258%26rft.issue%253D5083%26rft.spage%253D801%26rft.epage%253D803%26rft.atitle%253DSaltation%2Band%2Bstasis%253A%2Ba%2Bmodel%2Bof%2Bhuman%2Bgrowth%26rft_id%253Dinfo%253Adoi%252F10.1126%252Fscience.1439787%26rft_id%253Dinfo%253Apmid%252F1439787%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[43]: /lookup/ijlink/YTozOntzOjQ6InBhdGgiO3M6MTQ6Ii9sb29rdXAvaWpsaW5rIjtzOjU6InF1ZXJ5IjthOjQ6e3M6ODoibGlua1R5cGUiO3M6NDoiQUJTVCI7czoxMToiam91cm5hbENvZGUiO3M6Mzoic2NpIjtzOjU6InJlc2lkIjtzOjEyOiIyNTgvNTA4My84MDEiO3M6NDoiYXRvbSI7czoyMjoiL3NjaS8zNzMvNjU1NS82MjAuYXRvbSI7fXM6ODoiZnJhZ21lbnQiO3M6MDoiIjt9
[44]: #xref-ref-13-1 “View reference 13 in text”
[45]: {openurl}?query=rft.jtitle%253DPsychological%2Breview%26rft.stitle%253DPsychol%2BRev%26rft.aulast%253DAdolph%26rft.auinit1%253DK.%2BE.%26rft.volume%253D115%26rft.issue%253D3%26rft.spage%253D527%26rft.epage%253D543%26rft.atitle%253DWhat%2Bis%2Bthe%2Bshape%2Bof%2Bdevelopmental%2Bchange%253F%26rft_id%253Dinfo%253Adoi%252F10.1037%252F0033-295X.115.3.527%26rft_id%253Dinfo%253Apmid%252F18729590%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx
[46]: /lookup/external-ref?access_num=10.1037/0033-295X.115.3.527&link_type=DOI
[47]: /lookup/external-ref?access_num=18729590&link_type=MED&atom=%2Fsci%2F373%2F6555%2F620.atom
[48]: /lookup/external-ref?access_num=000258016400001&link_type=ISI

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