On the transfer of spatial learning between geometrically different shaped environments in the terrestrial toad, Rhinella arenarum

When trained in a rectangular arena, some research has suggested that rats are guided by local features rather than overall boundary geometry. We explored this hypothesis using the terrestrial toad, Rhinella arenarum, as a comparative contrast. In two experiments, toads were trained to find a water-reward goal location in either a featureless rectangular arena (Experiment 1) or in a rectangular arena with a removable colored feature panel covering one short wall (Experiment 2). After learning to successfully locate the water reward, probe trials were carried out by changing the shape of the arena into a kite form with two 90°-angled corners, and in the case of Experiment 2, also shifting the location of the color panel. The results of Experiment 1 indicated that the toads, in contrast to rats, relied primarily on overall shape or boundary geometry to encode the location of a goal. Under the probe conditions of the altered environmental geometry in Experiment 2, the toads seemed to preferentially choose a corner that was generally correct relative to the feature panel experienced during training. Together, the data of the current study suggest that toads and rats differ in the strategies they employ to represent spatial information available in a rectangular arena. Further, the results support the hypothesis that amphibians and mammals engage different neural mechanisms, perhaps related to different evolutionary selective pressures, for the representation of environmental geometry used for navigation.

[1]  M. Papini,et al.  Vulnerability of long-term memory to temporal delays in amphibians , 2013, Behavioural Processes.

[2]  Yuxiang Liu,et al.  Sex differences during place learning in the túngara frog , 2017, Animal Behaviour.

[3]  R. Soni The International Union for the Conservation of Nature and Natural Resources , 1960, Oryx.

[4]  Peter M. Jones,et al.  Potentiation, overshadowing, and blocking of spatial learning based on the shape of the environment. , 2006, Journal of experimental psychology. Animal behavior processes.

[5]  M Zanforlin,et al.  Geometric modules in animals' spatial representations: a test with chicks (Gallus gallus domesticus). , 1990, Journal of comparative psychology.

[6]  J. Tukey,et al.  Transformations Related to the Angular and the Square Root , 1950 .

[7]  Peter M. Jones,et al.  Transfer of spatial behavior between different environments: implications for theories of spatial learning and for the role of the hippocampus in spatial learning. , 2004, Journal of experimental psychology. Animal behavior processes.

[8]  Daniele Nardi,et al.  Pigeon (Columba livia) encoding of a goal location: the relative importance of shape geometry and slope information. , 2009, Journal of comparative psychology.

[9]  K. Summers,et al.  Learning to learn: advanced behavioural flexibility in a poison frog , 2016, Animal Behaviour.

[10]  J. Uher Comparative personality research: methodological approaches , 2008 .

[11]  V. D. Chamizo,et al.  Competition between landmarks in spatial learning: The role of proximity to the goal , 2006, Behavioural Processes.

[12]  V. Bingman,et al.  Telencephalic Neuronal Activation Associated with Spatial Memory in the Terrestrial Toad Rhinella arenarum: Participation of the Medial Pallium during Navigation by Geometry , 2016, Brain, Behavior and Evolution.

[13]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[14]  E. Wagenmakers,et al.  Why psychologists must change the way they analyze their data: the case of psi: comment on Bem (2011). , 2011, Journal of personality and social psychology.

[15]  María Inés Sotelo,et al.  Goal orientation by geometric and feature cues: spatial learning in the terrestrial toad Rhinella arenarum , 2014, Animal Cognition.

[16]  J. Pearce,et al.  Spatial Learning Based on Boundaries in Rats Is Hippocampus-Dependent and Prone to Overshadowing , 2010, Behavioral neuroscience.

[17]  D. Nardi,et al.  Local Geometric Properties Do Not Support Reorientation in Hippocampus-Engaged Homing Pigeons , 2019, Behavioral neuroscience.

[18]  Giorgio Vallortigara,et al.  View-based strategy for reorientation by geometry , 2010, Journal of Experimental Biology.

[19]  Nora S. Newcombe,et al.  1 Explaining the Development of Spatial Reorientation : Modularity-Plus-Language Versus the Emergence of Adaptive Combination , 2007 .

[20]  J. Rieser,et al.  Bayesian integration of spatial information. , 2007, Psychological bulletin.

[21]  R. Kesner Role of the hippocampus in mediating interference as measured by pattern separation processes , 2013, Behavioural Processes.

[22]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[23]  V. Bingman,et al.  Reflections on the Structural-Functional Evolution of the Hippocampus: What Is the Big Deal about a Dentate Gyrus , 2017, Brain, Behavior and Evolution.

[24]  Juan Pedro Vargas,et al.  Encoding of geometric and featural spatial information by goldfish (Carassius auratus). , 2004, Journal of comparative psychology.

[25]  G. Vallortigara,et al.  Complementary right and left hemifield use for predatory and agonistic behaviour in toads , 1998, Neuroreport.

[26]  L. Hedges,et al.  Categories and particulars: prototype effects in estimating spatial location. , 1991, Psychological review.

[27]  Alexandra D. Twyman,et al.  Young children's use of features to reorient is more than just associative: further evidence against a modular view of spatial processing. , 2010, Developmental science.

[28]  G. Vallortigara,et al.  Lateralisation of predator avoidance responses in three species of toads , 2002, Laterality.

[29]  Stella F. Lourenco,et al.  The potentiation of geometry by features in human children: Evidence against modularity in the domain of navigation. , 2015, Journal of experimental child psychology.

[30]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[31]  Numerical discrimination by frogs (Bombina orientalis) , 2014, Animal Cognition.

[32]  Ken Cheng,et al.  25 years of research on the use of geometry in spatial reorientation: a current theoretical perspective , 2013, Psychonomic Bulletin & Review.

[33]  Incentive or Habit Learning in Amphibians? , 2011, PloS one.

[34]  S. Gosling From mice to men: what can we learn about personality from animal research? , 2001, Psychological bulletin.

[35]  Mattias Johansson,et al.  Genetic Variability of the mTOR Pathway and Prostate Cancer Risk in the European Prospective Investigation on Cancer (EPIC) , 2011, PloS one.

[36]  Sasha R. X. Dall,et al.  The behavioural ecology of personality: consistent individual differences from an adaptive perspective , 2004 .

[37]  J Ward-Robinson,et al.  Influence of a beacon on spatial learning based on the shape of the test environment. , 2001, Journal of experimental psychology. Animal behavior processes.

[38]  Elizabeth S. Spelke,et al.  Sources of Flexibility in Human Cognition: Dual-Task Studies of Space and Language , 1999, Cognitive Psychology.

[39]  G. Vallortigara,et al.  Re-orienting in space: do animals use global or local geometry strategies? , 2010, Biology Letters.

[40]  Sang Ah Lee,et al.  Navigation as a source of geometric knowledge: Young children’s use of length, angle, distance, and direction in a reorientation task , 2012, Cognition.

[41]  Debbie M. Kelly,et al.  Reorienting in Virtual 3D Environments: Do Adult Humans Use Principal Axes, Medial Axes or Local Geometry? , 2013, PloS one.

[42]  Antoine Wystrach,et al.  Geometry, features, and panoramic views: ants in rectangular arenas. , 2011, Journal of experimental psychology. Animal behavior processes.

[43]  K. Cheng A purely geometric module in the rat's spatial representation , 1986, Cognition.

[44]  E. Spelke,et al.  Children's use of geometry and landmarks to reorient in an open space , 2001, Cognition.

[45]  Debbie M. Kelly,et al.  Pigeons' (Columba livia) encoding of geometric and featural properties of a spatial environment. , 1998 .

[46]  R. Ruibal The Adaptive Value of Bladder Water in the Toad, Bufo cognatus , 1962, Physiological Zoology.

[47]  E. T. Segura,et al.  Effect of schedule and magnitude of reinforcement on instrumental learning in the toad, Bufo arenarum , 1992 .

[48]  E. Spelke,et al.  Modularity and development: the case of spatial reorientation , 1996, Cognition.

[49]  Daniele Nardi,et al.  Slope-driven goal location behavior in pigeons. , 2010, Journal of experimental psychology. Animal behavior processes.

[50]  G. Vallortigara,et al.  Right-pawedness in toads , 1996, Nature.

[51]  V. Bingman,et al.  Slope-Based and Geometric Encoding of a Goal Location by the Terrestrial Toad (Rhinella arenarum) , 2017, Journal of comparative psychology.

[52]  Division on Earth Guide for the Care and Use of Laboratory Animals , 1996 .

[53]  Caroline Murphy,et al.  Use of geometry for spatial reorientation in children applies only to symmetric spaces. , 2010, Developmental science.

[54]  C. Gallistel The organization of learning , 1990 .

[55]  Kent D. Bodily,et al.  Orientation in trapezoid-shaped enclosures: implications for theoretical accounts of geometry learning. , 2011, Journal of experimental psychology. Animal behavior processes.

[56]  Nelson B. Watts,et al.  When, Where and How Osteoporosis-Associated Fractures Occur: An Analysis from the Global Longitudinal Study of Osteoporosis in Women (GLOW) , 2013, PloS one.

[57]  Simon Benhamou,et al.  LANDMARK USE BY NAVIGATING RATS (RATTUS NORVEGICUS) : CONTRASTING GEOMETRIC AND FEATURAL INFORMATION , 1998 .

[58]  Giorgio Vallortigara,et al.  Reorienting strategies in a rectangular array of landmarks by domestic chicks (Gallus gallus). , 2010, Journal of comparative psychology.

[59]  Laurie L Bloomfield,et al.  Spatial encoding in mountain chickadees: features overshadow geometry , 2005, Biology Letters.

[60]  M. F. Daneri,et al.  Control of spatial orientation in terrestrial toads (Rhinella arenarum). , 2011, Journal of comparative psychology.

[61]  Spencer J. Price,et al.  Testing Principal- Versus Medial-Axis Accounts of Global Spatial Reorientation , 2018, Journal of experimental psychology. Animal learning and cognition.

[62]  Marcia L. Spetch,et al.  Comparing black-capped (Poecile atricapillus) and mountain chickadees (Poecile gambeli): use of geometric and featural information in a spatial orientation task , 2009, Animal Cognition.

[63]  Antoine Wystrach,et al.  Ants Learn Geometry and Features , 2009, Current Biology.

[64]  C R Gallistel,et al.  Shape parameters explain data from spatial transformations: comment on Pearce et al. (2004) and Tommasi & Polli (2004). , 2005, Journal of experimental psychology. Animal behavior processes.

[65]  W. Gerstner,et al.  Is there a geometric module for spatial orientation? Insights from a rodent navigation model. , 2009, Psychological review.

[66]  Almut Hupbach,et al.  Reorientation in a rhombic environment: No evidence for an encapsulated geometric module , 2005 .

[67]  Elizabeth S. Spelke,et al.  A geometric process for spatial reorientation in young children , 1994, Nature.

[68]  Enclosure size and the use of local and global geometric cues for reorientation , 2012, Psychonomic bulletin & review.

[69]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[70]  M A Good,et al.  Hippocampal lesions disrupt navigation based on the shape of the environment. , 2004, Behavioral neuroscience.

[71]  Antoine Wystrach,et al.  Ants in rectangular arenas , 2009, Communicative & integrative biology.