Separate Geometric and Non-Geometric Modules for Spatial Reorientation: Evidence from a Lopsided Animal Brain

Research has proved that disoriented children and nonhuman animals can reorient themselves using geometric and nongeometric features of the environment, showing conjoined use of both types of information to different degree depending on species and developmental level. Little is known of the neurobiological bases of these spatial reorientation processes. Here we take advantage of the neuroanatomical peculiarities of the visual system of birds (showing segregation of information between the two sides of the brain to a considerable degree) to investigate the way in which geometric and nongeometric information is encoded and used by the left and right hemispheres. Domestic chicks were trained binocularly in an environment with a distinctive geometry (a rectangular cage) with panels at the corners providing nongeometric cues. Between trials, chicks were passively disoriented to disable dead reckoning. When tested after removal of the panels, lefteyed chicks, but not right-eyed chicks, reoriented using the residual information provided by the geometry of the cage. When tested after removal of geometric information (i.e., in a square-shaped cage), both rightand left-eyed chicks reoriented using the residual nongeometric information provided by the panels. When trained binocularly with only geometric information, at test, left-eyed chicks reoriented better than right-eyed chicks. Finally, when geometric and nongeometric cues provided contradictory information, left-eyed chicks showed more reliance on geometric cues, whereas right-eyed chicks showed more reliance on nongeometric cues. The results suggest separate mechanisms for dealing with spatial reorientation problems, with the right hemisphere taking charge of large-scale geometry of the environment and with both hemispheres taking charge of local, nongeometric cues when available in isolation, but with a predominance of the left hemisphere when competition between geometric and nongeometric information occurs.

[1]  L. Pizzamiglio,et al.  TENS modulates spatial reorientantion in neglect patients , 2000, Neuroreport.

[2]  L. Regolin,et al.  Effects of light stimulation of embryos on the use of position-specific and object-specific cues in binocular and monocular domestic chicks (Gallus gallus) , 2005, Behavioural Brain Research.

[3]  G. Vallortigara Comparative Neuropsychology of the Dual Brain: A Stroll through Animals' Left and Right Perceptual Worlds , 2000, Brain and Language.

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

[5]  Lynn Nadel,et al.  Children's Use of Landmarks: Implications for Modularity Theory , 2002, Psychological science.

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

[7]  Valeria Anna Sovrano,et al.  Reorientation by geometric and landmark information in environments of different size. , 2005, Developmental science.

[8]  O. Güntürkün,et al.  Parallel working memory for spatial location and food-related object cues in foraging pigeons: binocular and lateralized monocular performance. , 2001, Learning & memory.

[9]  Luigi Pizzamiglio,et al.  Evidence for Separate Allocentric and Egocentric Space Processing in Neglect Patients , 1998, Cortex.

[10]  N. Newcombe,et al.  Is there a geometric module for spatial orientation? squaring theory and evidence , 2005, Psychonomic bulletin & review.

[11]  Richard S. J. Frackowiak,et al.  Recalling Routes around London: Activation of the Right Hippocampus in Taxi Drivers , 1997, The Journal of Neuroscience.

[12]  Valeria Anna Sovrano,et al.  Animals' use of landmarks and metric information to reorient: effects of the size of the experimental space , 2005, Cognition.

[13]  G. Vallortigara,et al.  Possible evolutionary origins of cognitive brain lateralization , 1999, Brain Research Reviews.

[14]  L. Hermer-Vazquez,et al.  Language, space, and the development of cognitive flexibility in humans: the case of two spatial memory tasks , 2001, Cognition.

[15]  L. Rogers,et al.  Organisation of the tectorotundal and SP/IPS‐rotundal projections in the chick , 1998 .

[16]  L. Rogers Comparative Vertebrate Lateralization: Preface , 2002 .

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

[18]  Giorgio Vallortigara,et al.  Hemispheric processing of landmark and geometric information in male and female domestic chicks (Gallus gallus) , 2004, Behavioural Brain Research.

[19]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[20]  Lesley J. Rogers,et al.  Development of Brain and Behaviour in the Chicken , 1995 .

[21]  P. Carruthers The cognitive functions of language , 2002, Behavioral and Brain Sciences.

[22]  J. Huttenlocher,et al.  Toddlers' use of metric information and landmarks to reorient. , 2001, Journal of experimental child psychology.

[23]  L. Rogers,et al.  Experience-induced modulation of the use of spatial information in the domestic chick , 2005, Animal Behaviour.

[24]  D. Nardi,et al.  A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass‐based spatial learning , 2005, The European journal of neuroscience.

[25]  G. Vallortigara,et al.  Lateralization of response by chicks to change in a model partner , 1991, Animal Behaviour.

[26]  Valeria Anna Sovrano,et al.  Modularity as a fish (Xenotoca eiseni) views it: conjoining geometric and nongeometric information for spatial reorientation. , 2003, Journal of experimental psychology. Animal behavior processes.

[27]  Stephen W. Wilson,et al.  fsi Zebrafish Show Concordant Reversal of Laterality of Viscera, Neuroanatomy, and a Subset of Behavioral Responses , 2005, Current Biology.

[28]  J. Fodor,et al.  The Modularity of Mind: An Essay on Faculty Psychology , 1984 .

[29]  Valeria Anna Sovrano,et al.  Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish , 2002, Cognition.

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

[31]  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.

[32]  Naoya Aoki,et al.  The Mind Through Chick Eyes : Memory, Cognition and Anticipation , 2003, Zoological science.

[33]  Marc D. Hauser,et al.  The role of landmarks in cotton-top tamarin spatial foraging: evidence for geometric and non-geometric features , 2001, Animal Cognition.

[34]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[35]  L. Regolin,et al.  Working memory in the chick: parallel and lateralized mechanisms for encoding of object- and position-specific information , 2005, Behavioural Brain Research.

[36]  Ken Cheng,et al.  Goldfish (Carassius auratus) matching geometric and featural cues: a reinterpretation of some of the data of Vargas, López, Salas, and Thinus-Blanc (2004). , 2005, Journal of comparative psychology.

[37]  L. Nadel,et al.  Behavioural brain research in naturalistic and semi-naturalistic settings , 1995 .

[38]  O. Güntürkün Avian visual lateralization: a review. , 1997, Neuroreport.

[39]  G. Vallortigara,et al.  Searching for the center: spatial cognition in the domestic chick (Gallus gallus). , 2000, Journal of experimental psychology. Animal behavior processes.

[40]  Giorgio Vallortigara,et al.  Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus , 2003, The European journal of neuroscience.

[41]  Giorgio Vallortigara,et al.  Right hemisphere advantage for social recognition in the chick , 1992, Neuropsychologia.

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

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

[44]  G. Vallortigara,et al.  Encoding of geometric and landmark information in the left and right hemispheres of the Avian Brain. , 2001, Behavioral neuroscience.

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

[46]  J. Krebs,et al.  Memory for spatial and object-specific cues in food-storing and non-storing birds , 1994, Journal of Comparative Physiology A.

[47]  L. Rogers,et al.  Bilaterally projecting neurons in the two visual pathways of chicks , 1998, Brain Research.

[48]  Naoya Aoki,et al.  Neural correlates of the proximity and quantity of anticipated food rewards in the ventral striatum of domestic chicks , 2005, The European journal of neuroscience.

[49]  R. Andrew The nature of behavioural lateralization in the chick , 1991 .

[50]  Lynn Nadel,et al.  The Psychobiology of Spatial Behavior: The Hippocampal Formation and Spatial Mapping , 1995 .

[51]  Lesley J. Rogers,et al.  Development of lateralization , 1991 .

[52]  G. Vallortigara,et al.  Functional asymmetry of left and right avian piriform cortex in homing pigeons' navigation , 2005, The European journal of neuroscience.

[53]  C Thinus-Blanc,et al.  Rhesus monkeys use geometric and nongeometric information during a reorientation task. , 2001, Journal of experimental psychology. General.

[54]  L. Rogers,et al.  Behavioral, Structural and Neurochemical Asymmetries in the Avian Brain: A Model System for Studying Visual Development and Processing , 1996, Neuroscience & Biobehavioral Reviews.

[55]  Marcia L. Spetch,et al.  Pigeons encode relative geometry. , 2001, Journal of experimental psychology. Animal behavior processes.

[56]  Valeria Anna Sovrano,et al.  Conjoining information from different modules: A comparative perspective , 2002 .

[57]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[58]  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.

[59]  M. Dadda,et al.  Lateralized fish perform better than nonlateralized fish in spatial reorientation tasks , 2005, Behavioural Brain Research.

[60]  E. Spelke,et al.  Human Spatial Representation: Insights from Animals , 2002 .

[61]  T G Bever,et al.  Peripheral and cerebral asymmetries in the rat. , 1997, Science.