Mouse Cognition-Related Behavior in the Open-Field: Emergence of Places of Attraction

Spatial memory is often studied in the Morris Water Maze, where the animal's spatial orientation has been shown to be mainly shaped by distal visual cues. Cognition-related behavior has also been described along “well-trodden paths”—spatial habits established by animals in the wild and in captivity reflecting a form of spatial memory. In the present study we combine the study of Open Field behavior with the study of behavior on well-trodden paths, revealing a form of locational memory that appears to correlate with spatial memory. The tracked path of the mouse is used to examine the dynamics of visiting behavior to locations. A visit is defined as either progressing through a location or stopping there, where progressing and stopping are computationally defined. We then estimate the probability of stopping at a location as a function of the number of previous visits to that location, i.e., we measure the effect of visiting history to a location on stopping in it. This can be regarded as an estimate of the familiarity of the mouse with locations. The recently wild-derived inbred strain CZECHII shows the highest effect of visiting history on stopping, C57 inbred mice show a lower effect, and DBA mice show no effect. We employ a rarely used, bottom-to-top computational approach, starting from simple kinematics of movement and gradually building our way up until we end with (emergent) locational memory. The effect of visiting history to a location on stopping in it can be regarded as an estimate of the familiarity of the mouse with locations, implying memory of these locations. We show that the magnitude of this estimate is strain-specific, implying a genetic influence. The dynamics of this process reveal that locations along the mouse's trodden path gradually become places of attraction, where the mouse stops habitually.

[1]  Richard Paylor,et al.  Behavioral dissociations between C57BL/6 and DBA/2 mice on learning and memory tasks: A hippocampal-dysfunction hypothesis , 1993, Psychobiology.

[2]  G Whitney,et al.  Specific anosmia in the laboratory mouse , 1977, Behavior genetics.

[3]  J. Wehner,et al.  Differences between inbred strains of mice in Morris water maze performance , 1988, Behavior genetics.

[4]  Ofer Tchernichovski,et al.  Constraints and the Emergence of 'Free' Exploratory Behavior in Rat Ontogeny , 1996 .

[5]  Lee M. Silver,et al.  Mouse Genetics: Concepts and Applications , 1995 .

[6]  Yoav Benjamini,et al.  Statistical discrimination of natural modes of motion in rat exploratory behavior , 2000, Journal of Neuroscience Methods.

[7]  M. Ammassari-Teule,et al.  What do comparative studies of inbred mice add to current investigations on the neural basis of spatial behaviors? , 1998, Experimental Brain Research.

[8]  Y. Benjamini,et al.  Estimating wall guidance and attraction in mouse free locomotor behavior , 2007, Genes, brain, and behavior.

[9]  T. Garland,et al.  Selection experiments: an under-utilized tool in biomechanics and organismal biology , 2002 .

[10]  Anat Sakov,et al.  New replicable anxiety-related measures of wall vs center behavior of mice in the open field. , 2004, Journal of applied physiology.

[11]  A. J Spink,et al.  The EthoVision video tracking system—A tool for behavioral phenotyping of transgenic mice , 2001, Physiology & Behavior.

[12]  S M Mihalick,et al.  Strain and sex differences on olfactory discrimination learning in C57BL/6J and DBA/2J inbred mice (Mus musculus). , 2000, Journal of comparative psychology.

[13]  J. Wehner,et al.  Hippocampal protein kinase C activity is reduced in poor spatial learners , 1990, Brain Research.

[14]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

[15]  Steven N. Austad,et al.  A mouse's tale , 2002 .

[16]  Etienne Save,et al.  The differences shown by C57BL/6 and DBA/2 inbred mice in detecting spatial novelty are subserved by a different hippocampal and parietal cortex interplay , 1996, Behavioural Brain Research.

[17]  Michael H. Kutner Applied Linear Statistical Models , 1974 .

[18]  Mark Von Tress,et al.  Generalized, Linear, and Mixed Models , 2003, Technometrics.

[19]  D. Eilam,et al.  Home base behavior of rats (Rattus norvegicus) exploring a novel environment , 1989, Behavioural Brain Research.

[20]  Ofer Tchernichovski,et al.  A phase plane representation of rat exploratory behavior , 1995, Journal of Neuroscience Methods.

[21]  F. Bonhomme,et al.  Wild mice: an ever-increasing contribution to a popular mammalian model. , 2003, Trends in genetics : TIG.

[22]  E. Thelen,et al.  The dynamics of embodiment: A field theory of infant perseverative reaching , 2001, Behavioral and Brain Sciences.

[23]  Clelia Rossi-Arnaud,et al.  Spatial learning in two inbred strains of mice: genotype-dependent effect of amygdaloid and hippocampal lesions , 1991, Behavioural Brain Research.

[24]  Douglas G Wallace,et al.  Quantification of a single exploratory trip reveals hippocampal formation mediated dead reckoning , 2002, Journal of Neuroscience Methods.

[25]  M A Geyer,et al.  Prepulse Inhibition Deficits and Perseverative Motor Patterns in Dopamine Transporter Knock-Out Mice: Differential Effects of D1 and D2 Receptor Antagonists , 2001, The Journal of Neuroscience.

[26]  Anat Sakov,et al.  The dynamics of spatial behavior: how can robust smoothing techniques help? , 2004, Journal of Neuroscience Methods.

[27]  S. Cooper,et al.  Ethology and psychopharmacology , 1994 .

[28]  Y. Benjamini,et al.  Wild mouse open field behavior is embedded within the multidimensional data space spanned by laboratory inbred strains , 2006, Genes, brain, and behavior.

[29]  J. Lassalle,et al.  Genetic variation, hippocampal mossy fibres distribution, novelty reactions and spatial representation in mice , 1990, Behavioural Brain Research.

[30]  J. Crabbe,et al.  A rating scale for wildness and ease of handling laboratory mice: results for 21 inbred strains tested in two laboratories , 2003, Genes, brain, and behavior.

[31]  Yoav Benjamini,et al.  SEE locomotor behavior test discriminates C57BL/6J and DBA/2J mouse inbred strains across laboratories and protocol conditions. , 2003, Behavioral neuroscience.

[32]  Anat Sakov,et al.  Genotype-environment interactions in mouse behavior: a way out of the problem. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[33]  David Eilam,et al.  Stopping behavior: constraints on exploration in rats (Rattus norvegicus) , 1993, Behavioural Brain Research.

[34]  Florian Holsboer,et al.  Impact of high and low anxiety on cognitive performance in a modified hole board test in C57BL/6 and DBA/2 mice , 2003, The European journal of neuroscience.

[35]  I. Whishaw,et al.  Dead reckoning (path integration) requires the hippocampal formation: evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests , 2001, Behavioural Brain Research.

[36]  D. Eilam,et al.  Quinpirole induces compulsive checking behavior in rats: a potential animal model of obsessive-compulsive disorder (OCD). , 1998, Behavioral neuroscience.

[37]  Antonio Caprioli,et al.  Spatial learning and memory, maze running strategies and cholinergic mechanisms in two inbred strains of mice , 1985, Behavioural Brain Research.

[38]  Patrick V. Russo,et al.  Multivariate assessment of locomotor behavior: Pharmacological and behavioral analyses , 1986, Pharmacology Biochemistry and Behavior.

[39]  J. B. Uexküll,et al.  Streifzüge durch die Umwelten von Tieren und Menschen : ein Bilderbuch unsichtbarer Welten , 1934 .

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

[41]  Neri Kafkafi,et al.  Natural segmentation of the locomotor behavior of drug-induced rats in a photobeam cage , 2001, Journal of Neuroscience Methods.

[42]  Douglas Wahlsten,et al.  Different rankings of inbred mouse strains on the Morris maze and a refined 4-arm water escape task , 2005, Behavioural Brain Research.

[43]  Yoav Benjamini,et al.  Rats and mice share common ethologically relevant parameters of exploratory behavior , 2001, Behavioural Brain Research.

[44]  R. Morris Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

[45]  Karin Schweizer,et al.  Spatial Cognition: The Role of Landmark, Route, and Survey Knowledge in Human and Robot Navigation , 1997, GI Jahrestagung.

[46]  David S. Olton,et al.  The radial arm maze as a tool in behavioral pharmacology , 1987, Physiology & Behavior.

[47]  Ofer Tchernichovski,et al.  The dynamics of long term exploration in the rat , 1998, Biological Cybernetics.

[48]  Janan T. Eppig,et al.  A mouse phenome project , 2000, Mammalian Genome.

[49]  Neri Kafkafi,et al.  Darting behavior: a quantitative movement pattern designed for discrimination and replicability in mouse locomotor behavior , 2003, Behavioural Brain Research.