Water maze and radial maze learning and the density of binding sites of glutamate, GABA, and serotonin receptors in the hippocampus of inbred mouse strains

Abstract

Correlations between the densities of ionotropic glutamate, GABA(A), and serotonin binding sites in the hippocampus of seven inbred mouse strains and strain-specific learning capacities in two types of maze were studied. Binding site densities were measured with quantitative receptor autoradiography. Learning capacities were determined in a water maze task as well as in spatial and nonspatial versions of an eight-arm radial maze. The densities of most binding sites differed significantly between the strains in the subfields of Ammon's horn (CA1 and CA3) and the dentate gyrus, except for serotonin binding sites in CA1. By comparing the different strains, significant receptor-behavioral correlations between the densities of the GABA(A) receptors and the activity-dependent behavior in the water maze as well as the spatial learning in the radial maze were found. The densities of D,L-alpha-amino-3-hydroxy-5-methyl-4-isoxalone propionate (AMPA) and kainate receptors correlated positively with learning capacity in the spatial eight-arm radial maze. We conclude that hereditary variations mainly in AMPA, kainate, and GABA(A) receptor densities are involved in behavioral variations in spatial and nonspatial learning tasks.

New boundaries and dissociation of the mouse hippocampus along the dorsal‐ventral axis based on glutamatergic, GABAergic and catecholaminergic receptor densities

“…Thereby, the hippocampus is regarded as a brain structure with highly conserved functions, since this region is considered homologous among amniotes like mammals (Amrein & Slomianka, 2010; Bannerman et al, 2002; Hong Wei Dong, 2008; Fanselow & Dong, 2010; Lein et al, 2007; Lowe et al, 2015; Moser & Moser, 1998; Plachti et al, 2019; Swanson & Cowan, 1977; Thompson et al, 2008; Witter & Amaral, 2004; Zeineh et al, 2017; Zhao et al, 2001), birds (Atoji & Wild, 2006; Colombo & Broadbent, 2000; Herold et al, 2014; Herold et al, 2019; Herold, Coppola, & Bingman, 2015), reptiles and teleost fish (Rodriguez et al, 2002; Striedter, 2016; Tosches et al, 2018). Here, the multireceptor data indicated sharp boundaries between the different subregions of the mouse hippocampus DG, Hilus/CA4, CA3, CA2 and CA1 in line with earlier receptor binding studies and maps in rodents (Cremer, Lubke, Palomero‐Gallagher, & Zilles, 2011; Cremer et al, 2009; Cremer et al, 2015; Dean, Scarr, & McLeod, 2005; Palomero‐Gallagher et al, 2003; Topic et al, 2007; K. Zilles et al, 2000), rabbits (Tocco et al, 1991), primates including human (Camps, Kelly, & Palacios, 1990; Kraemer et al, 1995; Palomero‐Gallagher, Kedo, Mohlberg, Zilles, & Amunts, 2020) and birds (Herold et al, 2014; Herold et al, 2015). However, although functional differences between the subunits of the Ammon's horn were described and analyzed by further anatomical and physiological techniques, CA2 in mammals, and particularly in mice, often remained elusive, sometimes referred to as a separate region and sometimes merely as a mixture of CA1 and CA3 cells (Grove & Tole, 1999; Woodhams, Celio, Ulfig, & Witter, 1993).…”

New boundaries and dissociation of the mouse hippocampus along the dorsal‐ventral axis based on glutamatergic, GABAergic and catecholaminergic receptor densities

“…Thereby, the hippocampus is regarded as a brain structure with highly conserved functions, since this region is considered homologous among amniotes like mammals (Amrein & Slomianka, 2010; Bannerman et al, 2002; Hong Wei Dong, 2008; Fanselow & Dong, 2010; Lein et al, 2007; Lowe et al, 2015; Moser & Moser, 1998; Plachti et al, 2019; Swanson & Cowan, 1977; Thompson et al, 2008; Witter & Amaral, 2004; Zeineh et al, 2017; Zhao et al, 2001), birds (Atoji & Wild, 2006; Colombo & Broadbent, 2000; Herold et al, 2014; Herold et al, 2019; Herold, Coppola, & Bingman, 2015), reptiles and teleost fish (Rodriguez et al, 2002; Striedter, 2016; Tosches et al, 2018). Here, the multireceptor data indicated sharp boundaries between the different subregions of the mouse hippocampus DG, Hilus/CA4, CA3, CA2 and CA1 in line with earlier receptor binding studies and maps in rodents (Cremer, Lubke, Palomero‐Gallagher, & Zilles, 2011; Cremer et al, 2009; Cremer et al, 2015; Dean, Scarr, & McLeod, 2005; Palomero‐Gallagher et al, 2003; Topic et al, 2007; K. Zilles et al, 2000), rabbits (Tocco et al, 1991), primates including human (Camps, Kelly, & Palacios, 1990; Kraemer et al, 1995; Palomero‐Gallagher, Kedo, Mohlberg, Zilles, & Amunts, 2020) and birds (Herold et al, 2014; Herold et al, 2015). However, although functional differences between the subunits of the Ammon's horn were described and analyzed by further anatomical and physiological techniques, CA2 in mammals, and particularly in mice, often remained elusive, sometimes referred to as a separate region and sometimes merely as a mixture of CA1 and CA3 cells (Grove & Tole, 1999; Woodhams, Celio, Ulfig, & Witter, 1993).…”

Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice

“…In summary, the present data provide important information on the behavioral performance of inbred strains commonly used as genetic backgrounds in gene mutant mouse studies on three recently adapted tests for cognition. The data also extend previous literature on strain comparisons for other learning and memory tests (Wehner & Silva 1996;Crawley et al 1997), and molecular (Zilles et al 2000), electrophysiological (Bampton et al 1999;Nguyen et al 2000), and anatomical (Schwegler & Crusio 1995) correlates of cognition. On the olfactory-based social transmission of food preference test, 129S6, C57BL/6J and DBA/2J all performed well.…”

Impaired maze performance in aged rats is accompanied by increased density of NMDA, 5‐HT1A, and α‐adrenoceptor binding in hippocampus

“…Furthermore, it is possible that the absence of significant differences in AMPA and M 2 receptor binding might be related to the particular ligand and/or the dosage used for receptor labeling and that subtle behavior-related changes in binding density could be identified with a more detailed analysis that varies the kind of ligand and/or its concentration. This possibility, however, is not likely since the pharmacological specificity of the binding procedures used in the present study has repeatedly been shown (e.g., Zilles et al, 1991Zilles et al, , 2000Zilles et al, , 2002.…”

New boundaries and dissociation of the mouse hippocampus along the dorsal‐ventral axis based on glutamatergic, GABAergic and catecholaminergic receptor densities

“…Thereby, the hippocampus is regarded as a brain structure with highly conserved functions, since this region is considered homologous among amniotes like mammals (Amrein & Slomianka, 2010; Bannerman et al, 2002; Hong Wei Dong, 2008; Fanselow & Dong, 2010; Lein et al, 2007; Lowe et al, 2015; Moser & Moser, 1998; Plachti et al, 2019; Swanson & Cowan, 1977; Thompson et al, 2008; Witter & Amaral, 2004; Zeineh et al, 2017; Zhao et al, 2001), birds (Atoji & Wild, 2006; Colombo & Broadbent, 2000; Herold et al, 2014; Herold et al, 2019; Herold, Coppola, & Bingman, 2015), reptiles and teleost fish (Rodriguez et al, 2002; Striedter, 2016; Tosches et al, 2018). Here, the multireceptor data indicated sharp boundaries between the different subregions of the mouse hippocampus DG, Hilus/CA4, CA3, CA2 and CA1 in line with earlier receptor binding studies and maps in rodents (Cremer, Lubke, Palomero‐Gallagher, & Zilles, 2011; Cremer et al, 2009; Cremer et al, 2015; Dean, Scarr, & McLeod, 2005; Palomero‐Gallagher et al, 2003; Topic et al, 2007; K. Zilles et al, 2000), rabbits (Tocco et al, 1991), primates including human (Camps, Kelly, & Palacios, 1990; Kraemer et al, 1995; Palomero‐Gallagher, Kedo, Mohlberg, Zilles, & Amunts, 2020) and birds (Herold et al, 2014; Herold et al, 2015). However, although functional differences between the subunits of the Ammon's horn were described and analyzed by further anatomical and physiological techniques, CA2 in mammals, and particularly in mice, often remained elusive, sometimes referred to as a separate region and sometimes merely as a mixture of CA1 and CA3 cells (Grove & Tole, 1999; Woodhams, Celio, Ulfig, & Witter, 1993).…”

Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice

“…In summary, the present data provide important information on the behavioral performance of inbred strains commonly used as genetic backgrounds in gene mutant mouse studies on three recently adapted tests for cognition. The data also extend previous literature on strain comparisons for other learning and memory tests (Wehner & Silva 1996;Crawley et al 1997), and molecular (Zilles et al 2000), electrophysiological (Bampton et al 1999;Nguyen et al 2000), and anatomical (Schwegler & Crusio 1995) correlates of cognition. On the olfactory-based social transmission of food preference test, 129S6, C57BL/6J and DBA/2J all performed well.…”

Impaired maze performance in aged rats is accompanied by increased density of NMDA, 5‐HT1A, and α‐adrenoceptor binding in hippocampus

“…Furthermore, it is possible that the absence of significant differences in AMPA and M 2 receptor binding might be related to the particular ligand and/or the dosage used for receptor labeling and that subtle behavior-related changes in binding density could be identified with a more detailed analysis that varies the kind of ligand and/or its concentration. This possibility, however, is not likely since the pharmacological specificity of the binding procedures used in the present study has repeatedly been shown (e.g., Zilles et al, 1991Zilles et al, , 2000Zilles et al, , 2002.…”

New boundaries and dissociation of the mouse hippocampus along the dorsal‐ventral axis based on glutamatergic, GABAergic and catecholaminergic receptor densities

“…Thereby, the hippocampus is regarded as a brain structure with highly conserved functions, since this region is considered homologous among amniotes like mammals (Amrein & Slomianka, 2010; Bannerman et al, 2002; Hong Wei Dong, 2008; Fanselow & Dong, 2010; Lein et al, 2007; Lowe et al, 2015; Moser & Moser, 1998; Plachti et al, 2019; Swanson & Cowan, 1977; Thompson et al, 2008; Witter & Amaral, 2004; Zeineh et al, 2017; Zhao et al, 2001), birds (Atoji & Wild, 2006; Colombo & Broadbent, 2000; Herold et al, 2014; Herold et al, 2019; Herold, Coppola, & Bingman, 2015), reptiles and teleost fish (Rodriguez et al, 2002; Striedter, 2016; Tosches et al, 2018). Here, the multireceptor data indicated sharp boundaries between the different subregions of the mouse hippocampus DG, Hilus/CA4, CA3, CA2 and CA1 in line with earlier receptor binding studies and maps in rodents (Cremer, Lubke, Palomero‐Gallagher, & Zilles, 2011; Cremer et al, 2009; Cremer et al, 2015; Dean, Scarr, & McLeod, 2005; Palomero‐Gallagher et al, 2003; Topic et al, 2007; K. Zilles et al, 2000), rabbits (Tocco et al, 1991), primates including human (Camps, Kelly, & Palacios, 1990; Kraemer et al, 1995; Palomero‐Gallagher, Kedo, Mohlberg, Zilles, & Amunts, 2020) and birds (Herold et al, 2014; Herold et al, 2015). However, although functional differences between the subunits of the Ammon's horn were described and analyzed by further anatomical and physiological techniques, CA2 in mammals, and particularly in mice, often remained elusive, sometimes referred to as a separate region and sometimes merely as a mixture of CA1 and CA3 cells (Grove & Tole, 1999; Woodhams, Celio, Ulfig, & Witter, 1993).…”

Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice

“…In summary, the present data provide important information on the behavioral performance of inbred strains commonly used as genetic backgrounds in gene mutant mouse studies on three recently adapted tests for cognition. The data also extend previous literature on strain comparisons for other learning and memory tests (Wehner & Silva 1996;Crawley et al 1997), and molecular (Zilles et al 2000), electrophysiological (Bampton et al 1999;Nguyen et al 2000), and anatomical (Schwegler & Crusio 1995) correlates of cognition. On the olfactory-based social transmission of food preference test, 129S6, C57BL/6J and DBA/2J all performed well.…”

Impaired maze performance in aged rats is accompanied by increased density of NMDA, 5‐HT1A, and α‐adrenoceptor binding in hippocampus

“…Furthermore, it is possible that the absence of significant differences in AMPA and M 2 receptor binding might be related to the particular ligand and/or the dosage used for receptor labeling and that subtle behavior-related changes in binding density could be identified with a more detailed analysis that varies the kind of ligand and/or its concentration. This possibility, however, is not likely since the pharmacological specificity of the binding procedures used in the present study has repeatedly been shown (e.g., Zilles et al, 1991Zilles et al, , 2000Zilles et al, , 2002.…”