The amygdala modulates neuronal activation in the hippocampus in response to spatial novelty
Emerging evidence indicates that the amygdala and the hippocampus play an important role in the pathophysiology of major psychotic disorders. Consistent with this evidence, and with data indicating amygdala modulation of hippocampal activity, animal model investigations have shown that a disruption...
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| Published in | Hippocampus Vol. 18; no. 2; pp. 169 - 181 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken
Wiley Subscription Services, Inc., A Wiley Company
01.01.2008
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| Online Access | Get full text |
| ISSN | 1050-9631 1098-1063 1098-1063 |
| DOI | 10.1002/hipo.20380 |
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| Abstract | Emerging evidence indicates that the amygdala and the hippocampus play an important role in the pathophysiology of major psychotic disorders. Consistent with this evidence, and with data indicating amygdala modulation of hippocampal activity, animal model investigations have shown that a disruption of amygdala activity induces neurochemical changes in the hippocampus that are similar to those detected in subjects with schizophrenia. With the present study, we used induction of the immediate early gene Fos, to test the hypothesis that the amygdala may affect neuronal activation of the hippocampus in response to different spatial environments (familiar, modified, and novel). Exploratory and anxiety related behaviors were also assessed. In vehicle‐treated rats, exposure to a modified version of the familiar environment was associated with an increase of numerical densities of Fos‐immunoreactive nuclei in sectors CA1 and CA2, while exposure to a completely novel environment was associated with an increase in sectors CA1, CA4, and DG, compared with the familiar environment. Pharmacological disruption of amygdala activity resulted in a failure to increase Fos induction in the hippocampus in response to these environments. Exploratory behavior in response to the different environments was not altered by manipulation of amygdala activity. These findings support the idea that the amygdala modulates spatial information processing in the hippocampus and may affect encoding of specific environmental features, while complex behavioral responses to environment may be the result of broader neural circuits. These findings also raise the possibility that amygdala abnormalities may contribute to impairments in cognitive information processing in subjects with major psychoses. © 2007 Wiley‐Liss, Inc. |
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| AbstractList | Emerging evidence indicates that the amygdala and the hippocampus play an important role in the pathophysiology of major psychotic disorders. Consistent with this evidence, and with data indicating amygdala modulation of hippocampal activity, animal model investigations have shown that a disruption of amygdala activity induces neurochemical changes in the hippocampus that are similar to those detected in subjects with schizophrenia. With the present study, we used induction of the immediate early gene Fos, to test the hypothesis that the amygdala may affect neuronal activation of the hippocampus in response to different spatial environments (familiar, modified, and novel). Exploratory and anxiety related behaviors were also assessed. In vehicle‐treated rats, exposure to a modified version of the familiar environment was associated with an increase of numerical densities of Fos‐immunoreactive nuclei in sectors CA1 and CA2, while exposure to a completely novel environment was associated with an increase in sectors CA1, CA4, and DG, compared with the familiar environment. Pharmacological disruption of amygdala activity resulted in a failure to increase Fos induction in the hippocampus in response to these environments. Exploratory behavior in response to the different environments was not altered by manipulation of amygdala activity. These findings support the idea that the amygdala modulates spatial information processing in the hippocampus and may affect encoding of specific environmental features, while complex behavioral responses to environment may be the result of broader neural circuits. These findings also raise the possibility that amygdala abnormalities may contribute to impairments in cognitive information processing in subjects with major psychoses. © 2007 Wiley‐Liss, Inc. Emerging evidence indicates that the amygdala and the hippocampus play an important role in the pathophysiology of major psychotic disorders. Consistent with this evidence, and with data indicating amygdala modulation of hippocampal activity, animal model investigations have shown that a disruption of amygdala activity induces neurochemical changes in the hippocampus that are similar to those detected in subjects with schizophrenia. With the present study, we used induction of the immediate early gene Fos, to test the hypothesis that the amygdala may affect neuronal activation of the hippocampus in response to different spatial environments (familiar, modified, and novel). Exploratory and anxiety related behaviors were also assessed. In vehicle-treated rats, exposure to a modified version of the familiar environment was associated with an increase of numerical densities of Fos-immunoreactive nuclei in sectors CA1 and CA2, while exposure to a completely novel environment was associated with an increase in sectors CA1, CA4, and DG, compared with the familiar environment. Pharmacological disruption of amygdala activity resulted in a failure to increase Fos induction in the hippocampus in response to these environments. Exploratory behavior in response to the different environments was not altered by manipulation of amygdala activity. These findings support the idea that the amygdala modulates spatial information processing in the hippocampus and may affect encoding of specific environmental features, while complex behavioral responses to environment may be the result of broader neural circuits. These findings also raise the possibility that amygdala abnormalities may contribute to impairments in cognitive information processing in subjects with major psychoses.Emerging evidence indicates that the amygdala and the hippocampus play an important role in the pathophysiology of major psychotic disorders. Consistent with this evidence, and with data indicating amygdala modulation of hippocampal activity, animal model investigations have shown that a disruption of amygdala activity induces neurochemical changes in the hippocampus that are similar to those detected in subjects with schizophrenia. With the present study, we used induction of the immediate early gene Fos, to test the hypothesis that the amygdala may affect neuronal activation of the hippocampus in response to different spatial environments (familiar, modified, and novel). Exploratory and anxiety related behaviors were also assessed. In vehicle-treated rats, exposure to a modified version of the familiar environment was associated with an increase of numerical densities of Fos-immunoreactive nuclei in sectors CA1 and CA2, while exposure to a completely novel environment was associated with an increase in sectors CA1, CA4, and DG, compared with the familiar environment. Pharmacological disruption of amygdala activity resulted in a failure to increase Fos induction in the hippocampus in response to these environments. Exploratory behavior in response to the different environments was not altered by manipulation of amygdala activity. These findings support the idea that the amygdala modulates spatial information processing in the hippocampus and may affect encoding of specific environmental features, while complex behavioral responses to environment may be the result of broader neural circuits. These findings also raise the possibility that amygdala abnormalities may contribute to impairments in cognitive information processing in subjects with major psychoses. Emerging evidence indicates that the amygdala and the hippocampus play an important role in the pathophysiology of major psychotic disorders. Consistent with this evidence, and with data indicating amygdala modulation of hippocampal activity, animal model investigations have shown that a disruption of amygdala activity induces neurochemical changes in the hippocampus that are similar to those detected in subjects with schizophrenia. With the present study, we used induction of the immediate early gene Fos, to test the hypothesis that the amygdala may affect neuronal activation of the hippocampus in response to different spatial environments (familiar, modified, and novel). Exploratory and anxiety related behaviors were also assessed. In vehicle-treated rats, exposure to a modified version of the familiar environment was associated with an increase of numerical densities of Fos-immunoreactive nuclei in sectors CA1 and CA2, while exposure to a completely novel environment was associated with an increase in sectors CA1, CA4, and DG, compared with the familiar environment. Pharmacological disruption of amygdala activity resulted in a failure to increase Fos induction in the hippocampus in response to these environments. Exploratory behavior in response to the different environments was not altered by manipulation of amygdala activity. These findings support the idea that the amygdala modulates spatial information processing in the hippocampus and may affect encoding of specific environmental features, while complex behavioral responses to environment may be the result of broader neural circuits. These findings also raise the possibility that amygdala abnormalities may contribute to impairments in cognitive information processing in subjects with major psychoses. |
| Author | Eichenbaum, Howard Lange, Nicholas Sheth, Archana Berretta, Sabina |
| Author_xml | – sequence: 1 givenname: Archana surname: Sheth fullname: Sheth, Archana organization: Department of Psychology, Boston University, Boston, Massachusetts – sequence: 2 givenname: Sabina surname: Berretta fullname: Berretta, Sabina organization: Laboratory for Translational Neuroscience, McLean Hospital, Belmont, Massachusetts – sequence: 3 givenname: Nicholas surname: Lange fullname: Lange, Nicholas organization: Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts – sequence: 4 givenname: Howard surname: Eichenbaum fullname: Eichenbaum, Howard email: hbe@bu.edu organization: Department of Psychology, Boston University, Boston, Massachusetts |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/17960646$$D View this record in MEDLINE/PubMed |
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Why there are complementary learning systems in the hippocampus and neocortex 2002; 16 2006; 31 1991; 14 1994; 654 2002; 12 2004; 7 2004; 161 2004; 24 1996; 71 1997; 3 1994; 61 1997b; 77 1997; 9 2003; 53 1978 1997; 8 1992; 8 1989; 107 1987; 237 2005; 102 2004; 174 2006; 26 1991; 84 1999; 55 1992; 49 2005; 77 1983; 305 1989; 61 2000; 911 2002; 134 2005; 119 1992 2001; 24 1996; 16 2001; 25 2001; 21 2004; 55 2001; 431 1973; 21 1990; 27 1995; 47 1971; 34 1996; 199 1998; 1 1994; 17 2005; 15 2005; 12 2003; 23 1997; 755 2004; 124 1990; 302 2002; 52 2000; 5 2002; 57 2005; 139 2002; 55 2005; 21 2002; 116 1999; 122 1988; 31 1999; 403 1998; 43 1998; 44 1996; 107 2006; 60 1997; 229 1999; 19 1991; 44 1997; 12 2002; 109 2001; 11 1996; 25 2001; 14 1980; 189 1998; 55 2005; 35 1996; 22 1991; 1 1987; 97 1995; 15 2000; 23 2000; 20 1996; 50 2006 1993; 261 1995; 356 2005; 1051 1988; 240 1985; 42 1998; 172 1989; 29 1987; 24 1993; 14 2006; 82 1987; 22 1993; 13 2002; 26 1983; 288 2004; 14 2000; 31 1997; 78 2002; 22 1997a; 76 1995; 102 1989; 290 1999; 71 2004; 118 1998; 34 2001; 356 1994; 4 e_1_2_1_119_1 e_1_2_1_111_1 e_1_2_1_81_1 e_1_2_1_115_1 e_1_2_1_20_1 e_1_2_1_66_1 e_1_2_1_89_1 e_1_2_1_24_1 e_1_2_1_62_1 e_1_2_1_43_1 e_1_2_1_85_1 e_1_2_1_28_1 e_1_2_1_47_1 Pare D (e_1_2_1_84_1) 1995; 15 e_1_2_1_92_1 e_1_2_1_103_1 e_1_2_1_122_1 e_1_2_1_107_1 e_1_2_1_31_1 e_1_2_1_54_1 e_1_2_1_77_1 e_1_2_1_8_1 e_1_2_1_12_1 e_1_2_1_35_1 e_1_2_1_50_1 e_1_2_1_73_1 e_1_2_1_96_1 e_1_2_1_4_1 Aleman A (e_1_2_1_3_1) 2005; 77 e_1_2_1_110_1 e_1_2_1_16_1 e_1_2_1_39_1 e_1_2_1_58_1 McNaughton BL (e_1_2_1_72_1) 1996; 199 e_1_2_1_82_1 e_1_2_1_114_1 e_1_2_1_118_1 e_1_2_1_40_1 e_1_2_1_67_1 e_1_2_1_121_1 e_1_2_1_21_1 e_1_2_1_44_1 e_1_2_1_63_1 e_1_2_1_86_1 e_1_2_1_25_1 e_1_2_1_48_1 e_1_2_1_29_1 e_1_2_1_93_1 e_1_2_1_70_1 e_1_2_1_102_1 e_1_2_1_106_1 e_1_2_1_7_1 e_1_2_1_55_1 e_1_2_1_78_1 e_1_2_1_13_1 e_1_2_1_51_1 e_1_2_1_97_1 e_1_2_1_32_1 e_1_2_1_74_1 Vann SD (e_1_2_1_109_1) 2000; 20 Hess US (e_1_2_1_46_1) 1995; 15 e_1_2_1_17_1 e_1_2_1_36_1 e_1_2_1_59_1 e_1_2_1_60_1 e_1_2_1_113_1 e_1_2_1_117_1 e_1_2_1_41_1 e_1_2_1_68_1 e_1_2_1_120_1 e_1_2_1_45_1 e_1_2_1_83_1 e_1_2_1_22_1 e_1_2_1_49_1 e_1_2_1_26_1 Swanson LW (e_1_2_1_104_1) 1992 Berretta S (e_1_2_1_18_1) 2006 e_1_2_1_101_1 e_1_2_1_71_1 e_1_2_1_90_1 Lipska BK (e_1_2_1_64_1) 2002; 22 e_1_2_1_105_1 e_1_2_1_56_1 e_1_2_1_79_1 e_1_2_1_98_1 e_1_2_1_6_1 e_1_2_1_10_1 e_1_2_1_33_1 e_1_2_1_52_1 e_1_2_1_75_1 e_1_2_1_94_1 e_1_2_1_14_1 e_1_2_1_37_1 e_1_2_1_112_1 Hughes P (e_1_2_1_53_1) 1995; 47 e_1_2_1_116_1 e_1_2_1_42_1 e_1_2_1_65_1 e_1_2_1_88_1 e_1_2_1_23_1 e_1_2_1_61_1 e_1_2_1_27_1 e_1_2_1_69_1 Akirav I (e_1_2_1_2_1) 1999; 19 e_1_2_1_108_1 Pennypacker K (e_1_2_1_87_1) 1997; 12 e_1_2_1_100_1 e_1_2_1_91_1 e_1_2_1_30_1 e_1_2_1_76_1 e_1_2_1_5_1 e_1_2_1_57_1 O'Keefe JA (e_1_2_1_80_1) 1978 e_1_2_1_99_1 e_1_2_1_34_1 e_1_2_1_11_1 e_1_2_1_95_1 e_1_2_1_38_1 e_1_2_1_15_1 e_1_2_1_9_1 e_1_2_1_19_1 |
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| SubjectTerms | amygdala Amygdala - cytology Amygdala - drug effects Amygdala - physiology Animals Convulsants - toxicity Disease Models, Animal Environment Exploratory Behavior - physiology FOS hippocampus Hippocampus - cytology Hippocampus - physiology Male Neural Pathways Neurons - drug effects Neurons - pathology Neurons - physiology Picrotoxin - toxicity Proto-Oncogene Proteins c-fos - metabolism Rats Rats, Long-Evans schizophrenia Schizophrenia - chemically induced Schizophrenia - pathology Schizophrenia - physiopathology Space Perception - physiology spatial processing |
| Title | The amygdala modulates neuronal activation in the hippocampus in response to spatial novelty |
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