Amygdala and Ventral Hippocampus Contribute Differentially to Mechanisms of Fear and Anxiety.

McHugh, Stephen B.; Deacon, R. M. J.; Rawlins, J. N. P.; Bannerman, David M.

doi:10.1037/0735-7044.118.1.63

Cited by 336 publications

(270 citation statements)

References 93 publications

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“…Our adult findings accord with prior studies in adult rodents (Crawley, 1981;Crawley & Goodwin, 1980;McHugh, Deacon, Rawlins, & Bannerman, 2004;Ramos, Berton, Mormede, & Chaouloff, 1997). The youngest rats reported with use of the black and white box in the literature are early adolescents (P28 -P32).…”

Section: Discussionsupporting

confidence: 90%

Comparison of infant and adult rats in exploratory activity, diurnal patterns, and responses to novel and anxiety-provoking environments.

Smith¹,

Morrell²

2007

Behavioral Neuroscience

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Infant rats emerge from the maternal nest at Postnatal Day 17-18 to have their first critical environmental experiences; they may be particularly sensitive to experiences or experimental interventions that can affect their adult capacity. The authors address open questions on 2 components of normative environmental exploration, locomotor activity and response to anxiety-provoking locations, in Postnatal Day 18 infant and Postnatal Day 60 adult rats. The authors compare diurnal patterns of locomotor activity, wheel running, novel and familiar open-field activity, and 2 measures of anxiety. Infants have an equivalent capacity to adults for locomotor activity and wheel running and a fundamentally adult-like diurnal rhythm, except that they do not anticipate light-dark transitions, are more perturbable at their most somnolent, and are more or less active during specific limited phases than adults. Infants initially have a lower rate of locomotor activity in novel environments and have a greater willingness to be active in anxiety-provoking locations. Such differences may allow enhanced gathering of environmental information by the infant and are important to consider in the design of experiments using infants. Keywordsinfant; adult; exploration; activity; anxiety In humans, late childhood and adolescence is the period when drug sampling and experimentation first begins (Brown & Tapert 2004;Johnston, O'Malley, Bachman, & Schulenberg, 2005;Spear, 2000;Turner, Mermelstein, & Flay, 2004), when clinical mental health disorders requiring pharmacologic intervention, such as attention-deficit/hyperactivity disorder, emerge (Andersen, 2003;Andersen, Arvanitogiannis, Pliakas, LeBlanc, & Carlezon, 2002), and when the central nervous system (CNS) is readily shaped by many stimuli, often with long-lasting consequences. Ultimately, studies using immature animals may inform us about human disorders with early life origins (e.g., hyperactivity) and may inform the beneficial use of pharmacological treatments. Further, these studies may provide insight into the effects of preadolescent sampling of drugs of abuse (Dahl & Spear, 2004).Prior to achieving sexual maturity between Postnatal Days (P) 55-60, immature rats are either infants (P1-P28) or adolescents (P28-P55; Ojeda & Urbanski, 1988;Spear, 2000). Infant rats are vigilantly kept in the protective maternal nest by their mothers until around P17-P18 (Barnett, 1958;Galef & Clark, 1972; Pereira & Morrell, 2007;Small, 1899), when they are allowed out into their larger environment. At this point, they have full motor and sensory capacity (Moorcroft, Lyttle, & Campbell, 1971). Experiences at this point readily produce longCorrespondence concerning this article should be addressed to Kiersten S. Smith, Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102. E-mail: kismith@pegasus.rutgers.edu. NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript term effects; enriched environments lead...

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Section: Discussionsupporting

confidence: 90%

Comparison of infant and adult rats in exploratory activity, diurnal patterns, and responses to novel and anxiety-provoking environments.

Smith¹,

Morrell²

2007

Behavioral Neuroscience

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“…Increased expression of NPY (which also has anticonvulsant features; Richichi et al, 2004) in the hippocampus may also help in explaining the slower dentate gyrus kindling rate in betamethasone-exposed immature rats compared to saline-exposed rats in our previous study (Velíšek, 2005b). Earlier studies have shown that mainly ventral but also dorsal hippocampus is involved in anxiety control (Andrews et al, 1997;Bannerman et al, 2002aBannerman et al, , b, 2003Gonzalez et al, 1998;Kjelstrup et al, 2002;McHugh et al, 2004) and NPY alterations in the hippocampus affect anxiety behaviors (Heilig, 2004;Thorsell et al, 2000). We did not see an increase in NPY expression in the basolateral amygdala; however, lesion studies have demonstrated that this region does not participate in the anxiety behavior tested in the elevated plus maze (Gonzalez et al, 1996;Treit et al, 1993), and that the amygdala is rather associated with fear control .…”

Section: Technical Considerationsmentioning

confidence: 62%

Prenatal Exposure to Betamethasone Decreases Anxiety in Developing Rats: Hippocampal Neuropeptide Y as a Target Molecule

Velı́šek

2006

Neuropsychopharmacol

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Repeated antenatal administration of betamethasone is frequently used as a life-saving treatment in obstetrics. However, limited information is available about the outcome of this therapy in children. The initial prospective studies indicate that there are behavioral impairments in children exposed to repeated courses of prenatal betamethasone during the third trimester of pregnancy. In this study, pregnant rats received two betamethasone injections on day 15 of gestation. Using immunohistochemistry, the expression of a powerful anxiolytic molecule neuropeptide Y (NPY) was determined on postnatal day (PN) 20 in the hippocampus and basolateral amygdala (structures related to anxiety and fear) of the offspring. Prenatal betamethasone exposure induced significant increases in NPY expression in the hippocampus but not in the amygdala. Indeed, behavioral tests in the offspring, between PN20 and PN22 in the open field, on the horizontal bar, and in the elevated plus maze, indicated decreases in anxiety, without impairments in motor performance or total activity. Decreased body weight in betamethasone-exposed rats confirmed long-lasting effects of prenatal exposure. Thus, prenatal betamethasone treatment consistently increases hippocampal NPY, with decreases in anxiety-related behaviors and hippocampal role in anxiety in rats. Animal models may assist in differentiation between pathways of the desired main effect of the antenatal corticosteroid treatment and pathways of unwanted side effects. This differentiation can lead to specific therapeutic interventions directed against the side effects without eliminating the beneficial main effect of the corticosteroid treatment.

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“…In previous studies, lesions of the amygdala have failed to alter behavior in the elevated plus maze or other tests of novelty (McHugh et al, 2004;Treit et al, 1993a, b). Similarly, in this set of experiments, lidocaine inactivation of the CeA or BLA did not attenuate the anxiolytic properties of diazepam or baseline anxiety-like behaviors in the plus maze.…”

Section: Discussionmentioning

confidence: 98%

“…Although this is in agreement with other literature, it is at odds with the idea that the anxiolytic actions of these drugs are localized to amygdalar nuclei. Lesion techniques, however, induce permanent destruction of large areas encompassing much of the amygdaloid complex (Treit et al, 1993a, b;McHugh et al, 2004). They also require animals to recover from surgery for several days after the lesion is introduced, potentially allowing for neural adaptations.…”

Section: Discussionmentioning

confidence: 99%

“…Further, the anxiolytic properties of some drugs are localized to the amygdala (for reviews see (File, 2000;Menard and Treit, 1999)). Lesioning the amygdala, however, fails to alter baseline behavior in some tests (McHugh et al, 2004) or block the properties of anxiolytic drugs (Treit et al, 1993b;Treit et al, 1993a) in tests that rely on novelty, suggesting that this region may not be critically involved in regulating anxiety-like behavior. Contrary to these reports, the effects of chlordiazepoxide were blocked by microinjection of GABA A receptor antagonists into the BLA (Sanders and Shekhar, 1995).…”

Section: Introductionmentioning

confidence: 99%

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Microinjection of Naltrexone into the Central, but not the Basolateral, Amygdala Blocks the Anxiolytic Effects of Diazepam in the Plus Maze

Burghardt

Wilson

2005

Neuropsychopharmacol

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The amygdala is involved in behavioral and physiological responses to fear, and the anxiolytic properties of several drugs are localized to this region. Activation of endogenous opioid systems is known to occur in response to stress and a growing body of literature suggests that opioid systems regulate the properties of anxiolytic drugs. These experiments sought to elucidate the role of opioid receptors in the central (CeA) and basolateral (BLA) nuclei of the amygdala in regulating the anxiolytic properties of ethanol and diazepam. Male rats fitted with cannula received bilateral microinjections of the nonselective opioid receptor antagonist naltrexone (NAL) immediately followed by systemic delivery of either ethanol (1 g/kg) or diazepam (2 mg/kg) in the elevated plus maze. Both diazepam and ethanol decreased anxiety-like behavior. Delivery of NAL into the CeA blocked the anxiolytic properties of diazepam. Delivery of NAL into the BLA slightly increased open arm avoidance, but had no effect on the anxiolytic properties of diazepam. Microinjection of NAL into either nucleus failed to block the effects of ethanol. These results were specific to the anxiolytic properties of diazepam, since baseline behaviors were unaffected by microinjection of NAL. Microinjection of lidocaine produced results distinct from NAL and failed to block the anxiolytic actions of diazepam. These studies indicate distinct roles for opioid receptor systems in the CeA and BLA in regulating the anxiolytic properties of diazepam in the elevated plus maze. Further, opioid receptor systems in the CeA and BLA do not regulate the anxiolytic properties of ethanol in this test.

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Amygdala and Ventral Hippocampus Contribute Differentially to Mechanisms of Fear and Anxiety.

Cited by 336 publications

References 93 publications

Comparison of infant and adult rats in exploratory activity, diurnal patterns, and responses to novel and anxiety-provoking environments.

Comparison of infant and adult rats in exploratory activity, diurnal patterns, and responses to novel and anxiety-provoking environments.

Prenatal Exposure to Betamethasone Decreases Anxiety in Developing Rats: Hippocampal Neuropeptide Y as a Target Molecule

Microinjection of Naltrexone into the Central, but not the Basolateral, Amygdala Blocks the Anxiolytic Effects of Diazepam in the Plus Maze

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