Hippocampal fibers make synaptic contacts with glutamate decar☐ylase-immunoreactive neurons in the rat nucleus accumbens

Meredith, Gloria E.; Wouterlood, Floris G.; Pattiselanno, A.

doi:10.1016/0006-8993(90)90476-r

Cited by 60 publications

(46 citation statements)

References 26 publications

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“…Despite a substantial number of studies documenting roles for the amygdala and hippocampus in encoding and processing memory for emotional events into long term storage (Cahill, et al, 1996;Canli, et al, 2000;Diamond, et al, 2005;Joels, et al, 2005;McGaugh 2004;Phelps, 2004;Richter-Levin & Akirav, 2003;van Stegeren, et al, 1998;Vianna, et al, 2004), the role of the accumbens shell which receives input from both areas (French & Totterdell, 2003;Groenewegen, et al, 1987;Meredith, et al, 1990;Mogenson, et al, 1980;Petrovich, et al, 1996;) as well as peripheral information from the NTS (Delfs, et al, 1998) has yet to be explored. The results from this study reveal a functional relationship between the NTS and nucleus accumbens shell in modulating memory following physiological arousal and suggests a role of norepinephrine in regulating synaptic activity in the accumbens shell to facilitate this mnemonic process.…”

Section: Discussionmentioning

confidence: 99%

“…In particular, the shell division receives input regarding decision related activities from the prefrontal cortex (French & Totterdell, 2002;Sesack & Pickel, 1992), affective components of experiences from the basolateral amygdala (Mogenson, et al, 1980;Petrovich, et al, 1996), contextual features comprising the environment from the hippocampus (Groenewegen, et al, 1987;Meredith, et al, 1990) and peripheral information in response to heightened states of physiological arousal from the vagus nerve and NTS (Delfs, et al, 1998;Kirouac & Ciriello, 1997;Mehendale, et al, 2004). It is important to note that the projections from the basolateral amygdala and hippocampus converge monosynaptically onto projection neurons within the caudomedial part of the accumbens shell (French & Totterdell, 2003).…”

Section: Discussionmentioning

confidence: 99%

“…This view derives from anatomical findings demonstrating that the accumbens shell receives neural input from the basolateral nucleus of the amygdala concerning the affective components of experiences (Mogenson, Jones, & Yim, 1980;Petrovich, Risold, & Swanson, 1996), projections from the ventral subiculum region of the hippocampus regarding contextual features from the environment (Groenewegen, Vermeulen-Van der Zee, Kortschot, & Witter, 1987;Meredith, Wouterlood, & Pattiselanno, 1990) and reward related components of learning experiences from the ventral tegmental area (Nauta, Smith, Faull, & Domesick, 1978).…”

Section: Introductionmentioning

confidence: 99%

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Functional interactions between the nucleus tractus solitarius (NTS) and nucleus accumbens shell in modulating memory for arousing experiences

Kerfoot

Chattillion

Williams

2008

Neurobiology of Learning and Memory

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The shell division of the nucleus accumbens receives noradrenergic input from neurons in the nucleus of the solitary tract (NTS) that transmit information regarding fluctuations in peripheral hormonal and autonomic activity. Accumbens shell neurons also receive converging inputs from limbic areas such as the hippocampus and amygdala that process newly acquired information. However, few studies have explored whether peripheral information regarding changes in emotional arousal contributes to memory processing in the accumbens. The beneficial effects on memory produced by emotional arousal and the corresponding activation of NTS neurons may be mediated through influences on neuronal activity in the accumbens shell during memory encoding. To explore this putative relationship, Experiment 1 examined interactions between the NTS and the accumbens shell in modulating memory for responses acquired after footshock training in a water-motivated inhibitory avoidance task. Memory for the noxious shock was significantly improved by posttraining excitation of noradrenergic NTS neurons. The enhanced retention produced by activating NTS neurons was attenuated by suppressing neuronal activity in the accumbens shell with bupivacaine (0.25%/0.5μl). Experiment 2 examined the direct involvement of accumbens shell noradrenergic activation in the modulation of memory for psychologically arousing events such as a reduction in perceived reward value. Noradrenergic activation of the accumbens shell with phenylephrine (1.0μg/0.5μl) produced an enhancement in memory for the frustrating experience relative to control injections as evidenced by runway performance on an extended seven-day retention test. These findings demonstrate a functional relationship between NTS neurons and the accumbens shell in modulating memory following physiological arousal and identifies a role of norepinephrine in modulating synaptic activity in the accumbens shell to facilitate this process.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Functional interactions between the nucleus tractus solitarius (NTS) and nucleus accumbens shell in modulating memory for arousing experiences

Kerfoot

Chattillion

Williams

2008

Neurobiology of Learning and Memory

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“…Along with noradrenergic innervation from A2 NTS neurons in the brainstem, the NAC also receives projections from both the hippocampus (Groenewegen et al 1987;Meredith et al 1990;French and Totterdell 2003) and basolateral amygdala (Mogenson et al 1980;Petrovich et al 1996;French and Totterdell 2003). These inputs may contribute to the capacity of the NAC to process declarative forms of information and store the motivational valence of stimuli into memory.…”

Section: Resultsmentioning

confidence: 99%

“…The shell division of the nucleus accumbens (NAC) receives highly processed information regarding affective and contextual features of new learning experiences from the amygdala and hippocampus, respectively (Mogenson et al 1980;Groenewegen et al 1987;Meredith et al 1990;Wang et al 1992;Brog et al 1993;Petrovich et al 1996;French and Totterdell 2003). These limbic inputs are complemented by norepinephrine containing axons supplied by the A2 class of noradrenergic neurons housed in the brainstem region of the nucleus of the solitary tract (NTS) (Delfs et al 1998).…”

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confidence: 99%

Interactions between brainstem noradrenergic neurons and the nucleus accumbens shell in modulating memory for emotionally arousing events

Kerfoot

Williams²

2011

Learn. Mem.

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The nucleus accumbens shell (NAC) receives axons containing dopamine-b-hydroxylase that originate from brainstem neurons in the nucleus of the solitary tract (NTS). Recent findings show that memory enhancement produced by stimulating NTS neurons after learning may involve interactions with the NAC. However, it is unclear whether these mnemonic effects are mediated by norepinephrine (NE) release from NTS terminals onto NAC neurons. The present studies approached this question by examining the contribution of NAC a-noradrenergic receptors in mediating this effect and assessed whether glutamatergic activation of the NTS alters NE concentrations in the NAC. Rats were trained for 6 d to drink from a water spout located at the end of an inhibitory avoidance chamber. On day 7, a 0.35-mA footshock was initiated once the rat approached the spout and remained active until it escaped into the neutral compartment. Blockade of a-noradrenergic receptors in the NAC with phentolamine (0.5 mg/0.5 mL) attenuated memory enhancement produced by glutamatergic (50 ng/0.5 mL) infusion on NTS neurons (P , 0.01). Experiment 2 used in vivo microdialysis to assess whether glutamate activation of NTS alters NAC NE concentrations. NE levels were unchanged by NTS infusion of phosphate-buffered saline (PBS) or low dose glutamate (50 ng/0.5 mL) but elevated significantly (P , 0.05) by combining the same dose with the footshock (0.35 mA, 2 sec) given in Study 1 or infusion of (100 ng/0.5 mL) glutamate alone. Findings demonstrate that NE released from NTS terminals enhances representations in memory by acting on a-noradrenergic receptors within the NAC.The shell division of the nucleus accumbens (NAC) receives highly processed information regarding affective and contextual features of new learning experiences from the amygdala and hippocampus, respectively (Mogenson et al. 1980;Groenewegen et al. 1987;Meredith et al. 1990;Wang et al. 1992;Brog et al. 1993;Petrovich et al. 1996;French and Totterdell 2003). These limbic inputs are complemented by norepinephrine containing axons supplied by the A2 class of noradrenergic neurons housed in the brainstem region of the nucleus of the solitary tract (NTS) (Delfs et al. 1998). Norepinephrine release from A2 NTS neurons play an important role in conveying information regarding experience-induced changes in the physiological state of the organism.The A2 neurons are activated during times of heightened arousal by the release of glutamate from vagal nerve fibers that ascend from the periphery to the brainstem (Allchin et al. 1994;King and Williams 2009). Highly arousing events increase epinephrine secretion from the adrenals and facilitate binding to b-adrenergic receptors along the vagus nerve (Lawrence et al. 1995) that in turn, increase impulse flow to brainstem neurons in the NTS (Lawrence et al. 1995;Miyashita and Williams 2006). Epinephrine administration, stimulation of the vagus nerve or direct infusion of glutamate onto A2 NTS neurons are all known to significantly potentiate norepinephrine release ...

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Injections of N‐methyl‐D‐aspartate into the ventral hippocampus increase extracellular dopamine in the ventral tegmental area and nucleus accumbens

Legault

Wise

1999

Synapse

117

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The nucleus accumbens septi receives inputs from dopaminergic neurons of the ventral tegmental area (VTA) and glutamatergic neurons of the ventral subiculum (VS). The convergence of these inputs in the NAS is important for the normal expression of exploratory locomotion; stimulation of the VS by injection of the glutamate receptor agonist N-methyl-D-aspartate (NMDA) causes dopamine-dependent increases in locomotion. In the present study, in vivo microdialysis in conjunction with high-performance liquid chromatography and electrochemical detection (HPLC-EC) was used to estimate changes in extracellular dopamine in the VTA and NAS in response to intra-VS injections of NMDA (0.074, 0.28, 0.74 microg). NMDA injections caused dose-dependent elevations in extracellular dopamine in each region. Each dose of NMDA clearly increased extracellular dopamine in the NAS, whereas only the two higher doses increased dopamine significantly in the VTA. The highest dose of NMDA elevated extracellular dopamine to approximately 180% of baseline in each region. Whereas elevations in NAS dopamine might be induced by impulse-independent local mechanisms, elevations of dopamine in the VTA are presumed to reflect increased somatodendritic release associated with increased impulse flow through dopamine neurons. Thus, the present study suggests that the modulation of dopaminergic neurotransmission by the ventral subiculum results from a trans-synaptic activation of dopamine cell bodies in the VTA.

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Hippocampal fibers make synaptic contacts with glutamate decar☐ylase-immunoreactive neurons in the rat nucleus accumbens

Cited by 60 publications

References 26 publications

Functional interactions between the nucleus tractus solitarius (NTS) and nucleus accumbens shell in modulating memory for arousing experiences

Functional interactions between the nucleus tractus solitarius (NTS) and nucleus accumbens shell in modulating memory for arousing experiences

Interactions between brainstem noradrenergic neurons and the nucleus accumbens shell in modulating memory for emotionally arousing events

Injections of N‐methyl‐D‐aspartate into the ventral hippocampus increase extracellular dopamine in the ventral tegmental area and nucleus accumbens

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