Glucocorticoid enhancement of dorsolateral striatum-dependent habit memory requires concurrent noradrenergic activity

Goodman, Jarid; Leong, Kah-Chung; Packard, Mark G.

doi:10.1016/j.neuroscience.2015.10.014

Cited by 31 publications

(25 citation statements)

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“…Region‐specific differences in cholinergic and dopaminergic signalling contributes to hippocampal versus striatal strategies in dual solution tasks (McIntyre, Marriott, & Gold, ; Packard and White, ). Reduced glucocorticoid‐norepinephrine signalling (Goodman, Leong, & Packard, ) or enhanced estrogen signalling (Korol and Pisani, ) are also candidates for exercise‐mediated spatial bias. Finally, animals with hippocampal damage can demonstrate a limited degree of spatial learning (Day, Weisand, Sutherland, & Schallert, ; Eichenbaum et al, ; Whishaw, Cassel, & Jarrad, ).…”

Section: Discussionmentioning

confidence: 99%

Running promotes spatial bias independently of adult neurogenesis

2017

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Different memory systems offer distinct advantages to navigational behavior. The hippocampus forms complex associations between environmental stimuli, enabling flexible navigation through space. In contrast, the dorsal striatum associates discrete cues and favorable behavioral responses, enabling habit-like, automated navigation. While these two systems often complement one another, there are instances where striatal-dependent responses (e.g. approach a cue) conflict with hippocampal representations of spatial goals. In conflict situations, preference for spatial vs. response strategies varies across individuals and depends on previous experience, plasticity and the integrity of these two memory systems. Here, we investigated the role of adult hippocampal neurogenesis and exercise on mouse search strategies in a water maze task that can be solved with either a hippocampal-dependent place strategy or a striatal-dependent cue-response strategy. We predicted that inhibiting adult neurogenesis would impair hippocampal function and shift behavior towards striatal-dependent cue responses. However, blocking neurogenesis in a transgenic nestin-TK mouse did not affect strategy choice. We then investigated whether a pro-neurogenic stimulus, running, would bias mice towards hippocampal-dependent spatial strategies. While running indeed promoted spatial strategies, it did so even when neurogenesis was inhibited in nestin-TK mice. These findings indicate that exercise-induced increases in neurogenesis are not always required for enhanced cognitive function. Furthermore, our data identify exercise as a potentially useful strategy for promoting flexible, cognitive forms of memory in habit-related disorders that are characterized by excessive responding to discrete cues.

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Section: Discussionmentioning

confidence: 99%

Running promotes spatial bias independently of adult neurogenesis

2017

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“…One possibility is that stress hormones directly increase activation of the DLS. Indeed, previous evidence indicates that systemic or direct administration of corticosterone into the dorsal striatum enhances memory consolidation in both the cued water maze and inhibitory avoidance task (Medina et al., 2007, Quirarte et al., 2009, Goodman et al., 2015). Thus, fear CS exposure may be associated with the release of stress hormones such as corticosterone that directly increase activity of the DLS and consequently enhance habit memory consolidation in the plus-maze.…”

Section: Discussionmentioning

confidence: 99%

“…Notably, we have recently demonstrated that the corticosterone-induced enhancement of DLS-dependent habit memory may also be blocked by concurrent propranolol administration (Goodman et al., 2015). Thus, consistent with the view that glucocorticoid and noradrenergic mechanisms might interact to produce the emotional enhancement of habit memory, CS exposure in the present study would be expected to increase the release of glucocorticoids (Goldstein et al., 1996, Cordero et al., 1998, Hagewoud et al., 2011), whereas administration of propranolol might prevent glucocorticoids from enhancing habit memory (Goodman et al., 2015). …”

Section: Discussionmentioning

confidence: 99%

“…Converging evidence indicates that DLS-dependent habit memory in the plus-maze may be facilitated by the induction of emotional arousal through the exposure of animals to aversive unconditioned stimuli (Packard, 2009, Packard and Goodman, 2012, Packard and Goodman, 2013, Sandi, 2013, Schwabe, 2013). For example, DLS-dependent habit memory may be facilitated following chronic restraint stress, tail shock, exposure to predator odor, or administration of anxiogenic drugs (Kim et al., 2001, Packard and Wingard, 2004, Wingard and Packard, 2008, Elliott and Packard, 2008, Schwabe et al., 2010c, Packard and Gabriele, 2009, Leong et al., 2012, Leong and Packard, 2014, Taylor et al., 2014, Goodman et al., 2015). Furthermore, some evidence suggests that, as observed with unconditioned emotional stimuli, exposure to emotionally arousing conditioned stimuli also modulates memory (Holahan and White, 2002, Holahan and White, 2004, Hawley et al., 2013, Leong et al., 2015).…”

Section: Introductionmentioning

confidence: 99%

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Enhancement of striatum-dependent memory by conditioned fear is mediated by beta-adrenergic receptors in the basolateral amygdala

Goode

Leong

Goodman

et al. 2016

Neurobiology of Stress

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Emotional arousal can have a profound impact on various learning and memory processes. For example, unconditioned emotional stimuli (e.g., predator odor or anxiogenic drugs) enhance dorsolateral striatum (DLS)-dependent habit memory. These effects critically depend on a modulatory role of the basolateral complex of the amygdala (BLA). Recent work indicates that, like unconditioned emotional stimuli, exposure to an aversive conditioned stimulus (CS) (i.e., a tone previously paired with shock) can also enhance consolidation of DLS-dependent habit memory. The present experiments examined whether noradrenergic activity, particularly within the BLA, is required for a fear CS to enhance habit memory consolidation. First, rats underwent a fear conditioning procedure in which a tone CS was paired with an aversive unconditioned stimulus. Over the course of the next five days, rats received training in a DLS-dependent water plus-maze task, in which rats were reinforced to make a consistent body-turn response to reach a hidden escape platform. Immediately after training on days 1–3, rats received post-training systemic (Experiment 1) or intra-BLA (Experiment 2) administration of the β-adrenoreceptor antagonist, propranolol. Immediately after drug administration, half of the rats were re-exposed to the tone CS in the conditioning context (without shock). Post-training CS exposure enhanced consolidation of habit memory in vehicle-treated rats, and this effect was blocked by peripheral (Experiment 1) or intra-BLA (Experiment 2) propranolol administration. The present findings reveal that noradrenergic activity within the BLA is critical for the enhancement of DLS-dependent habit memory as a result of exposure to conditioned emotional stimuli.

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“…Most interestingly, there is first evidence that stress effects on dorsal striatum‐dependent memory may necessitate simultaneous glucocorticoid and noradrenergic activity as well. Specifically, a recent study showed that corticosterone injections shortly after training in a cued water maze task or a response‐based version of the water plus maze task enhanced subsequent memory and this memory enhancement disappeared after concurrent administration of propranolol (Goodman et al ., ). Although this study administered the drugs systemically and therefore allows no conclusions regarding the site of the glucocorticoid‐noradrenaline interactions, it is well‐known that the amygdala projects directly to the caudate nucleus (Pikänen, ), making it tempting to speculate that also stress (hormone) effects on dorsal striatal memory are mediated by the stress‐related noradrenergic activation of the amygdala.…”

Section: Focus On Single Memory Systemsmentioning

confidence: 98%

Memory under stress: from single systems to network changes

Schwabe

2016

Eur J of Neuroscience

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Stressful events have profound effects on learning and memory. These effects are mainly mediated by catecholamines and glucocorticoid hormones released from the adrenals during stressful encounters. It has been known for long that both catecholamines and glucocorticoids influence the functioning of the hippocampus, a critical hub for episodic memory. However, areas implicated in other forms of memory, such as the insula or the dorsal striatum, can be affected by stress as well. Beyond changes in single memory systems, acute stress triggers the reconfiguration of large scale neural networks which sets the stage for a shift from thoughtful, 'cognitive' control of learning and memory toward more reflexive, 'habitual' processes. Stress-related alterations in amygdala connectivity with the hippocampus, dorsal striatum, and prefrontal cortex seem to play a key role in this shift. The bias toward systems proficient in threat processing and the implementation of well-established routines may facilitate coping with an acute stressor. Overreliance on these reflexive systems or the inability to shift flexibly between them, however, may represent a risk factor for psychopathology in the long-run.

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Glucocorticoid enhancement of dorsolateral striatum-dependent habit memory requires concurrent noradrenergic activity

Cited by 31 publications

References 70 publications

Running promotes spatial bias independently of adult neurogenesis

Running promotes spatial bias independently of adult neurogenesis

Enhancement of striatum-dependent memory by conditioned fear is mediated by beta-adrenergic receptors in the basolateral amygdala

Memory under stress: from single systems to network changes

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