Association learning-dependent increases in acetylcholine release in the rat auditory cortex during auditory classical conditioning

Department of Psychology, California State University San Bernardino, San Bernardino, CA 92399, USA.
Neurobiology of Learning and Memory (Impact Factor: 3.65). 06/2009; 92(3):400-9. DOI: 10.1016/j.nlm.2009.05.006
Source: PubMed


The cholinergic system has been implicated in sensory cortical plasticity, learning and memory. This experiment determined the relationship between the acquisition of a Pavlovian conditioned approach response (CR) to an auditory conditioned stimulus (CS) and the release of acetylcholine (ACh) in the primary auditory cortex in rats. Samples of ACh were collected via microdialysis during behavioral training in either an auditory classical conditioning task or in a non-associative control task. The conditioning group received daily pairings of a white noise CS with a sucrose pellet unconditioned stimulus (US), while the control group received an equal number of CS and US presentations, but with these stimuli being presented randomly. Training was conducted on three consecutive days, with microdialysis samples being collected on Days 1 and 3 in separate sub-groups. The level of ACh released in the auditory cortex during conditioning trials increased from the first to the third day of training in the conditioning group as rats acquired the CR, but did not change in the control group, which did not acquire a CR. These data provide direct evidence for the hypothesis that ACh release increases in the primary auditory cortex during natural memory formation, where cholinergic activation is known to contribute to the formation of specific associative representational plasticity in conjunction with specific memory formation.

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    • "Area A1 is strongly innervated by cholinergic afferents, notably from the nucleus basalis (NB), which can induce strong local plasticity via muscarinic receptors (Ji et al. 2001; Miasnikov et al. 2001; Butt et al. 2009; Froemke et al. 2013). Electrically stimulating the NB during tone presentation alters the tuning of individual neurons (Froemke et al. 2013) and remaps cortex to selectively expand the region representing the corresponding tone (Dimyan and Weinberger 1999) or other acoustic features like frequency sweeps and pulse sequences (Kilgard and Merzenich 1998a,b; Weinberger 1998; Kilgard et al. 2001). "
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    ABSTRACT: Historically, the body's sensory systems have been presumed to provide the brain with raw information about the external environment, which the brain must interpret to select a behavioral response. Consequently, studies of the neurobiology of learning and memory have focused on circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulus-specific changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. This review synthesizes evidence across sensory modalities to report emerging themes, including the systems' flexibility to emphasize different aspects of a sensory stimulus depending on its predictive features and ability of different forms of learning to produce similar plasticity in sensory structures. Potential functions of this learning-induced neuroplasticity are discussed in relation to the challenges faced by sensory systems in changing environments, and evidence for absolute changes in sensory ability is considered. We also emphasize that this plasticity may serve important nonsensory functions, including balancing metabolic load, regulating attentional focus, and facilitating downstream neuroplasticity.
    Preview · Article · Nov 2015 · Learning & memory (Cold Spring Harbor, N.Y.)
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    • "The apparent " return " to normality of memory at 4 days for VAChT KD HET mice may simply reflect a much slower build-up of memory to regular LTM levels in the animals with decreased ACh tone, so that it would take 4 days instead of one to encode the trace. Such an explanation would be in line with recent observations of a very protracted ACh intervention in other forms of memory [28]. Unfortunately, we were not able to see if the VAChT KD HOM mice would be able to remember the object after a longer delay (8 days) because this memory is absent even in the WT mice. "
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    ABSTRACT: Acetylcholine (ACh) is important for different cognitive functions such as learning, memory and attention. The release of ACh depends on its vesicular loading by the vesicular acetylcholine transporter (VAChT). It has been demonstrated that VAChT expression can modulate object recognition memory. However, the role of VAChT expression on object recognition memory persistence still remains to be understood. To address this question we used distinct mouse lines with reduced expression of VAChT, as well as pharmacological manipulations of the cholinergic system. We showed that reduction of cholinergic tone impairs object recognition memory measured at 24h. Surprisingly, object recognition memory, measured at 4 days after training, was impaired by substantial, but not moderate, reduction in VAChT expression. Our results suggest that levels of acetylcholine release strongly modulate object recognition memory consolidation and appear to be of particular importance for memory persistence 4 days after training.
    Full-text · Article · Oct 2012 · Behavioural brain research
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    • "Apparently, synchronization patterns become more important for perception as task demands become more difficult either by having highly perceptually similar odors (Stopfer et al., 1997) or because more complicated processes than odor discrimination are involved, especially memorization and comparison of stimuli across time. Indeed, tasks in which a small temporal delay between stimulus and decision is involved may rely on bulbar plasticity which could be facilitated by muscarinic receptor modulation as shown in other systems (Weinberger, 2003; Roberts et al., 2005; Butt et al., 2009), however this hypothetical role of muscarinic receptors in the bulb remains to be tested. "
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    ABSTRACT: Neuromodulation in sensory perception serves important functions such as regulation of signal to noise ratio, attention, and modulation of learning and memory. Neuromodulators in specific sensory areas often have highly similar cellular, but distinct behavioral effects. To address this issue, we here review the function and role of two neuromodulators, acetylcholine (Ach) and noradrenaline (NE) for olfactory sensory processing in the adult main olfactory bulb. We first describe specific bulbar sensory computations, review cellular effects of each modulator and then address their specific roles in bulbar sensory processing. We finally put these data in a behavioral and computational perspective.
    Preview · Article · Aug 2012 · Frontiers in Behavioral Neuroscience
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