Cortical cholinergic activity is related to the novelty of the stimulus

Miranda, Marı́a Isabel; Ramı́rez-Lugo, Leticia; Bermúdez‐Rattoni, Federico

doi:10.1016/s0926-6410(00)00050-1

Cited by 96 publications

(64 citation statements)

References 26 publications

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“…Dynamic changes in neuromodulation that are contingent on task context and behavioral performance could promote efficient perceptual and semantic processing, allowing lower, transient activity to suffice when possible. Such ideas are consistent with evidence that the release of acetylcholine and norepinephrine is enhanced during the presentation of novel or behaviorally relevant stimuli, as well as following poor behavioral performance (Acquas et al, 1996;Aston-Jones & Bloom, 1981;Butt et al, 1997;Coull, 1994Coull, , 1998Miranda et al, 2000;Ressler & Nemeroff, 1999). In addition to dynamic changes in neuromodulatory levels, top-down neural activity from the prefrontal cortex may help to sustain perceptual and semantic processing in more posterior cortical regions that would otherwise attenuate owing to synaptic depression (see Grossberg, 1976Grossberg, , 1980, for similar ideas).…”

Section: Theoretical Considerationssupporting

confidence: 75%

“…Norepinephrine also appears to be integral to arousal, detection of changes in the external environment, aspects of emotional processing, and executive function (Aston-Jones & Bloom, 1981;Coull, 1994Coull, , 1998Ressler & Nemeroff, 1999;Servan-Schreiber, Printz, & Cohen, 1990). Increased levels of acetylcholine appear to be associated with the presentation of novel or behaviorally relevant sensory stimuli (e.g., Acquas, Wilson, & Fibiger, 1996;Butt, Testylier, & Dykes, 1997;Miranda, Ramirez-Lugo, & Bermudez-Rattoni, 2000). The brain's supply of acetylcholine and norepinephrine is provided by subcortical nuclei of the basal forebrain and brain stem (a series of basal forebrain nuclei, Ch1-Ch4, along with the reticular formation in the brain stem, supplies acetylcholine; the locus coeruleus in the brainstem supplies norepinephrine).…”

Section: Neuromodulation and Refractory Processesmentioning

confidence: 99%

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The impact of synaptic depression following brain damage: A connectionist account of "access/refractory" and "degraded-store" semantic impairments

Gotts

Plaut

2002

Cognitive, Affective, & Behavioral Neuroscience

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Neuropsychological studies of patients with acquired semantic impairments have yielded two distinct and contrasting patterns of performance in a spoken-word/picture-matching task (Warrington & Cipolotti, 1996). Patients labeled access/refractory are strongly influenced by presentation rate, semantic relatedness of distractors, and repetition, yet they seem relatively unaffected by lexical frequency. Degraded-store patients, on the other hand, are strongly affected by lexical frequency but are less affected by presentation rate, semantic relatedness, or repetition. Our account of these patterns of performance is based on the distinction between two different types of neurological damage:(1) damage to neuromodulatory systems that function to amplify neural signals while suppressing normal refractory-like effects and (2) damage to connections between groups of neurons that encode semantic information and are sensitive to frequency/familiarity. We present a connectionist model that learns to map spoken-word input to semantic representations and that incorporates a particular form of neural refractoriness referred to as synaptic depression, as well as a simple form of neuromodulation. We show that the model is capable of accounting for the contrasting patterns of semantic impairment under these two different forms of damage and, furthermore, demonstrate how it is capable of handling several documented cases that are exceptions to the basic patterns of impairment. Several predictions and limitations of the present model are discussed.

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Section: Theoretical Considerationssupporting

confidence: 75%

Section: Neuromodulation and Refractory Processesmentioning

confidence: 99%

The impact of synaptic depression following brain damage: A connectionist account of "access/refractory" and "degraded-store" semantic impairments

Gotts

Plaut

2002

Cognitive, Affective, & Behavioral Neuroscience

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“…Relationship between cholinergic inputs to the insular cortex (IC), the primary gustatory cortex, and gustatory processing are well established by studies of behavioral pharmacology and physiology (reviewed by Miranda et al 2003). Novel tastes increase the concentration of acetylcholine (ACh) in the IC, whereas familiar tastes do not (Miranda et al 2000). Inactivation of the nucleus basalis magnocellularis, which is one cholinergic source in the basal forebrain, impairs CTA acquisition (Miranda and Bermúdez-Rattoni 1999).…”

Section: Introductionmentioning

confidence: 99%

Postsynaptic Cell Type–Dependent Cholinergic Regulation of GABAergic Synaptic Transmission in Rat Insular Cortex

Yamamoto¹,

Koyanagi²,

Koshikawa

et al. 2010

Journal of Neurophysiology

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Yamamoto K, Koyanagi Y, Koshikawa N, Kobayashi M. Postsynaptic cell type-dependent cholinergic regulation of GABAergic synaptic transmission in rat insular cortex. J Neurophysiol 104: 1933-1945. First published August 4, 2010 doi:10.1152/jn.00438.2010. The cerebral cortex consists of multiple neuron subtypes whose electrophysiological properties exhibit diverse modulation patterns in response to neurotransmitters, including noradrenaline and acetylcholine (ACh). We performed multiple whole cell patch-clamp recording from layer V GABAergic interneurons and pyramidal cells of rat insular cortex (IC) to examine whether cholinergic effects on unitary inhibitory postsynaptic currents (uIPSCs) are differentially regulated by ACh receptors, depending on their presynaptic and postsynaptic cell subtypes. In fast-spiking (FS) to pyramidal cell synapses, carbachol (10 M) invariably decreased uIPSC amplitude by 51.0%, accompanied by increases in paired-pulse ratio (PPR) of the second to first uIPSC amplitude, coefficient of variation (CV) of the first uIPSC amplitude, and failure rate. Carbachol-induced uIPSC suppression was dose dependent and blocked by atropine, a muscarinic ACh receptor antagonist. Similar cholinergic suppression was observed in non-FS to pyramidal cell synapses. In contrast, FS to FS/non-FS cell synapses showed heterogeneous effects on uIPSC amplitude by carbachol. In roughly 40% of pairs, carbachol suppressed uIPSCs by 35.8%, whereas in a similar percentage of pairs uIPSCs were increased by 34.8%. Non-FS to FS/non-FS cell synapses also showed carbacholinduced uIPSC facilitation by 29.2% in about half of the pairs, whereas nearly 40% of pairs showed carbachol-induced suppression of uIPSCs by 40.3%. Carbachol tended to increase uIPSC amplitude in interneuron-to-interneuron synapses with higher PPR, suggesting that carbachol facilitates GABA release in interneuron synapses with lower release probability. These results suggest that carbachol-induced effects on uIPSCs are not homogeneous but preiotropic: i.e., cholinergic modulation of GABAergic synaptic transmission is differentially regulated depending on postsynaptic neuron subtypes.

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“…Therefore, the present study examined the involvement of the IC in the consolidation of object recognition memory, a task based on the tendency of rodents to explore a novel object more than a familiar one (Ennaceur and Delacour 1988). As microdialysis studies have shown that the release of acetylcholine in the IC in response to a novel, but not a familiar, taste stimulus (Miranda et al 2000) and cortical cholinergic activity is involved in the acquisition of object recognition memory (Tang et al 1997;Warburton et al 2003), the present study examined whether the muscarinic cholinergic receptor antagonist scopolamine infused into the IC immediately after training impairs the consolidation of object recognition memory. To control for site specificity, other rats received posttraining infusions of scopolamine into the frontoparietal cortex (FPC), dorsomedial but adjacent to the IC.…”

mentioning

confidence: 99%

“…These findings indicate a timelimited involvement of cholinergic activation in the IC in the consolidation of recognition memory and are congruent with extensive evidence indicating a critical role of the cholinergic system of the IC in taste memory consolidation (Naor and Dudai 1996;Gutierrez et al 2003a,b). Microdialysis studies have shown that exposure to novel environments or novel tastes produces a significant cortical release of acetylcholine, but not of glutamate or GABA (Miranda et al 2000(Miranda et al , 2002Giovannini et al 2001). However, after several presentations of a given taste or exposures to the same environment, there is a significant weakening of the acetylcholine response until it reaches baseline levels (Acquas et al 1996;Pepeu and Blandina 1998;Miranda et al 2000).…”

mentioning

confidence: 99%

Insular cortex is involved in consolidation of object recognition memory

Bermúdez-Rattoni¹,

Okuda²,

Roozendaal³

et al. 2005

Learn. Mem.

105

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Previous findings indicate that the insular cortex (IC) is involved in conditioned taste aversion and taste recognition. Here we report evidence that the IC is not uniquely dedicated to taste learning but plays a more general role in consolidating recognition memories. Immediate post-training infusions of the muscarinic cholinergic receptor antagonist scopolamine administered into the IC produced locus-specific and time-dependent impairment of object recognition memory.Extensive evidence indicates that the IC, also termed gustatory cortex, is critically involved in conditioned taste aversion and taste recognition memory (Bermudez-Rattoni 2004). Although most studies of the involvement of the IC in memory have investigated taste, there is some evidence that the IC is involved in memory that is not based on taste Paller et al. 2003;Reed et al. 2004). Converging evidence from animal and human studies suggests that a network of temporal cortical regions participates in recognition memory (Tang et al. 1997;Aggleton and Brown 1999;Malkova and Mishkin 2003;Reed et al. 2004). However, there is little information on the role of the IC in visual recognition memory. Therefore, the present study examined the involvement of the IC in the consolidation of object recognition memory, a task based on the tendency of rodents to explore a novel object more than a familiar one (Ennaceur and Delacour 1988). As microdialysis studies have shown that the release of acetylcholine in the IC in response to a novel, but not a familiar, taste stimulus (Miranda et al. 2000) and cortical cholinergic activity is involved in the acquisition of object recognition memory (Tang et al. 1997;Warburton et al. 2003), the present study examined whether the muscarinic cholinergic receptor antagonist scopolamine infused into the IC immediately after training impairs the consolidation of object recognition memory. To control for site specificity, other rats received posttraining infusions of scopolamine into the frontoparietal cortex (FPC), dorsomedial but adjacent to the IC. All experimental procedures were in compliance with NIH guidelines and approved by the UC Irvine's Institutional Animal Care and Use Committee.Adult male Sprague-Dawley rats (280-320 g at time of surgery) from Charles River Laboratories were implanted under sodium pentobarbital anesthesia (50 mg/kg, ip) with bilateral guide cannulae (23-ga.) aimed either at the IC [coordinates of the infusion sites from bregma (Paxinos and Watson 1986): anteroposterior (AP), +1.2 mm; mediolateral (ML), ‫5.5ע‬ mm; dorsoventral (DV), ‫5.6מ‬ mm] or the FPC (AP, +1.2 mm; ML, ‫0.4ע‬ mm; DV, ‫0.3מ‬ mm). Histological examination revealed that the injection needle tips were placed in the granular and agranular divisions of the IC, from ‫3.0מ‬ to +1.7 mm from bregma (Fig. 1A). Needles aimed at the FPC were found in the dorsal FPC from ‫8.0מ‬ to +1.7 mm from bregma (Fig. 1B). Three animals with cannulae misplacements were excluded from analyses, leaving 8-11 animals per group.After recovery, the rats were trai...

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Cortical cholinergic activity is related to the novelty of the stimulus

Cited by 96 publications

References 26 publications

The impact of synaptic depression following brain damage: A connectionist account of "access/refractory" and "degraded-store" semantic impairments

The impact of synaptic depression following brain damage: A connectionist account of "access/refractory" and "degraded-store" semantic impairments

Postsynaptic Cell Type–Dependent Cholinergic Regulation of GABAergic Synaptic Transmission in Rat Insular Cortex

Insular cortex is involved in consolidation of object recognition memory

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