Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection

Sarter, Martin; Hasselmo, Michael E.; Bruno, John P.; Givens, Bennet

doi:10.1016/j.brainresrev.2004.08.006

Cited by 596 publications

(576 citation statements)

References 185 publications

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“…We suggest that, by affecting these neural parameters, cholinergic modulation can play an important role in shaping the attentional learning process. This idea is consistent with the proposal that ACh seems to be involved in modulating the signal-noise ratio in neural activation (Patil et al, 1998;Sarter et al, 2005). Specifically, more recent analyzes indicate that ACh is capable of reducing background noise (Patil et al, 1998), which is consistent with an increase in contrast and layer gain, as implemented in our model.…”

Section: Ach Modulation Of Attention Via Layer Gainsupporting

confidence: 92%

Attentional control of associative learning—A possible role of the central cholinergic system

Pauli

O’Reilly

2008

Brain Research

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How does attention interact with learning? Kruschke [Kruschke, J.K. (2001). Toward a unified Model of Attention in Associative Learning. J. Math. Psychol. 45, proposed a model (EXIT) that captures Mackintosh's [Mackintosh, N.J. (1975). A theory of attention: Variations in the associability of stimuli with reinforcement. Psychological Review, 82(4), 276-298.] framework for attentional modulation of associative learning. We developed a computational model that showed analogous interactions between selective attention and associative learning, but is significantly simplified and, in contrast to EXIT, is motivated by neurophysiological findings. Competition among input representations in the internal representation layer, which increases the contrast between stimuli, is critical for simulating these interactions in human behavior. Furthermore, this competition is modulated in a way that might be consistent with the phasic activation of the central cholinergic system, which modulates activity in sensory cortices. Specifically, phasic increases in acetylcholine can cause increased excitability of both pyramidal excitatory neurons in cortical layers II/III and cortical GABAergic inhibitory interneurons targeting the same pyramidal neurons. These effects result in increased attentional contrast in our model. This model thus represents an initial attempt to link human attentional learning data with underlying neural substrates. KeywordsSelective attention; Associative learning; Layer gain; Acetylcholine; Neural network Except for moments of a "confused, dazed, scatterbrained state which in French is called distraction, and Zerstreutheit in German" (James, 1890, p. 404), we can hardly attend to more than one object or idea at one point in time. Mechanisms of selective attention control which information influences our behavior and our decisions. The focus of our attention can be redirected endogenously because of internal states, or shifted exogenously because of an innate or acquired salience of sensory stimuli. Endogenous attentional control depends on executive functions of the prefrontal cortex (and in the case of spatial attention, interactions with spatial systems in parietal lobes), which enables us to focus our attention based on our current needs or interests (Corbetta and Shulman, 2002). In contrast, this study addresses the neural mechanisms that drive the acquisition of attentional salience for sensory stimuli, which can then overcome the dominance of executive processes to allow our attention to be directed by significant events in our sensory environment. We developed a computational model of learned attentional salience, intended to capture in a very simplified framework the essential dynamics of processing in sensory and association cortex. The central cholinergic system can play an important additional modulatory role as part of a "circuit breaker" (Corbetta and Shulman, 2002) of the fronto-parietal attention system (see also Kimura et al., 1999). Our model incorporates another potential idea a...

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Section: Ach Modulation Of Attention Via Layer Gainsupporting

confidence: 92%

Attentional control of associative learning—A possible role of the central cholinergic system

Pauli

O’Reilly

2008

Brain Research

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“…In contrast, the recruitment of prefrontal cholinergic inputs in task-performing animals is thought to be mediated via direct prefrontal projections to the basal forebrain as well as via multi-synaptic circuits involving the nucleus accumbens and perhaps also the amygdala (Holland et al, 2000;Lee et al, 2006;Neigh-McCandless et al, 2002;Sarter et al, 2001Sarter et al, , 2005aZaborszky, 1997Zaborszky, , 2002Zahm, 2000). Together with evidence demonstrating the disruption of the prefrontal modulation of accumbens neurons following repeated psychostimulant exposure (Goto and Grace, 2005), the present findings suggest that repeated AMPH-exposure disrupts such telencephalic innervation of basal forebrain cholinergic neurons and thus, prefrontal ACh release.…”

Section: Discussionmentioning

confidence: 99%

“…Substantial evidence supports a crucial role of the cortical cholinergic input system in the mediation of attentional functions and capacities (Everitt and Robbins, 1997;Sarter et al, 2001Sarter et al, , 2005a. Removal of cortical cholinergic inputs produces persistent impairments in attentional performance.…”

Section: Introductionmentioning

confidence: 95%

Toward a Neuro-Cognitive Animal Model of the Cognitive Symptoms of Schizophrenia: Disruption of Cortical Cholinergic Neurotransmission Following Repeated Amphetamine Exposure in Attentional Task-Performing, but Not Non-Performing, Rats

Kozak

Martı́nez

Young

et al. 2007

Neuropsychopharmacol

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Impairments in attentional functions and capacities represent core aspects of the cognitive symptoms of schizophrenia. Attentional performance has been demonstrated to depend on the integrity and activity of cortical cholinergic inputs. The neurobiological, behavioral, and cognitive effects of repeated exposure to psychostimulants model important aspects of schizophrenia. In the present experiment, prefrontal acetylcholine (ACh) release was measured in attentional task-performing and non-performing rats pretreated with an escalating dosing regimen of amphetamine (AMPH) and following challenges with AMPH. In non-performing rats, pretreatment with AMPH did not affect the increases in ACh release produced by AMPH-challenges. In contrast, attentional task performanceassociated increases in ACh release were attenuated in AMPH-pretreated and AMPH-challenged rats. This effect of repeated AMPH exposure on ACh release was already present before task-onset, suggesting that the loss of cognitive control that characterized these animals' performance was a result of cholinergic dysregulation. The findings indicate that the demonstration of repeated AMPH-induced dysregulation of the prefrontal cholinergic input system depends on interactions between the effects of repeated AMPH exposure and cognitive performance-associated recruitment of this neuronal system. Repeated AMPH-induced disruption of prefrontal cholinergic activity and attentional performance represents a useful model to investigate the cholinergic mechanisms contributing to the cognitive impairments of schizophrenia.

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“…Acetylcholine modulates a wide array of cognitive functions, including arousal, attention, learning and memory [1][2][3]. Cholinergic input to the hippocampus originating predominantly from the medial septum (MS) is particularly important for learning and memory [4][5][6][7].…”

Section: Introductionmentioning

confidence: 99%

Vestibular stimulation enhances hippocampal long-term potentiation via activation of cholinergic septohippocampal cells

Tai

Leung

2012

Behavioural Brain Research

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Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection

Cited by 596 publications

References 185 publications

Attentional control of associative learning—A possible role of the central cholinergic system

Attentional control of associative learning—A possible role of the central cholinergic system

Toward a Neuro-Cognitive Animal Model of the Cognitive Symptoms of Schizophrenia: Disruption of Cortical Cholinergic Neurotransmission Following Repeated Amphetamine Exposure in Attentional Task-Performing, but Not Non-Performing, Rats

Vestibular stimulation enhances hippocampal long-term potentiation via activation of cholinergic septohippocampal cells

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