Cholinergic modulation of response gain in the rat primary visual cortex

Soma, Shogo; Shimegi, Satoshi; Suematsu, Naofumi; Sato, Hiromichi

doi:10.1038/srep01138

Cited by 44 publications

(47 citation statements)

References 52 publications

(116 reference statements)

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“…For example, the BF modulates the response gain of single neurons in the VC as well as enhancing the sensitivity of these neurons to low-contrast visual stimuli (45)(46)(47)(48)(49), highlighting that the BF augments the cortical representation of sensory stimuli, consistent with some aspects of attentional modulation (50). Along related lines, BF stimulation also accelerates visual learning and up-regulates cortical visually-evoked potentials (51,52) as well as boosting the reliability of neural signals about sensory information (53)(54)(55).…”

Section: Discussionmentioning

confidence: 78%

Basal forebrain contributes to default mode network regulation

Nair

Klaassen

Arató³

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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The default mode network (DMN) is a collection of cortical brain regions that is active during states of rest or quiet wakefulness in humans and other mammalian species. A pertinent characteristic of the DMN is a suppression of local field potential gamma activity during cognitive task performance as well as during engagement with external sensory stimuli. Conversely, gamma activity is elevated in the DMN during rest. Here, we document that the rat basal forebrain (BF) exhibits the same pattern of responses, namely pronounced gamma oscillations during quiet wakefulness in the home cage and suppression of this activity during active exploration of an unfamiliar environment. We show that gamma oscillations are localized to the BF and that gamma-band activity in the BF has a directional influence on a hub of the rat DMN, the anterior cingulate cortex, during DMNdominated brain states. The BF is well known as an ascending, activating, neuromodulatory system involved in wake-sleep regulation, memory formation, and regulation of sensory information processing. Our findings suggest a hitherto undocumented role of the BF as a subcortical node of the DMN, which we speculate may be important for switching between internally and externally directed brain states. We discuss potential BF projection circuits that could underlie its role in DMN regulation and highlight that certain BF nuclei may provide potential target regions for up-or down-regulation of DMN activity that might prove useful for treatment of DMN dysfunction in conditions such as epilepsy or major depressive disorder.gamma suppression | anterior cingulate cortex | granger causality A highly consistent finding across a wide range of functional imaging studies in humans is that a network of brain regions, referred to as the "default mode network" (DMN), increases its activity during passive mental states compared with the performance of cognitive tasks. This was initially shown in a metaanalysis of several PET studies (1), in which a distribution of brain regions broadly including the medial prefrontal, retrosplenial, and anterior cingulate cortex (ACC), as well as lateral parietal and temporal cortices, was shown to be activated when subjects were in a state of quiet restfulness. The DMN areas are thought to form a cohesive set of intrinsically coupled brain regions, such that fMRI activations in its component regions exhibit similar time courses, allowing them to be identified reliably using seed-region analysis (2-4). Activity in the DMN exhibits anticorrelation with a complementary, largely nonoverlapping, set of fronto-parietal brain areas known as the "dorsal attention network" (DAN) (5). It should be noted, however, that particular brain structures may harbor functionally heterogeneous elements and thus may contribute to multiple functions, as was shown for the ACC (6). During wakefulness, the human brain thus alternates between DAN-and DMN-dominated activation states, corresponding to effortful cognitive task performance on the one hand and quiet restful...

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Section: Discussionmentioning

confidence: 78%

Basal forebrain contributes to default mode network regulation

Nair

Klaassen

Arató³

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

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“…On the other hand, we recently found that microionophoretic administration of ACh in rat V1 causes no biased laminar distribution of the ACh effects [26]. One plausible explanation for the discrepancy is the ACh distribution.…”

Section: Introductionmentioning

confidence: 87%

“…The primary visual cortex (V1) is one target of cholinergic projections, and its visual information processing is modulated by ACh in many species including primate [17]–[21], tree shrew [22], cat [23]–[25], and rodent [26]. The modulatory effects of ACh have been mainly examined using local microionophoretic administration of ACh or agonists/antagonists of ACh receptors (AChRs).…”

Section: Introductionmentioning

confidence: 99%

“…The modulatory effects of ACh have been mainly examined using local microionophoretic administration of ACh or agonists/antagonists of ACh receptors (AChRs). ACh facilitates or suppresses the visual responses of individual V1 neurons [17]–[26], and its modulatory effects are associated with changes in the gain of the contrast-response function [17], [18], [20], [22], [26]. Moreover, ACh has been known to change the selectivity of stimulus-features such as orientation, direction, and size [19], [21]–[25].…”

Section: Introductionmentioning

confidence: 99%

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Modulation-Specific and Laminar-Dependent Effects of Acetylcholine on Visual Responses in the Rat Primary Visual Cortex

et al. 2013

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Acetylcholine (ACh) is secreted from cholinergic neurons in the basal forebrain to regions throughout the cerebral cortex, including the primary visual cortex (V1), and influences neuronal activities across all six layers via a form of diffuse extrasynaptic modulation termed volume transmission. To understand this effect in V1, we performed extracellular multi-point recordings of neuronal responses to drifting sinusoidal grating stimuli from the cortical layers of V1 in anesthetized rats and examined the modulatory effects of topically administered ACh. ACh facilitated or suppressed the visual responses of individual cells with a laminar bias: response suppression prevailed in layers 2/3, whereas response facilitation prevailed in layer 5. ACh effects on the stimulus contrast-response function showed that ACh changes the response gain upward or downward in facilitated or suppressed cells, respectively. Next, ACh effects on the signal-to-noise (S/N) ratio and the grating-phase information were tested. The grating-phase information was calculated as the F1/F0 ratio, which represents the amount of temporal response modulation at the fundamental frequency (F1) of a drifting grating relative to the mean evoked response (F0). In facilitated cells, ACh improved the S/N ratio, while in suppressed cells it enhanced the F1/F0 ratio without any concurrent reduction in the S/N ratio. These effects were predominantly observed in regular-spiking cells, but not in fast-spiking cells. Electrophysiological and histological findings suggest that ACh promotes the signaling of grating-phase information to higher-order areas by a suppressive effect on supragranular layers and enhances feedback signals with a high S/N ratio to subcortical areas by a facilitatory effect on infragranular layers. Thus, ACh distinctly and finely controls visual information processing in a manner that is specific for the modulation and cell type and is also laminar dependent.

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“…ACh executes an action by controlling the gain of the neuron response (Soma et al, 2012, 2013a). For example, ACh increases the gain of the visual response to contrast (Bhattacharyya et al, 2013; Soma et al, 2013a) or orientation selectivity (Zinke et al, 2006).…”

Section: Muscarinic Influence On Visual Processing In V1mentioning

confidence: 99%

Distribution and effects of the muscarinic receptor subtypes in the primary visual cortex

Groleau

Kang

Huppé-Gourgues

et al. 2015

Front. Synaptic Neurosci.

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Muscarinic cholinergic receptors modulate the activity and plasticity of the visual cortex. Muscarinic receptors are divided into five subtypes that are not homogeneously distributed throughout the cortical layers and cells types. This distribution results in complex action of the muscarinic receptors in the integration of visual stimuli. Selective activation of the different subtypes can either strengthen or weaken cortical connectivity (e.g., thalamocortical vs. corticocortical), i.e., it can influence the processing of certain stimuli over others. Moreover, muscarinic receptors differentially modulate some functional properties of neurons during experience-dependent activity and cognitive processes and they contribute to the fine-tuning of visual processing. These functions are involved in the mechanisms of attention, maturation and learning in the visual cortex. This minireview describes the anatomo-functional aspects of muscarinic modulation of the primary visual cortex’s (V1) microcircuitry.

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Cholinergic modulation of response gain in the rat primary visual cortex

Cited by 44 publications

References 52 publications

Basal forebrain contributes to default mode network regulation

Basal forebrain contributes to default mode network regulation

Modulation-Specific and Laminar-Dependent Effects of Acetylcholine on Visual Responses in the Rat Primary Visual Cortex

Distribution and effects of the muscarinic receptor subtypes in the primary visual cortex

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