Cholinergic and serotonergic modulation of visual information processing in monkey V1

Abstract

The brain dynamically changes its input-output relationship depending on the behavioral state and context in order to optimize information processing. At the molecular level, cholinergic/monoaminergic transmitters have been extensively studied as key players for the state/context-dependent modulation of brain function. In this paper, we review how cortical visual information processing in the primary visual cortex (V1) of macaque monkey, which has a highly differentiated laminar structure, is optimized by serotonergic and cholinergic systems by examining anatomical and in vivo electrophysiological aspects to highlight their similarities and distinctions. We show that these two systems have a similar layer bias for axonal fiber innervation and receptor distribution. The common target sites are the geniculorecipient layers and geniculocortical fibers, where the appropriate gain control is established through a geniculocortical signal transformation. Both systems exert activity-dependent response gain control across layers, but in a manner consistent with the receptor subtype. The serotonergic receptors 5-HT1B and 5HT2A modulate the contrast-response curve in a manner consistent with bi-directional response gain control, where the sign (facilitation/suppression) is switched according to the firing rate and is complementary to the other. On the other hand, cholinergic nicotinic/muscarinic receptors exert mono-directional response gain control without a sign reversal. Nicotinic receptors increase the response magnitude in a multiplicative manner, while muscarinic receptors exert both suppressive and facilitative effects. We discuss the implications of the two neuromodulator systems in hierarchical visual signal processing in V1 on the basis of the developed laminar structure.

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“…5HTR2 The action of the receptor 5HTR2 can be formulated in a much simpler way: it adds a certain gain to the processing in a cortical neuron which can be seen as a multiplicative term which then scales Eq. 1 and reflects the model by Carhart-Harris and Nutt (2017) and the findings by Shimegi et al (2016). It can be seen in Fig.…”

“…While 5HTR1 is inhibitory, 5HTR2 is excitatory. Recent findings point to a more sophisticated role of these receptors when investigating response curves of cortical processing as done in the visual cortex (Shimegi et al, 2016;Seillier et al, 2017) and we propose that 5HT alters the signal processing in the mPFC in a similar way.…”

“…The argument is that they enhance cortical processing by boosting activity in the cortex and activating 5HTR2 receptors. However, this might not always be desirable, in particular in tasks which require patience due to the fact that the activation of 5HTR2 receptors increase the gain of cortical processing (Shimegi et al, 2016). This might lead to more rewards because of more (random) activity but won't provide measured goal directed behaviour.…”

“…5HTR1 Based on Shimegi et al (2016) we model the action of the receptor 5HTR1 as a parameter in a psychometric function which slowly saturates towards one:…”

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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).…”