Guide Monoaminergic Modulation of Cortical Excitability

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One important consideration in the assessment of DCMs is that the modeled effects represent effective as opposed to axonal connectivity. That is, although one usually strives to constrain to anatomically plausible connections, DCM does not rely on a direct axonal connection between 2 regions. Rather, the observed functional effects may also be mediated by implicitly captured relays Friston et al.

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Interactions in cortical networks underlying behavioral performance are ultimately driven by the interplay of neurotransmitters with their specific receptors Loubinoux, Pariente, Rascol, et al. However, the effects exerted upon the neural architecture by pharmacological stimulation most likely differ between the different receptor systems and the task under investigation. For example, there is growing evidence that stimulating the human NA system with RBX does not affect performance in simple motor tasks resembling the hand clenching task of the present study Plewnia et al.

Loubinoux et al. These use-dependent effects are associated with an increase of BOLD response in contralateral sensorimotor areas Loubinoux, Pariente, Boulanouar, et al. The neurotransmitter system that has been frequently associated with influencing alertness and attention is the noradrenergic system Posner and Petersen The most important source for cortical NA is the locus ceruleus LC in the pontine brainstem which widely projects to the spinal cord, thalamus, and cortex Berridge and Waterhouse ; Logan et al. Such effects may well result from increased extracellular NA acting at alpha-2 autoreceptors on LC neurons Berridge and Abercrombie ; Wong et al.

However, the question remains why enhancing noradrenergic transmission selectively improves visuomotor network functions given the broad distribution of norepinephrine fibers and the presumably system wide action of RBX on NA release. Studies in rats showed that low-dose administration of the NA reuptake inhibitor methylphenidate may differentially enhance NA transmission in prefrontal cortex compared with other cortical regions Berridge et al.

This gradient of efficacy of RBX to raise NA levels may explain differences in connectivity changes between more frontal cortical regions and those more posterior. The cellular mechanisms underlying such regionally specific effects are likely to comprise differences in the distribution of adrenergic receptor subtypes alpha-1, alpha-2, beta-receptors , in the respective receptor sensitivity for NA binding, and in the local modulation of NA release Bonanno et al.

Similar mechanisms may also underlie the regionally specific changes in BOLD signal and connectivity observed as a result of RBX stimulation. The findings that 1 neural changes were not correlated with RBX plasma concentrations and 2 RBX effects were absent in the visuomotor control task suggest that rather other, more indirect mechanisms e. For example, data derived from studies in macaques suggest that changes in the phasic discharge of LC neurons during target detection may enhance the gain of neural responses in sensorimotor regions, thereby speeding up behavioral responses Aston-Jones and Cohen b.

Electrophysiological studies imply that an appropriate state of arousal might facilitate the task-related phasic discharge of the LC Aston-Jones et al. Studies in rats showed that both frequency and pattern of LC discharge may determine NA release in cortical regions such as the prefrontal or parietal cortex Florin-Lechner et al. Also within the same region, stimulation of the LC or application of NA can differentially modulate the responsiveness of neighboring neurons responding to the same peripheral stimulus Devilbiss et al.

The effects of RBX on extracellular levels of norepinephrine might also depend upon the impulse activity of the LC. This activity may change according to the behavioral state as might occur under conditions of higher LC output, for example, during the challenges of the joystick task opposed to the less demanding fist closure task. However, the behavioral data did not show significant differences in reaction times when subjects were stimulated with RBX. Hence, RBX might not have facilitated stimulus detection but rather the neural mechanisms subserving the control of guiding the cursor into the target circle as suggested by the faster movements under RBX.

Electrophysiological studies in rodents showed that enhancing NA transmission has divergent effects on neurons found in different cortical layers, thereby modulating stimulus feature coding and signal-to-noise ratio Hurley et al. For example, in visual cortex, enhancing NA may increase the signal-to-noise ratio measured as spike train activity by decreasing spontaneous activity Hasselmo et al. Furthermore, global enhancement of NA transmission by systemic administration of a NA reuptake blocker might have facilitated the gating of neural information, that is, the increase in the responsiveness of neurons to otherwise subthreshold stimuli Devilbiss and Waterhouse Accordingly, the better use of sensory visual, proprioceptive feedback information during movement execution due to RBX-induced neural gating might have speeded up the joystick movements in the present study.

Although RBX may have induced a system-wide increase in NA levels, neuronal processing might have been especially facilitated in those regions contributing to the actual task. Consistent with this view, the imaging data point to a modulation of areas known to be involved in visuospatial attention and online control of hand movements. Also the connectivity analysis implies that neural gating mechanisms might play a crucial role for the RBX effects observed in the present study, for example, by enhancing the functional interactions among areas in the right hemisphere.

Such a hypothesis is in line with a recent study in rats demonstrating that overall functional connectivity among ensembles of neurons may be enhanced with increasing LC output and NA efflux Devilbiss et al. The connectivity analysis suggested a preferred flow of neural information from V1 over IPS to premotor and motor areas Figs 5 and 6 , which is in good accordance with data derived from studies in nonhuman primates Rizzolatti et al.

The IPS is, however, not only engaged in visual attention Nobre et al. Our results suggest that the stronger implementation of right frontoparietal areas into the visuomotor network subserving the joystick movements may have reduced the computational load posed onto the left hemisphere. In macaques, medial intraparietal cortex area MIP is engaged in planning and execution of reaching movements Colby , and is strongly connected to the dorsal premotor cortex Rizzolatti et al. Medial IPS is supposed to transform sensory e. Therefore, stronger activation of intraparietal cortex mediated by RBX stimulation might reflect enhanced engagement of transformation processes facilitating the integration of visual information into planned motor programs i.

Although it is tempting to conclude that the critical neural correlate for improved task performance is the human homologue of area MIP, we cannot make such a clear anatomical statement as also the human homologue of the LIP area is found on medial IPS in humans Koyama et al.

This area is involved in the transformation of visuo- spatial coordinates in saccadic eye movements Andersen ; Snyder et al. In a more conceptual framework, the FEF is thought to transform visual signals into motor commands i. However, cell recordings in macaques demonstrated that more than half of FEF neurons can be modulated by hand position signals Boussaoud et al.

Although we cannot exclude that changes in eye movements might have played a role for the BOLD signal increases observed under RBX stimulation, the strong lateralization of activity to the right hemisphere and the asymmetric changes in interhemispheric connectivity speak against a purely saccade related effect: Both saccades and also the suppression of eye movements typically show strong bilateral activations of the frontal eye fields Paus ; Corbetta et al. Furthermore, the faster joystick movements under RBX were not associated with faster reaction times in starting the joystick movements after target onset.

Hence, although we cannot rule out differences in eye movements between the RBX and PBO session, the missing effects on reaction times imply that target selection and control of saccades might not have played a dominant role for the neural effects observed. Such a view is consistent with data showing that also human oculomotor areas in IPS and FEF are involved in pointing preparation and execution Simon et al. It remains, therefore, difficult to separate the specific contributions of different attentional mechanisms to the joystick task. Andersen and Buneo also emphasize the extremely similar coding strategies of the reaching and saccade related areas in IPS suggesting that both regions MIP, LIP are parts of a single network for the purpose of coordinating hand and eye movements, and which might both have been activated by the current experiment.

The present study shows that improvements in visuomotor performance following noradrenergic stimulation with RBX underlie not only changes in regional activity but also complex network effects affecting both neural processing within and across the hemispheres. We, therefore, conclude that motor improvements under noradrenergic stimulation Evans et al.

Such a view is compatible with data from animal experiments showing that stimulation of the LC—NA system may change functional connectivity among selective ensembles of neurons, thereby maximizing information processing capabilities of cerebral networks Devilbiss et al. Modulation of connectivity among cellular assemblies might also account for the beneficial effects of NA enhancing drugs in pathological conditions, for example, after a stroke Zittel et al.

As stroke patients may show profound changes in the effective connectivity among motor areas across both hemispheres Grefkes et al. Analyses of effective connectivity e.

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We thank Dr Manuel Dafotakis for his medical support. We are grateful to the M. Conflict of Interest : None declared. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide.

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Volume Article Contents. Material and Methods. Oxford Academic. Google Scholar. Ling E. Simon B. Gereon R. Cite Citation. Permissions Icon Permissions. Abstract Both animal and human data suggest that stimulation of the noradrenergic system may influence neuronal excitability in regions engaged in sensory processing and visuospatial attention.

Open in new tab Download slide. A key focus of the present study was to investigate whether and—if so—how RBX stimulation of the noradrenergic system modulates the interregional coupling of areas involved in visuomotor control. Such changes in interregional coupling may occur independently from the actual task or might be linked to a specific condition e. DCM Friston et al.

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DCM treats the brain as a nonlinear deterministic system in which external inputs cause changes in neural activity that in turn lead to changes in the fMRI signal Friston et al. As this approach explicitly models neuronal activity, which is then linked via a biophysically validated hemodynamic model Friston et al.

The changes in neuronal states over time are modeled as. Table 1. Open in new tab. Table 2. Table 3. Encoding of intention and spatial location in the posterior parietal cortex. Search ADS. Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing.

The locus coeruleus: behavioral functions of locus coeruleus derived from cellular attributes. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance.

Relationship between locus coeruleus discharge rates and rates of norepinephrine release within neocortex assess by in vivo microdialysis. Methylphenidate preferentially increases catecolamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Presynaptic mechanisms underlying the gamma-aminobutyric acid-evoked receptor-independent release of [3H]norepinephrine in rat hippocampus. Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey.

Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study. Primate frontal eye fields. Single neurons discharging before saccades. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. Phasic activation of monkey locus ceruleus neurons by simple decisions in a forced-choice task.

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