Frequency- and State-Dependent Network Effects of Electrical Stimulation Targeting the Ventral Tegmental Area in Macaques

Murris, Sjoerd R; Arsenault, John; Vanduffel, Wim

doi:10.1093/cercor/bhaa007

Cited by 27 publications

(45 citation statements)

References 58 publications

(105 reference statements)

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“…However, it is also possible that our imaging methods limited the ability to detect contralateral activations. Indeed, other studies have shown some contralateral activations induced by EM, consistent with anatomical connections across hemispheres (Ekstrom et al, 2008;Moeller et al, 2008;Premereur et al, 2015;Murris et al, 2020). As expected for the EM of striatal regions, the activated areas were known constituents of the basal ganglia circuit (Draganski et al, 2008;Haber & Knutson, 2010).…”

Section: Performance Of the Microdrive During Em-coupled Mri Scanningsupporting

confidence: 78%

MRI Compatible, Customizable, and 3D-Printable Microdrive for Neuroscience Research

Baeg

Doudlah

Swader

et al. 2021

eNeuro

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The effective connectivity of brain networks can be assessed using functional magnetic resonance imaging (fMRI) to quantify the effects of local electrical microstimulation (EM) on distributed neuronal activity. The delivery of EM to specific brain regions, particularly with layer specificity, requires MRI compatible equipment that provides fine control of a stimulating electrode's position within the brain while minimizing imaging artifacts. To this end, we developed a microdrive made entirely of MRI compatible materials. The microdrive uses an integrated penetration grid to guide electrodes and relies on a micro-drilling technique to eliminate the need for large craniotomies, further reducing implant maintenance and image distortions. The penetration grid additionally serves as a built-in MRI marker, providing a visible fiducial reference for estimating probe trajectories. Following the initial implant procedure, these features allow for multiple electrodes to be inserted, removed, and repositioned with minimal effort, using a screw-type actuator. To validate the design of the microdrive, we conducted an EM-coupled fMRI study with a male macaque monkey. The results verified that the microdrive can be used to deliver EM during MRI procedures with minimal imaging artifacts, even within a 7 Tesla (7T) environment. Future applications of the microdrive include neuronal recordings and targeted drug delivery. We provide computer aided design (CAD) templates and a parts list for modifying and fabricating the microdrive for specific research needs. These designs provide a convenient, cost-effective approach to fabricating MRI compatible microdrives for neuroscience research.

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Section: Performance Of the Microdrive During Em-coupled Mri Scanningsupporting

confidence: 78%

MRI Compatible, Customizable, and 3D-Printable Microdrive for Neuroscience Research

Baeg

Doudlah

Swader

et al. 2021

eNeuro

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show abstract

“…Particularly, the strength of stimulation effects is modulated by the brain state (e.g. anaesthetized vs. awake) (Murris et al, 2020), the properties of the employed visual stimuli such as contrast or the visual responsiveness of activated voxels (Ekstrom et al, 2009(Ekstrom et al, , 2008 and task demands (Premereur et al, 2013). The first goal of this study was to identify the shared functional circuitry of dPul and LIP during oculomotor tasks.…”

Section: Highlightsmentioning

confidence: 99%

Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP

Kagan

Gibson

Spanou

et al. 2020

Preprint

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The thalamic pulvinar and the lateral intraparietal area (LIP) share reciprocal anatomical connections and are part of an extensive cortical and subcortical network involved in spatial attention and oculomotor processing. The goal of this study was to compare the effective connectivity of dorsal pulvinar (dPul) and LIP and to probe the dependency of microstimulation effects on task demands and spatial tuning properties of a given brain region. To this end, we applied unilateral electrical microstimulation in the dPul and LIP in combination with event-related BOLD fMRI in monkeys performing fixation and memory-guided saccade tasks. Microstimulation in both dPul and LIP enhanced task-related activity in monosynaptically-connected prefrontal cortex and along the superior temporal sulcus (STS) as well as in extrastriate cortex. Both dPul and LIP stimulation also elicited activity in several cortical areas in the opposite hemisphere, implying polysynaptic propagation of excitation. LIP microstimulation elicited strong activity in the opposite homotopic LIP while no homotopic activation was found during dPul stimulation. Despite extensive activation along the intraparietal sulcus evoked by LIP stimulation, there was a difference in frontal and occipital connectivity elicited by posterior and anterior LIP stimulation sites. Comparison of dPul stimulation with the adjacent but functionally distinct ventral pulvinar also showed distinct connectivity. On the level of single trial timecourses within a region, most microstimulation regions did not show task-dependence of stimulation-elicited response modulation. Across regions, however, there was an interaction between the task and the stimulation, and task-specific correlations between the initial spatial selectivity and the magnitude of stimulation effect were observed. Consequently, stimulation-elicited modulation of task-related activity was best fitted by an additive model scaled down by the initial response amplitude. In summary, we identified overlapping and distinct patterns of thalamocortical and corticocortical connectivity of the two key visuospatial areas, highlighting the dorsal bank and fundus of STS as a prominent node of shared circuitry. Spatial task-specific and partly polysynaptic modulations of cue and saccade planning delay period activity in both hemispheres exerted by unilateral pulvinar and parietal stimulation provide insight into the distributed interhemispheric processing underlying spatial behavior.HighlightsElectrical stimulation of pulvinar and LIP was used to study fMRI effective connectivityBoth regions activated prefrontal cortex and the dorsal bank of superior temporal sulcusActivations within and across hemispheres suggest polysynaptic propagationStimulation effects show interactions between task- and spatial selectivityStimulation effects are best fitted by an additive model scaled by the initial response

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“…An inverted-U relationship between dopamine and distributed working memory activity Previous experimental and modelling studies have shown an inverted-U relationship between D1 receptor stimulation and persistent activity in the prefrontal cortex in monkeys performing working memory tasks (Brunel and Wang 2001;Vijayraghavan et al 2007;Wang et al 2019). Stimulation of VTA (presumably leading to cortical dopamine release) in resting monkeys also has an inverted-U effect on cortical activity in distributed areas across cortex (Murris et al 2020).…”

Section: A Gradient Of D1 Receptors Along the Cortical Hierarchymentioning

confidence: 98%

A dopamine gradient controls access to distributed working memory in monkey cortex

Bliss

Ding

Jankovic-Rapan

et al. 2020

Preprint

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SummaryDopamine is critical for working memory. However, its effects throughout the large-scale primate cortex are poorly understood. Here we report that dopamine receptor density per neuron, measured by receptor autoradiography in the macaque monkey cortex, displays a macroscopic gradient along the cortical hierarchy. We developed a connectome- and biophysically-based model for distributed working memory that incorporates multiple neuron types and a dopamine gradient. The model captures an inverted U-shaped dependence of working memory on dopamine. The spatial distribution of mnemonic persistent activity matches that observed in over 90 experimental studies. We show that dopamine filters out irrelevant stimuli by enhancing inhibition of pyramidal cell dendrites. The level of cortical dopamine can also determine whether memory encoding is through persistent activity or an internal synaptic state. Taken together, our work represents a cross-level understanding that links molecules, cell types, recurrent circuit dynamics and a core cognitive function distributed across the cortex.

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Frequency- and State-Dependent Network Effects of Electrical Stimulation Targeting the Ventral Tegmental Area in Macaques

Cited by 27 publications

References 58 publications

MRI Compatible, Customizable, and 3D-Printable Microdrive for Neuroscience Research

MRI Compatible, Customizable, and 3D-Printable Microdrive for Neuroscience Research

Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP

A dopamine gradient controls access to distributed working memory in monkey cortex

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