Dataset Information

Rapid event-related, BOLD fMRI, non-human primates (NHP): choose two out of three.

ABSTRACT: Human functional magnetic resonance imaging (fMRI) typically employs the blood-oxygen-level-dependent (BOLD) contrast mechanism. In non-human primates (NHP), contrast enhancement is possible using monocrystalline iron-oxide nanoparticles (MION) contrast agent, which has a more temporally extended response function. However, using BOLD fMRI in NHP is desirable for interspecies comparison, and the BOLD signal's faster response function promises to be beneficial for rapid event-related (rER) designs. Here, we used rER BOLD fMRI in macaque monkeys while viewing real-world images, and found visual responses and category selectivity consistent with previous studies. However, activity estimates were very noisy, suggesting that the lower contrast-to-noise ratio of BOLD, suboptimal behavioural performance, and motion artefacts, in combination, render rER BOLD fMRI challenging in NHP. Previous studies have shown that rER fMRI is possible in macaques with MION, despite MION's prolonged response function. To understand this, we conducted simulations of the BOLD and MION response during rER, and found that no matter how fast the design, the greater amplitude of the MION response outweighs the contrast loss caused by greater temporal smoothing. We conclude that although any two of the three elements (rER, BOLD, NHP) have been shown to work well, the combination of all three is particularly challenging.

SUBMITTER: Pelekanos V

PROVIDER: S-EPMC7198564 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Rapid event-related, BOLD fMRI, non-human primates (NHP): choose two out of three.

Pelekanos Vassilis V Mok Robert M RM Joly Olivier O Ainsworth Matthew M Kyriazis Diana D Kelly Maria G MG Bell Andrew H AH Kriegeskorte Nikolaus N

Scientific reports 20200504 1

Human functional magnetic resonance imaging (fMRI) typically employs the blood-oxygen-level-dependent (BOLD) contrast mechanism. In non-human primates (NHP), contrast enhancement is possible using monocrystalline iron-oxide nanoparticles (MION) contrast agent, which has a more temporally extended response function. However, using BOLD fMRI in NHP is desirable for interspecies comparison, and the BOLD signal's faster response function promises to be beneficial for rapid event-related (rER) design ...[more]

PMID: 32366956

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Project description:BACKGROUND:Approximately 20% of the adult population suffer from chronic pain that is not adequately treated by current therapies, highlighting a great need for improved treatment options. To develop effective analgesics, experimental human and animal models of pain are critical. Topically/intra-dermally applied capsaicin induces hyperalgesia and allodynia to thermal and tactile stimuli that mimics chronic pain and is a useful translation from preclinical research to clinical investigation. Many behavioral and self-report studies of pain have exploited the use of the capsaicin pain model, but objective biomarker correlates of the capsaicin augmented nociceptive response in nonhuman primates remains to be explored. METHODOLOGY:Here we establish an aversive capsaicin-induced fMRI model using non-noxious heat stimuli in Cynomolgus monkeys (n = 8). BOLD fMRI data were collected during thermal challenge (ON:20 s/42°C; OFF:40 s/35°C, 4-cycle) at baseline and 30 min post-capsaicin (0.1 mg, topical, forearm) application. Tail withdrawal behavioral studies were also conducted in the same animals using 42°C or 48°C water bath pre- and post- capsaicin application (0.1 mg, subcutaneous, tail). PRINCIPAL FINDINGS:Group comparisons between pre- and post-capsaicin application revealed significant BOLD signal increases in brain regions associated with the 'pain matrix', including somatosensory, frontal, and cingulate cortices, as well as the cerebellum (paired t-test, p<0.02, n = 8), while no significant change was found after the vehicle application. The tail withdrawal behavioral study demonstrated a significant main effect of temperature and a trend towards capsaicin induced reduction of latency at both temperatures. CONCLUSIONS:These findings provide insights into the specific brain regions involved with aversive, 'pain-like', responses in a nonhuman primate model. Future studies may employ both behavioral and fMRI measures as translational biomarkers to gain deeper understanding of pain processing and evaluate the preclinical efficacy of novel analgesics.

Project description:Functional magnetic resonance imaging (fMRI) has revolutionized human brain research. But there exists a fundamental mismatch between the rapid time course of neural events and the sluggish nature of the fMRI blood oxygen level-dependent (BOLD) signal, which presents special challenges for cognitive neuroscience research. This limitation in the temporal resolution of fMRI puts constraints on the information about brain function that can be obtained with fMRI and also presents methodological challenges. Most notably, when using fMRI to measure neural events occurring closely in time, the BOLD signals may temporally overlap one another. This overlap problem may be exacerbated in complex experimental paradigms (stimuli and tasks) that are designed to manipulate and isolate specific cognitive-neural processes involved in perception, cognition, and action. Optimization strategies to deconvolve overlapping BOLD signals have proven effective in providing separate estimates of BOLD signals from temporally overlapping brain activity, but there remains reduced efficacy of such approaches in many cases. For example, when stimulus events necessarily follow a non-random order, like in trial-by-trial cued attention or working memory paradigms. Our goal is to provide guidance to improve the efficiency with which the underlying responses evoked by one event type can be detected, estimated, and distinguished from other events in designs common in cognitive neuroscience research. We pursue this goal using simulations that model the nonlinear and transient properties of fMRI signals, and which use more realistic models of noise. Our simulations manipulated: (i) Inter-Stimulus-Interval (ISI), (ii) proportion of so-called null events, and (iii) nonlinearities in the BOLD signal due to both cognitive and design parameters. We offer a theoretical framework along with a python toolbox called deconvolve to provide guidance on the optimal design parameters that will be of particular utility when using non-random, alternating event sequences in experimental designs. In addition, though, we also highlight the challenges and limitations in simultaneously optimizing both detection and estimation efficiency of BOLD signals in these common, but complex, cognitive neuroscience designs.

Dataset Information

Rapid event-related, BOLD fMRI, non-human primates (NHP): choose two out of three.

Publications

Rapid event-related, BOLD fMRI, non-human primates (NHP): choose two out of three.

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