Octopus visual system: A functional MRI model for detecting neuronal electric currents without a blood‐oxygen‐level‐dependent confound

Abstract

Purpose Despite the efforts that have been devoted to detecting the transient magnetic fields generated by neuronal firing, the conclusion that a functionally relevant signal can be measured with magnetic resonance imaging (MRI) is still controversial. For human studies of neuronal current MRI (nc-MRI), the blood-oxygen-level-dependent (BOLD) effect remains an irresolvable confound. For tissue studies where hemoglobin is removed, natural sensory stimulation is not possible. This study investigates the feasibility of detecting a physiologically induced nc-MRI signal in vivo in a BOLD-free environment. Methods The cephalopod mollusc Octopus bimaculoides has vertebrate-like eyes, large optic lobes (OLs) and blood that does not contain hemoglobin. Visually evoked potentials were measured in the octopus retina and OL by electroretinogram and local field potential. nc-MRI scans were conducted at 9.4 Tesla to capture these activities. Results Electrophysiological recording detected strong responses in the retina and OL in vivo; however, nc-MRI failed to demonstrate any statistically significant signal change with a detection threshold of 0.2° for phase and 0.2% for magnitude. Experiments in a dissected eye-OL preparation yielded similar results. Conclusion These findings in a large hemoglobin-free nervous system suggest that sensory evoked neuronal magnetic fields are too weak for direct detection with current MRI technology.

Direct detection of neural activity in vitro using magnetic resonance electrical impedance tomography (MREIT)

“…While no previous experiments on MREIT detection of neural activity have been published, there are several published experimental ncMRI studies (Huang, 2014; Huang and Zhu, 2015; Jiang et al, 2014; Luo et al, 2009; Park et al, 2006; Petridou et al, 2006). Petridou et al (Petridou et al, 2006) reported significant differences in spectroscopic images caused by administration of TTX to cultured tissue.…”

“…Many methods have sought to directly image neural activity in vivo using magnetic resonance methods. These include the area of neural current magnetic resonance imaging (ncMRI), where disturbances in the main magnetic field of an MR system caused by intrinsic neural currents have been observed to produce artifacts in magnitude or phase images (Bandettini et al, 2005; Huang, 2014; Huang and Zhu, 2015; Jiang et al, 2014; Luo and Gao, 2009; Park et al, 2006; Petridou et al, 2006; Sundaram et al, 2016). More recently, attempts have been made to detect the effects of ion flow using Lorentz force imaging (Pourtaheri et al, 2013; Truong et al, 2008) and Mg enhanced MR imaging (Radecki et al, 2014).…”

“…In a final phase of each experiment, performed approximately 19 hours after the sample was placed in the machine, the same image set was acquired from the ganglion remains (DEAD). Within each phase of each experiment, data were also gathered from ganglia with no injected current (NC), providing an opportunity to qualitatively compare findings with those in ncMRI studies (Huang, 2014; Huang and Zhu, 2015; Jiang et al, 2014; Luo et al, 2009). …”

Digital Three-Dimensional Imaging Techniques Provide New Analytical Pathways for Malacological Research

“…Several studies on molluscan specimens have so far been conducted using preclinical MRI, including analyses of the single-cell and sub-cellular composition of neurons from derived taxa (Hsu et al 1996, Grant et al 2000, Gozansky et al 2003, Lee et al 2015, physiological capacities of cephalopods and bivalves measured in vivo (Bock et al 2004, Melzner et al 2006, Melzner et al 2007, Lannig et al 2008, Gutowska et al 2010, Lee et al 2010, Seo et al 2014, Sukhotin et al 2017, reproductive organ maturation and sex determination in oysters (Davenel et al 2006, Davenel et al 2010, Smith and Reddy 2012, or visual system anatomy in cephalopods (Jiang et al 2013, Chung and Marshall 2014, Chung and Marshall 2017, Liu et al 2017, Liu et al 2018. In addition, preclinical MRI was applied to study the anatomy of a cobalt-labeled cephalopod brain (Quast et al 2001), to conduct analyses of pathological alterations in belemnites (Mietchen et al 2005, Mietchen et al 2008 and to study the internal anatomy of a gastropod .…”

Neuroethology of the visual communication in the mourning cuttlefish Sepia plangon

“…These investigations used conventional histological methods, such as Golgi and Cajal staining to analyse brain morphology. Recent studies are implementing modern methods to analyse cephalopods brain anatomy and function; for instance, Computational Tomography (CT) [Grimaldi et al, 2007, Kerbl et al, 2013, Magnetic Resonance Imaging (MRI) [Chung and Marshall, 2014,Jiang et al, 2014, Chung et al, 2020 and Calcium Imaging [Koizumi et al, 2018].…”