BOLD responses to different temporal frequency stimuli in the lateral geniculate nucleus and visual cortex: Insights into the neural basis of fMRI

Abstract

The neural basis of the blood oxygenation level dependent (BOLD) functional magnetic resonance imaging (fMRI) remains largely unknown after decades of research. To investigate this issue, the unique property of the temporal frequency tuning that could separate neural input and output in the primary visual cortex was used as a model. During moving grating stimuli of 1, 2, 10 and 20 Hz temporal frequencies, we measured 9.4-T BOLD fMRI responses simultaneously in the primary visual cortex of area 17 (A17) and area 18 (A18), and the lateral geniculate nucleus (LGN) of isoflurane-anesthetized cat. Our results showed preferred temporal frequencies of the BOLD responses for A17, A18 and LGN were 3.1 Hz, 4.5 Hz and 6.0 Hz, respectively, which were comparable to the previously reported electrophysiological data. Additionally, the difference of BOLD response onset time between LGN and A17 was 0.5 s, which is 18 times larger than the difference of neural activity onset time between these areas. We then compared the frequency-dependent BOLD fMRI response of A17 with tissue partial pressure of oxygen (pO2) and electrophysiological data of the same animal model reported by Viswanathan and Freeman (Nature Neuroscience, 2007). The BOLD tuning curve resembled the low frequency band (<12 Hz) of local field potential (LFP) tuning curve rather than spiking activity, gamma band (25–90 Hz) of LFP, and tissue pO2 tuning curves, suggesting that the BOLD fMRI signal relates closer to low frequency LFP.

Noise and non-neuronal contributions to the BOLD signal: applications to and insights from animal studies

“…The lack of local energy stores in the brain requires that the vasculature respond dynamically to changes in neuronal activity, and it appears that this neurovascular coupling is also relatively conserved across species, although the timing and shape of the hemodynamic response vary (de Zwart et al, 2005). As expected based on these similarities, fMRI studies in cats, rodents, and monkeys have demonstrated patterns of activation in response to sensory stimuli similar to those detected in humans (Aksenov et al, 2015; Huang et al, 1996; Keilholz et al, 2004; Kim and Uğurbil, 1997; Lee et al, 1999; Logothetis et al, 2001; Schroeter et al, 2014; Yang et al, 1996; Yen et al, 2011). Likewise, using rs-fMRI researchers have shown that numerous networks (including somatosensory, motor, visual, and even “default mode”) are present across species (Belcher et al, 2016, 2013; Ghahremani et al, 2016; Lu et al, 2012; Mantini et al, 2011; Pawela et al, 2008; Schroeder et al, 2016; Vincent et al, 2007; Williams et al, 2010; Zhao et al, 2008).…”

“…Their brains are small and unconvoluted, and their controlled genetic backgrounds result in high similarity across individual animals. Cats have more complex brains and a visual system that more closely approximates that of a human, and are widely used in visual studies (Moon et al, 2013; Yen et al, 2011). Nonhuman primates have the most complex brains and are the most costly to work with, but provide the closest approximation to the human brain and have provided key insights into the neurophysiology underlying the BOLD response (Hutchison and Everling, 2012; J.…”

Neural Circuit Modulation During Deep Brain Stimulation at the Subthalamic Nucleus for Parkinson's Disease: What Have We Learned from Neuroimaging Studies?

“…Thus, non-neuronal contributions to effects reported in these studies cannot be ruled out. Related to this point, when compared with multi-unit recordings or LFPs, the BOLD signal detected in fMRI is more greatly correlated with LFPs, reflecting a potential bias in fMRI for the detection of input activity rather than local cell spiking (Goense and Logothetis, 2008;Lippert et al, 2010;Logothetis et al, 2001;Yen et al, 2011). Although this relationship may not hold true at high spatial resolution (Kahn et al, 2013;Shih et al, 2013), it is worth noting that low-frequency LFP oscillations (1-1.5 Hz) may be increased during STN-DBS (Priori et al, 2006), with possible relevance for the activation profile detected with BOLD fMRI.…”

Study of the Spatial Correlation Between Neuronal Activity and BOLD fMRI Responses Evoked by Sensory and Channelrhodopsin-2 Stimulation in the Rat Somatosensory Cortex

“…Similar to other hemodynamics-based functional brain imaging techniques, the blood oxygenation level dependent (BOLD) fMRI signal is an indirect measurement of the neuronal activity. The exact relationship between the neuronal responses and hemodynamic responses remain unclear and under debates (Attwell et al 2002; Logothetis 2008; Vanzetta et al 2008; Enager et al 2009; van Eijsden et al 2009; Ekstrom 2010; Yen et al 2011). Indeed, in recent years there have been great efforts to resolve this controversial topic.…”