BOLD responses in the superior colliculus and lateral geniculate nucleus of the rat viewing an apparent motion stimulus
Research highlights
► Responses were measured in the SC at all stimulus speeds tested (7 to 164°/s). ► The SC response during 164°/s was significantly lower than during slower stimuli. ► The findings are in agreement with previous electrophysiology findings in rats.
Introduction
In rats, light emanating from external objects is focused by the cornea and lens onto the retina. Photosensitive cells in the retina project axons carrying information about the light. The axons from both eyes come together to form the optic nerves, which transmit information from the retina to the brain. The majority of these nerve fibers, 90–95% in rats (Polyak, 1957), cross the midline to the opposite side of the brain. From there, fibers are known to project to the ventral and dorsal lateral geniculate nuclei (vLGN and dLGN), lateral posterior nucleus, pretectum, and superior colliculus (SC) (Sefton et al., 2004). The majority of retinal axons project to the superficial layers of the superior colliculus located in the dorsal midbrain. It is involved in numerous functions related to responding to visual stimuli, including orienting the body to the stimulus (Sahibzada et al., 1986), guiding spatial movement using visual information (Cooper et al., 1998), controlling eye movements (McHaffie and Stein, 1982), and initiating defensive reactions (King, 1999, Vargas et al., 2000). Individual neurons of the SC are known to be highly sensitive to visual stimuli moving in their receptive fields (Stein, 1981).
To date, most studies of the SC's motion dependence have been conducted with invasive and/or small field of view techniques such as electrical recordings. These studies have examined the motion response of SC cells in multiple species, including rodents, and observed that the highest number of impulses was recorded for slow moving stimuli (Stein, 1981). For example, Humphrey et al. observed that the SC cells of hooded rats responded to small dark objects moving across their receptive fields (Humphrey, 1968). Binns et al. presented moving bars to hooded rats and recorded increased neuronal impulse rate (Binns and Salt, 1997). In rats, the direction of motion does not appear to be a significant factor. Multiple studies have observed that the majority of SC cells (> 85%) do not respond selectively to any specific direction in the visual field (Fukuda and Iwama, 1978, Humphrey, 1968, Prevost et al., 2007).
Blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) is a non-invasive technique that can simultaneously examine a large field of view with high spatial resolution (Ogawa et al., 1990). However, few fMRI studies have been conducted on the human SC because of technical challenges, such as its small size, deep position near the brainstem, and proximity to pulsating flow artifacts (DuBois and Cohen, 2000, Himmelbach et al., 2007, Wall et al., 2009). The rat SC occupies a significantly larger portion of the brain and is located closer to the skull. It also receives a greater fraction of retinal projections (compared to the primate SC) (Linden and Perry, 1982, Linden and Perry, 1983, Perry and Cowey, 1984). Considering these technical and possible biological advantages, we choose the rat as a mammalian model for functional imaging studies of the SC responding to moving visual stimuli. Note lower order animals such as fish have been used extensively to study the optic tectum (Nevin et al., 2010). The tectum is usually referred to as the SC in mammalian species. BOLD fMRI can expand our understanding of the SC's motion response because it examines the entire structure, along with nearby visual centers such as the LGN and visual cortex, simultaneously with high spatial resolution. A recent human fMRI study examined the SC and LGN's BOLD responses during a slow moving (7°/s) visual stimulus (Schneider and Kastner, 2005) and observed signal change greater than 1%. In another study, Wall et al. observed BOLD responses in SC, LGN, and primary visual cortex during a slightly faster 12°/s stimulus (Wall et al., 2009). However, neither group of authors examined responses at different stimulus speeds and human subjects may not be optimal for SC functional imaging studies due to the aforementioned technical challenges.
In this study, we apply BOLD fMRI on albino Sprague Dawley (SD) rats responding to four small, stationary light spots switched on and off sequentially to mimic motion. The on–off rate is varied to produce different effective stimulus speeds. This setup is similar to those used in long-range apparent motion studies using animals (Ahmed et al., 2008). The speed response functions (hemodynamic response amplitude at different stimulus speeds) are measured in the SC and neighboring lateral geniculate nucleus (LGN). This work represents the first fMRI study of stimulus speed dependence in the SC.
Section snippets
Animal preparation
All aspects of this study were approved by the Committee on the Use of Live Animals in Teaching and Research (CULATR) of the University of Hong Kong (CULATR Number: 2041–09). Eight male SD rats weighing between 250 and 300 g were used in this study. Each animal was anesthetized with 4% isofluorane (mixed with room air) for 5 minutes in a plastic anesthetizing box (Harvard Apparatus, Holliston, MA). Controlled dosages were provided by an isofluorane vaporizer (ISOTEC 4, SurgiVet, Waukesha, WI).
Results
Fig. 2 shows the response map measured from a representative animal with responsive voxels defined by r > 0.41, which corresponds to an approximately p < 0.001 probability of false response (Bandettini et al., 1993). The underlying fMRI images span the four scan slices in Fig. 1A and five stimulus speeds. Significant SC responses in both hemispheres can be observed at all speeds in slices 1–3, although the higher r value voxels are mostly in the right hemisphere. The highest r voxels also appear to
Discussion
This study applies BOLD fMRI to measure the hemodynamic response in the rat brain, particularly in the superior colliculus, during travelling light spot stimulation moving at different speeds. Significant portions of the SC and LGN respond at all speeds. For the SC, the speed response function (SRF) increases monotonically from 7 to 82°/s before a large decrease at 164°/s. The SC BOLD response during moving stimulation is prominent at low speeds, but reduced at higher speeds. In the LGN, the
Conclusion
This study applied BOLD fMRI to measure the hemodynamic responses in the rat SC and LGN to four small light spots turned on and off sequentially to mimic motion at different effective speeds. The SC speed response function showed non-zero BOLD signals at all speeds tested. The response amplitude was statistically significantly lower during 164°/s stimulation compared to during slower speeds. In the LGN, the speed response function exhibited a similar trend to the SC, but response amplitude
Acknowledgments
This project was supported by the Hong Kong Research Grants Council (GRF HKU 7808/09M).
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