Optometry and Vision Sciences - Research Publications

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    A Three-Dimensional Atlas of the Honeybee Neck
    Berry, RP ; Ibbotson, MR ; Giurfa, M (PUBLIC LIBRARY SCIENCE, 2010-05-24)
    Three-dimensional digital atlases are rapidly becoming indispensible in modern biology. We used serial sectioning combined with manual registration and segmentation of images to develop a comprehensive and detailed three-dimensional atlas of the honeybee head-neck system. This interactive atlas includes skeletal structures of the head and prothorax, the neck musculature, and the nervous system. The scope and resolution of the model exceeds atlases previously developed on similar sized animals, and the interactive nature of the model provides a far more accessible means of interpreting and comprehending insect anatomy and neuroanatomy.
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    Ocellar structure and neural innervation in the honeybee
    Hung, Y-S ; Ibbotson, MR (FRONTIERS MEDIA SA, 2014-02-19)
    Honeybees have a visual system composed of three ocelli (simple eyes) located on the top of the head, in addition to two large compound eyes. Although experiments have been conducted to investigate the role of the ocelli within the visual system, their optical characteristics, and function remain controversial. In this study, we created three-dimensional (3-D) reconstructions of the honeybee ocelli, conducted optical measurements and filled ocellar descending neurons to assist in determining the role of ocelli in honeybees. In both the median and lateral ocelli, the ocellar retinas can be divided into dorsal and ventral parts. Using the 3-D model we were able to assess the viewing angles of the retinas. The dorsal retinas view the horizon while the ventral retinas view the sky, suggesting quite different roles in attitude control. We used the hanging drop technique to assess the spatial resolution of the retinas. The lateral ocelli have significantly higher spatial resolution compared to the median ocellus. In addition, we established which ocellar retinas provide the input to five pairs of large ocellar descending neurons. We found that four of the neuron pairs have their dendritic fields in the dorsal retinas of the lateral ocelli, while the fifth has fine dendrites in the ventral retina. One of the neuron pairs also sends very fine dendrites into the border region between the dorsal and ventral retinas of the median ocellus.
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    Comparison of contrast-dependent phase sensitivity in primary visual cortex of mouse, cat and macaque
    Yunzab, M ; Cloherty, SL ; Ibbotson, MR (LIPPINCOTT WILLIAMS & WILKINS, 2019-10-09)
    Neurones in the primary visual cortex (V1) are classified into simple and complex types. Simple cells are phase-sensitive, that is, they modulate their responses according to the position and brightness polarity of edges in their receptive fields. Complex cells are phase invariant, that is, they respond to edges in their receptive fields regardless of location or brightness polarity. Simple and complex cells are quantified by the degree of sensitivity to the spatial phases of drifting sinusoidal gratings. Some V1 complex cells become more phase-sensitive at low contrasts. Here we use a standardized analysis method for data derived from grating stimuli developed for macaques to reanalyse data previously collected from cats, and also collect and analyse the responses of 73 mouse V1 neurons. The analysis provides the first consistent comparative study of contrast-dependent phase sensitivity in V1 of mouse, cat and macaque monkey.
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    Synaptic Basis for Contrast-Dependent Shifts in Functional Identity in Mouse V1
    Yunzab, M ; Choi, V ; Meffin, H ; Cloherty, SL ; Priebe, NJ ; Ibbotson, MR (Society for Neuroscience., 2019-03)
    A central transformation that occurs within mammalian visual cortex is the change from linear, polarity-sensitive responses to nonlinear, polarity-insensitive responses. These neurons are classically labelled as either simple or complex, respectively, on the basis of their response linearity (Skottun et al., 1991). While the difference between cell classes is clear when the stimulus strength is high, reducing stimulus strength diminishes the differences between the cell types and causes some complex cells to respond as simple cells (Crowder et al., 2007; van Kleef et al., 2010; Hietanen et al., 2013). To understand the synaptic basis for this shift in behavior, we used in vivo whole-cell recordings while systematically shifting stimulus contrast. We find systematic shifts in the degree of complex cell responses in mouse primary visual cortex (V1) at the subthreshold level, demonstrating that synaptic inputs change in concert with the shifts in response linearity and that the change in response linearity is not simply due to the threshold nonlinearity. These shifts are consistent with a visual cortex model in which the recurrent amplification acts as a critical component in the generation of complex cell responses (Chance et al., 1999).
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    Pattern Motion Processing by MT Neurons
    Eskikand, PZ ; Kameneva, T ; Burkitt, AN ; Grayden, DB ; Ibbotson, MR (Frontiers Media, 2019-06-21)
    Based on stimulation with plaid patterns, neurons in the Middle Temporal (MT) area of primate visual cortex are divided into two types: pattern and component cells. The prevailing theory suggests that pattern selectivity results from the summation of the outputs of component cells as part of a hierarchical visual pathway. We present a computational model of the visual pathway from primary visual cortex (V1) to MT that suggests an alternate model where the progression from component to pattern selectivity is not required. Using standard orientation-selective V1 cells, end-stopped V1 cells, and V1 cells with extra-classical receptive fields (RFs) as inputs to MT, the model shows that the degree of pattern or component selectivity in MT could arise from the relative strengths of the three V1 input types. Dominance of end-stopped V1 neurons in the model leads to pattern selectivity in MT, while dominance of V1 cells with extra-classical RFs result in component selectivity. This model may assist in designing experiments to further understand motion processing mechanisms in primate MT.
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    Upper stimulation threshold for retinal ganglion cell activation
    Meng, K ; Fellner, A ; Rattay, F ; Ghezzi, D ; Meffin, H ; Ibbotson, MR ; Kameneva, T (IOP PUBLISHING LTD, 2018-08)
    OBJECTIVE: The existence of an upper threshold in electrically stimulated retinal ganglion cells (RGCs) is of interest because of its relevance to the development of visual prosthetic devices, which are designed to restore partial sight to blind patients. The upper threshold is defined as the stimulation level above which no action potentials (direct spikes) can be elicited in electrically stimulated retina. APPROACH: We collected and analyzed in vitro recordings from rat RGCs in response to extracellular biphasic (anodic-cathodic) pulse stimulation of varying amplitudes and pulse durations. Such responses were also simulated using a multicompartment model. MAIN RESULTS: We identified the individual cell variability in response to stimulation and the phenomenon known as upper threshold in all but one of the recorded cells (n  =  20/21). We found that the latencies of spike responses relative to stimulus amplitude had a characteristic U-shape. In silico, we showed that the upper threshold phenomenon was observed only in the soma. For all tested biphasic pulse durations, electrode positions, and pulse amplitudes above lower threshold, a propagating action potential was observed in the distal axon. For amplitudes above the somatic upper threshold, the axonal action potential back-propagated in the direction of the soma, but the soma's low level of hyperpolarization prevented action potential generation in the soma itself. SIGNIFICANCE: An upper threshold observed in the soma does not prevent spike conductance in the axon.
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    Feasibility of Nitrogen Doped Ultrananocrystalline Diamond Microelectrodes for Electrophysiological Recording From Neural Tissue
    Wong, YT ; Ahnood, A ; Maturana, M ; Kentler, W ; Ganesan, K ; Grayden, DB ; Meffin, H ; Prawer, S ; Ibbotson, MR ; Burkitt, AN (FRONTIERS MEDIA SA, 2018-06-22)
    Neural prostheses that can monitor the physiological state of a subject are becoming clinically viable through improvements in the capacity to record from neural tissue. However, a significant limitation of current devices is that it is difficult to fabricate electrode arrays that have both high channel counts and the appropriate electrical properties required for neural recordings. In earlier work, we demonstrated nitrogen doped ultrananocrystalline diamond (N-UNCD) can provide efficacious electrical stimulation of neural tissue, with high charge injection capacity, surface stability and biocompatibility. In this work, we expand on this functionality to show that N-UNCD electrodes can also record from neural tissue owing to its low electrochemical impedance. We show that N-UNCD electrodes are highly flexible in their application, with successful recordings of action potentials from single neurons in an in vitro retina preparation, as well as local field potential responses from in vivo visual cortex tissue. Key properties of N-UNCD films, combined with scalability of electrode array fabrication with custom sizes for recording or stimulation along with integration through vertical interconnects to silicon based integrated circuits, may in future form the basis for the fabrication of versatile closed-loop neural prostheses that can both record and stimulate.
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    Neural basis of forward flight control and landing in honeybees
    Ibbotson, MR ; Hung, Y-S ; Meffin, H ; Boeddeker, N ; Srinivasan, MV (NATURE PORTFOLIO, 2017-11-06)
    The impressive repertoire of honeybee visually guided behaviors, and their ability to learn has made them an important tool for elucidating the visual basis of behavior. Like other insects, bees perform optomotor course correction to optic flow, a response that is dependent on the spatial structure of the visual environment. However, bees can also distinguish the speed of image motion during forward flight and landing, as well as estimate flight distances (odometry), irrespective of the visual scene. The neural pathways underlying these abilities are unknown. Here we report on a cluster of descending neurons (DNIIIs) that are shown to have the directional tuning properties necessary for detecting image motion during forward flight and landing on vertical surfaces. They have stable firing rates during prolonged periods of stimulation and respond to a wide range of image speeds, making them suitable to detect image flow during flight behaviors. While their responses are not strictly speed tuned, the shape and amplitudes of their speed tuning functions are resistant to large changes in spatial frequency. These cells are prime candidates not only for the control of flight speed and landing, but also the basis of a neural 'front end' of the honeybee's visual odometer.
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    Long-term sensorimotor adaptation in the ocular following system of primates
    Hietanen, MA ; Price, NSC ; Cloherty, SL ; Hadjidimitrakis, K ; Ibbotson, MR ; Sakakibara, M (PUBLIC LIBRARY SCIENCE, 2017-12-04)
    The sudden movement of a wide-field image leads to a reflexive eye tracking response referred to as short-latency ocular following. If the image motion occurs soon after a saccade the initial speed of the ocular following is enhanced, a phenomenon known as post-saccadic enhancement. We show in macaque monkeys that repeated exposure to the same stimulus regime over a period of months leads to progressive increases in the initial speeds of ocular following. The improvement in tracking speed occurs for ocular following with and without a prior saccade. As a result of the improvement in ocular following speeds, the influence of post-saccadic enhancement wanes with increasing levels of training. The improvement in ocular following speed following repeated exposure to the same oculomotor task represents a novel form of sensori-motor learning in the context of a reflexive movement.
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    Electrical receptive fields of retinal ganglion cells: Influence of presynaptic neurons
    Maturana, MI ; Apollo, NV ; Garrett, DJ ; Kameneva, T ; Cloherty, SL ; Grayden, DB ; Burkitt, AN ; Ibbotson, MR ; Meffin, H ; Fine, I (PUBLIC LIBRARY SCIENCE, 2018-02)
    Implantable retinal stimulators activate surviving neurons to restore a sense of vision in people who have lost their photoreceptors through degenerative diseases. Complex spatial and temporal interactions occur in the retina during multi-electrode stimulation. Due to these complexities, most existing implants activate only a few electrodes at a time, limiting the repertoire of available stimulation patterns. Measuring the spatiotemporal interactions between electrodes and retinal cells, and incorporating them into a model may lead to improved stimulation algorithms that exploit the interactions. Here, we present a computational model that accurately predicts both the spatial and temporal nonlinear interactions of multi-electrode stimulation of rat retinal ganglion cells (RGCs). The model was verified using in vitro recordings of ON, OFF, and ON-OFF RGCs in response to subretinal multi-electrode stimulation with biphasic pulses at three stimulation frequencies (10, 20, 30 Hz). The model gives an estimate of each cell's spatiotemporal electrical receptive fields (ERFs); i.e., the pattern of stimulation leading to excitation or suppression in the neuron. All cells had excitatory ERFs and many also had suppressive sub-regions of their ERFs. We show that the nonlinearities in observed responses arise largely from activation of presynaptic interneurons. When synaptic transmission was blocked, the number of sub-regions of the ERF was reduced, usually to a single excitatory ERF. This suggests that direct cell activation can be modeled accurately by a one-dimensional model with linear interactions between electrodes, whereas indirect stimulation due to summated presynaptic responses is nonlinear.