Optometry and Vision Sciences - Research Publications
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ItemComparison of contrast-dependent phase sensitivity in primary visual cortex of mouse, cat and macaque(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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ItemSynaptic Basis for Contrast-Dependent Shifts in Functional Identity in Mouse V1(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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ItemPattern Motion Processing by MT Neurons(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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ItemUpper stimulation threshold for retinal ganglion cell activation(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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ItemFeasibility of Nitrogen Doped Ultrananocrystalline Diamond Microelectrodes for Electrophysiological Recording From Neural Tissue(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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ItemNeural basis of forward flight control and landing in honeybees(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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ItemLong-term sensorimotor adaptation in the ocular following system of primates(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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ItemElectrical receptive fields of retinal ganglion cells: Influence of presynaptic neurons(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.
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ItemSensory experience modifies feature map relationships in visual cortex(ELIFE SCIENCES PUBLICATIONS LTD, 2016-06-16)The extent to which brain structure is influenced by sensory input during development is a critical but controversial question. A paradigmatic system for studying this is the mammalian visual cortex. Maps of orientation preference (OP) and ocular dominance (OD) in the primary visual cortex of ferrets, cats and monkeys can be individually changed by altered visual input. However, the spatial relationship between OP and OD maps has appeared immutable. Using a computational model we predicted that biasing the visual input to orthogonal orientation in the two eyes should cause a shift of OP pinwheels towards the border of OD columns. We then confirmed this prediction by rearing cats wearing orthogonally oriented cylindrical lenses over each eye. Thus, the spatial relationship between OP and OD maps can be modified by visual experience, revealing a previously unknown degree of brain plasticity in response to sensory input.
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ItemFrequency Responses of Rat Retinal Ganglion Cells(PUBLIC LIBRARY SCIENCE, 2016-06-24)There are 15-20 different types of retinal ganglion cells (RGC) in the mammalian retina, each encoding different aspects of the visual scene. The mechanism by which post-synaptic signals from the retinal network generate spikes is determined by each cell's intrinsic electrical properties. Here we investigate the frequency responses of morphologically identified rat RGCs using intracellular injection of sinusoidal current waveforms, to assess their intrinsic capabilities with minimal contributions from the retinal network. Recorded cells were classified according to their morphological characteristics (A, B, C or D-type) and their stratification (inner (i), outer (o) or bistratified) in the inner plexiform layer (IPL). Most cell types had low- or band-pass frequency responses. A2, C1 and C4o cells were band-pass with peaks of 15-30 Hz and low-pass cutoffs above 56 Hz (A2 cells) and ~42 Hz (C1 and C4o cells). A1 and C2i/o cells were low-pass with peaks of 10-15 Hz (cutoffs 19-25 Hz). Bistratified D1 and D2 cells were also low-pass with peaks of 5-10 Hz (cutoffs ~16 Hz). The least responsive cells were the B2 and C3 types (peaks: 2-5 Hz, cutoffs: 8-11 Hz). We found no difference between cells stratifying in the inner and outer IPL (i.e., ON and OFF cells) or between cells with large and small somas or dendritic fields. Intrinsic physiological properties (input resistance, spike width and sag) had little impact on frequency response at low frequencies, but account for 30-40% of response variability at frequencies >30 Hz.