Case Studies in Invertebrate Visual Processing: I. Spectral and Spatial Processing in the Early Visual System of Drosophila melanogaster II. Binocular Stereopsis in Sepia officinalis

This thesis addresses two aspects of visual processing in two different invertebrate organisms. The fruit fly, Drosophila melanogaster, has emerged as a key model for invertebrate vision research. Despite extensive characterisation of motion vision, very little is known about how flies process colour information, or how the spectral content of light affects other visual modalities. With the aim to accurately dissect the different components of the Drosophila visual system responsible for processing colour, I have developed a versatile visual stimulation setup to probe for the combinations of spatial, temporal and spectral visual response properties. Using flies that express neural activity indicators, I can track visual responses to a colour stimulus (i.e. narrow bands of light across the spectrum) via a two-photon imaging system. The visual stimulus is projected on a specialised screen material that scatters wavelengths of light across the spectrum equally at all locations of the screen, thus enabling presentation of spatially structured stimuli. Using this setup, I have characterised spectral responses, intensity-response relationships, and receptive fields of neurons in the early visual system of a variety of genetically modified strains of Drosophila. Specifically, I compared visual responses in the medulla of flies expressing either a subset or all photoreceptor opsins, with differing levels of screening pigment present in the eye. I found layer-specific shifts of spectral response properties correlating with projection regions of photoreceptor terminals. I also 3 found that a reduction in screening pigment shifts the general spectral response in the neuropil towards the longer wavelengths of light. I have also mapped receptive fields across the different layers of the medulla for the peak spectral response wavelength. My results suggest that receptive field dimensions match the expected size predicted by the conservation of a columnar organisation in the medulla, with little variation from layer to layer. In a subset of these cells, we see an elongated receptive field suggestive of static orientation selectivity with an apparent split in the preferred axis of orientation of these receptive fields, with a near-orthogonal angle between the summed vectors of the split populations. The camera type eyes of vertebrates and cephalopods exhibit remarkable convergence, but it is currently unknown if the mechanisms for visual information processing in these brains, which exhibit wildly disparate architecture, is also shared. I chose to investigate the visual processing mechanism known as stereopsis in the cuttlefish Sepia officinalis. Stereoscopic vision is used to assess depth information by comparing the disparity between left and right visual fields. This strategy is commonplace in vertebrates having evolved multiple times independently but has only been demonstrated in one invertebrate: the praying mantis. Cuttlefish require precise distance estimation during their predatory hunt when they extend two tentacles in a ballistic strike to catch their target. Using a 3D perception paradigm whereby the cuttlefish were fitted with anaglyph glasses, I show that these animals use stereopsis to resolve distance to their prey. Although this is not an exclusive depth perception mechanism for hunting, it does shorten the time and distance covered prior to striking at a target. Furthermore, stereopsis in cuttlefish works differently to vertebrates, as cuttlefish can extract stereopsis cues from anti-correlated stimuli.BBSRC Doctoral Training Partnershi

A comparative study of cortical computations in the mammalian visual cortex

textA common feature of all mammals is the cerebral cortex, which is essential for higher-order functions and processing information to generate motor actions. While cortical circuits exhibit a striking uniformity in anatomical organization, it is unknown whether these circuits preform similar computations across mammalian species. In this dissertation I compare the emergence of two computations in the primary visual cortex (V1) of carnivores and rodents. A cortical computation is a transformation in neural representation, such that the spiking output of a cortical neuron exhibits a selectivity not present in the inputs from upstream neurons. Here I explore two computations: orientation selectivity, the preference of neurons for oriented edges in the visual world, and binocularity, the integration of signals from the two eyes. In the first section, I compare the emergence of orientation selectivity in the early visual pathway of mouse and cat. Recordings from thalamic relay cells and V1 neurons in both species reveal orientation selectivity in mouse V1 is not emergent, and could be inherited subcortically. In a second set of experiments, I measure orientation selectivity and the organization of V1 orientation preference in a grasshopper mouse with predatory behavior, compared to the scavenger lab mouse. Here I find the same functional properties. In the second section, I focus on the integration of ocular inputs in V1 of mouse and cat. I first compare disparity selectivity in cats, where convergence of ocular inputs has long been established, with mice, where ocular integration had not previously been investigated. Similar to cats, mouse V1 neurons were sensitive to binocular disparity, albeit to a lesser degree, and could be described by a linear feed-forward model. I next explore the disruption of binocular disparity tuning in both animals. In cats, strabismus induced during development causes increased monocularity in V1 and a loss of disparity selectivity. In mice, monocular deprivation causes increased ocular input, which also manifests as decreased disparity selectivity. Finally, I explore how excitatory and inhibitory neurons in mouse V1 integrate binocular signals. Paravalbumin-expressing inhibitory interneurons are more binocular but less disparity tuned than surrounding cortical neurons, providing a canonical mechanism explaining loss of disparity selectivity in both carnivores and rodents.Neuroscienc

Neurons in striate cortex limit the spatial and temporal resolution for detecting disparity modulation.

Stereopsis is the process of seeing depth constructed from binocular disparity. The human ability to perceive modulation of disparity over space (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004a) and time (Norcia and Tyler, 1984) is surprisingly poor, compared with the ability to detect spatial and temporal modulation of luminance contrast. In order to examine the physiological basis of this poor spatial and temporal resolution of stereopsis, I quantified responses to disparity modulation in disparity selective V1 neurons from four awake behaving monkeys. To study the physiological basis of the spatial resolution of stereopsis, I characterized the three-dimensional structure of 55 V1 receptive fields (RF) using random dot stereograms in which disparity varied as a sinusoidal function of vertical position (“corrugations”). At low spatial frequencies, this produced a modulation in neuronal firing at the temporal frequency of the stimulus. As the spatial frequency increased, the modulation reduced. The mean response rate changed little, and was close to that produced by a uniform stimulus at the mean disparity of the corrugation. In 48/55 (91%) of the neurons, the modulation strength was a lowpass function of spatial frequency. These results suggest that the neurons have fronto-parallel planar receptive fields, no disparity-based surround inhibition and no selectivity for disparity gradients. This scheme predicts a relationship between RF size and the high frequency cutoff. Comparison with independent measurements of RF size was compatible with this. All of this behavior closely matches the binocular energy model, which functionally corresponds to cross-correlation: the disparity modulated activity of the binocular neuron measures the correlation between the filtered monocular images. To examine the physiological basis of the temporal resolution of stereopsis, I measured for 59 neurons the temporal frequency tuning with random dot stereograms in which disparity varied as a sinusoidal function of time. Temporal frequency tuning in response to disparity modulation was not correlated with temporal frequency tuning in response to contrast modulation, and had lower temporal frequency high cutoffs on average. The temporal frequency high cut for disparity modulation was negatively correlated with the response latency, the speed of the response onset and the temporal integration time (slope of the line relating response phase and temporal frequency). Binocular cross-correlation of the monocular images after bandpass filtering can explain all these results. Average peak temporal frequency in response to disparity modulation was 2Hz, similar to the values I found in four human observers (1.5-3Hz). The mean cutoff spatial frequency, 0.5 cpd, was similar to equivalent measures of decline in human psychophysical sensitivity for such depth corrugations as a function of frequency (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004a). This suggests that the human temporal and spatial resolution for stereopsis is limited by selectivity of V1 neurons. For both, space and time, the lower resolution for disparity modulation than for contrast modulation can be explained by a single mechanism, binocular cross-correlation of the monocular images. The findings also represent a significant step towards understanding the process by which neurons solve the stereo correspondence problem (Julesz, 1971)

Kinetic Monte Carlo simulations for heterogeneous catalysis: Fundamentals, current status and challenges

Kinetic Monte Carlo (KMC) simulations in combination with first-principles-based calculations are rapidly becoming the gold-standard computational framework for bridging the gap between the wide range of length and time-scales over which heterogeneous catalysis unfolds. First-principles KMC (1p-KMC) simulations provide accurate insights into reactions over surfaces, a vital step towards the rational design of novel catalysts. In this perspective article, we briefly outline basic principles, computational challenges, successful applications, as well as future directions and opportunities of this promising and ever more popular kinetic modeling approach

Change blindness: eradication of gestalt strategies

Arrays of eight, texture-defined rectangles were used as stimuli in a one-shot change blindness (CB) task where there was a 50% chance that one rectangle would change orientation between two successive presentations separated by an interval. CB was eliminated by cueing the target rectangle in the first stimulus, reduced by cueing in the interval and unaffected by cueing in the second presentation. This supports the idea that a representation was formed that persisted through the interval before being 'overwritten' by the second presentation (Landman et al, 2003 Vision Research 43149–164]. Another possibility is that participants used some kind of grouping or Gestalt strategy. To test this we changed the spatial position of the rectangles in the second presentation by shifting them along imaginary spokes (by ±1 degree) emanating from the central fixation point. There was no significant difference seen in performance between this and the standard task [F(1,4)=2.565, p=0.185]. This may suggest two things: (i) Gestalt grouping is not used as a strategy in these tasks, and (ii) it gives further weight to the argument that objects may be stored and retrieved from a pre-attentional store during this task

Comodulation enhances signal detection via priming of auditory cortical circuits

Acoustic environments are composed of complex overlapping sounds that the auditory system is required to segregate into discrete perceptual objects. The functions of distinct auditory processing stations in this challenging task are poorly understood. Here we show a direct role for mouse auditory cortex in detection and segregation of acoustic information. We measured the sensitivity of auditory cortical neurons to brief tones embedded in masking noise. By altering spectrotemporal characteristics of the masker, we reveal that sensitivity to pure tone stimuli is strongly enhanced in coherently modulated broadband noise, corresponding to the psychoacoustic phenomenon comodulation masking release. Improvements in detection were largest following priming periods of noise alone, indicating that cortical segregation is enhanced over time. Transient opsin-mediated silencing of auditory cortex during the priming period almost completely abolished these improvements, suggesting that cortical processing may play a direct and significant role in detection of quiet sounds in noisy environments

Pitch Processing Sites in the Human Auditory Brain

Lateral Heschl's gyrus (HG), a subdivision of the human auditory cortex, is commonly believed to represent a general “pitch center,” responding selectively to the pitch of sounds, irrespective of their spectral characteristics. However, most neuroimaging investigations have used only one specialized pitch-evoking stimulus: iterated-ripple noise (IRN). The present study used a novel experimental design in which a range of different pitch-evoking stimuli were presented to the same listeners. Pitch sites were identified by searching for voxels that responded well to the range of pitch-evoking stimuli. The first result suggested that parts of the planum temporale are more relevant for pitch processing than lateral HG. In some listeners, pitch responses occurred elsewhere, such as the temporo-parieto-occipital junction or prefrontal cortex. The second result demonstrated a different pattern of response to the IRN and raises the possibility that features of IRN unrelated to pitch might contribute to the earlier results. In conclusion, it seems premature to assign special status to lateral HG solely on the basis of neuroactivation patterns. Further work should consider the functional roles of these multiple pitch processing sites within the proposed network

Signal transformation and noise correlation in the primate dorsal stream during sensory decision-making

Neuroscientists have long sought a link between the activity of single neurons and our thoughts, perceptions and ultimately our mental experiences. As our senses provide the input into the brain, understanding the computations that transform signals along the sensory pathways has remained central to this endeavor. Remarkable progress has been made by studying neural correlates of perceptual decisions in motion-processing and oculomotor areas of the primate brain. In particular, when monkeys indicate their decisions about the direction of motion with eye movements, neurons in the middle temporal area (MT) represent the instantaneous motion evidence and neurons in the lateral intraparietal area (LIP) resemble the integration of motion evidence, effectively transforming the sensory signal into a decision variable. In the main body of this thesis, I describe the results of an effort to measure the sensorimotor transformation between MT and LIP on single trials. First, I describe a motion-discrimination task that is amenable to reverse correlation analysis, allowing the experimenter to measure the temporal dependencies of neural responses and choices on the instantaneous motion energy. I then use a unified statistical framework to analyze simultaneous recordings from both areas during decision-making. Primarily, I found that MT neurons exhibited time-varying sensitivity to motion direction, with important consequences for the behavior and neurophysiology in downstream areas. Individual LIP neurons also carried a signature of an integrated motion signal in their spike rates, however, it was unlikely that this signal results from direct MT input. Finally, I show that a biologically plausible simple decoder can perform as well as the monkey at coarse direction-discrimination task. In the appendix, I describe the results of pharmacological inactivations of MT and LIP and statistical models of single trial dynamics in LIP that were performed in collaboration with fellow graduate students, Leor Katz and Kenneth Latimer, respectively.Neuroscienc

Local Sensitivity to Stimulus Orientation and Spatial Frequency within the Receptive Fields of Neurons in Visual Area 2 (V2) of Macaque Monkeys

We used dynamic dense noise stimuli and local spectral reverse correlation methods to reveal the local sensitivities of neurons in visual area 2 (V2) of macaque monkeys to orientation and spatial frequency within their receptive fields. This minimized the potentially confounding assumptions that are inherent in stimulus selections. The majority of neurons exhibited a relatively high degree of homogeneity for the preferred orientations and spatial frequencies in the spatial matrix of facilitatory subfields. However, about 20% of all neurons showed maximum orientation differences between neighboring subfields that were greater than 25 deg. The neurons preferring horizontal or vertical orientations showed less inhomogeneity in space than the neurons preferring oblique orientations. Over 50% of all units also exhibited suppressive profiles, and those were more heterogeneous than facilitatory profiles. The preferred orientation and spatial frequency of suppressive profiles differed substantially from those of facilitatory profiles, and the neurons with suppressive subfields had greater orientation selectivity than those without suppressive subfields. The peak suppression occurred with longer delays than the peak facilitation. These results suggest that the receptive field profiles of the majority of V2 neurons reflect the orderly convergence of V1 inputs over space, but that a subset of V2 neurons exhibit more complex response profiles having both suppressive and facilitatory subfields. These V2 neurons with heterogeneous subfield profiles could play an important role in the initial processing of complex stimulus features