How fly neurons compute the direction of visual motion
Detecting the direction of image motion is important for visual navigation, predator avoidance and prey capture, and thus essential for the survival of all animals that have eyes. However, the direction of motion is not explicitly represented at the level of the photoreceptors: it rather needs to be computed by subsequent neural circuits, involving a comparison of the signals from neighboring photoreceptors over time. The exact nature of this process represents a classic example of neural computation and has been a longstanding question in the field. Much progress has been made in recent years in the fruit fly Drosophila melanogaster by genetically targeting individual neuron types to block, activate or record from them. Our results obtained this way demonstrate that the local direction of motion is computed in two parallel ON and OFF pathways. Within each pathway, a retinotopic array of four direction-selective T4 (ON) and T5 (OFF) cells represents the four Cartesian components of local motion vectors (leftward, rightward, upward, downward). Since none of the presynaptic neurons is directionally selective, direction selectivity first emerges within T4 and T5 cells. Our present research focuses on the cellular and biophysical mechanisms by which the direction of image motion is computed in these neurons.
Direction-selective ganglion cells in primate retina: a subcortical substrate for reflexive gaze stabilization?
To maintain a stable and clear image of the world, our eyes reflexively follow the direction in which a visual scene is moving. Such gaze stabilization mechanisms reduce image blur as we move in the environment. In non-primate mammals, this behavior is initiated by ON-type direction-selective ganglion cells (ON-DSGCs), which detect the direction of image motion and transmit signals to brainstem nuclei that drive compensatory eye movements. However, ON-DSGCs have not yet been functionally identified in primates, raising the possibility that the visual inputs that drive this behavior instead arise in the cortex. In this talk, I will present molecular, morphological and functional evidence for identification of an ON-DSGC in macaque retina. The presence of ON-DSGCs highlights the need to examine the contribution of subcortical retinal mechanisms to normal and aberrant gaze stabilization in the developing and mature visual system. More generally, our findings demonstrate the power of a multimodal approach to study sparsely represented primate RGC types.
How fly neurons compute the direction of visual motion
Detecting the direction of image motion is important for visual navigation, predator avoidance and prey capture, and thus essential for the survival of all animals that have eyes. However, the direction of motion is not explicitly represented at the level of the photoreceptors: it rather needs to be computed by subsequent neural circuits. The exact nature of this process represents a classic example of neural computation and has been a longstanding question in the field. Our results obtained in the fruit fly Drosophila demonstrate that the local direction of motion is computed in two parallel ON and OFF pathways. Within each pathway, a retinotopic array of four direction-selective T4 (ON) and T5 (OFF) cells represents the four Cartesian components of local motion vectors (leftward, rightward, upward, downward). Since none of the presynaptic neurons is directionally selective, direction selectivity first emerges within T4 and T5 cells. Our present research focuses on the cellular and biophysical mechanisms by which the direction of image motion is computed in these neurons.
Heading perception in crowded environments
Self-motion through a visual world creates a pattern of expanding visual motion called optic flow. Heading estimation from the optic flow is accurate in rigid environments. But it becomes challenging when other humans introduce an independent motion to the scene. The biological motion of human walkers consists of translation through space and associated limb articulation. The characteristic motion pattern is regular, though complex. A world full of humans moving around is nonrigid, causing heading errors. But limb articulation alone does not perturb the global structure of the flow field, matching the rigidity assumption. For heading perception from optic flow analysis, limb articulation alone should not impair heading estimates. But we observed heading biases when participants encountered a group of point-light walkers. Our research investigates the interactions between optic flow perception and biological motion perception. We further analyze the impact of environmental information.
On the contributions of retinal direction selectivity to cortical motion processing in mice
Cells preferentially responding to visual motion in a particular direction are said to be direction-selective, and these were first identified in the primary visual cortex. Since then, direction-selective responses have been observed in the retina of several species, including mice, indicating motion analysis begins at the earliest stage of the visual hierarchy. Yet little is known about how retinal direction selectivity contributes to motion processing in the visual cortex. In this talk, I will present our experimental efforts to narrow this gap in our knowledge. To this end, we used genetic approaches to disrupt direction selectivity in the retina and mapped neuronal responses to visual motion in the visual cortex of mice using intrinsic signal optical imaging and two-photon calcium imaging. In essence, our work demonstrates that direction selectivity computed at the level of the retina causally serves to establish specialized motion responses in distinct areas of the mouse visual cortex. This finding thus compels us to revisit our notions of how the brain builds complex visual representations and underscores the importance of the processing performed in the periphery of sensory systems.
Attention to visual motion: shaping sensation into perception
Evolution has endowed primates, including humans, with a powerful visual system, seemingly providing us with a detailed perception of our surroundings. But in reality the underlying process is one of active filtering, enhancement and reshaping. For visual motion perception, the dorsal pathway in primate visual cortex and in particular area MT/V5 is considered to be of critical importance. Combining physiological and psychophysical approaches we have used the processing and perception of visual motion and area MT/V5 as a model for the interaction of sensory (bottom-up) signals with cognitive (top-down) modulatory influences that characterizes visual perception. Our findings document how this interaction enables visual cortex to actively generate a neural representation of the environment that combines the high-performance sensory periphery with selective modulatory influences for producing an “integrated saliency map’ of the environment.
Synergy of color and motion vision for detecting approaching objects in Drosophila
I am working on color vision in Drosophila, identifying behaviors that involve color vision and understanding the neural circuits supporting them (Longden 2016). I have a long-term interest in understanding how neural computations operate reliably under changing circumstances, be they external changes in the sensory context, or internal changes of state such as hunger and locomotion. On internal state-modulation of sensory processing, I have shown how hunger alters visual motion processing in blowflies (Longden et al. 2014), and identified a role for octopamine in modulating motion vision during locomotion (Longden and Krapp 2009, 2010). On responses to external cues, I have shown how one kind of uncertainty in the motion of the visual scene is resolved by the fly (Saleem, Longden et al. 2012), and I have identified novel cells for processing translation-induced optic flow (Longden et al. 2017). I like working with colleagues who use different model systems, to get at principles of neural operation that might apply in many species (Ding et al. 2016, Dyakova et al. 2015). I like work motivated by computational principles - my background is computational neuroscience, with a PhD on models of memory formation in the hippocampus (Longden and Willshaw, 2007).
Vision in dynamically changing environments
Many visual systems can process information in dynamically changing environments. In general, visual perception scales with changes in the visual stimulus, or contrast, irrespective of background illumination. This is achieved by adaptation. However, visual perception is challenged when adaptation is not fast enough to deal with sudden changes in overall illumination, for example when gaze follows a moving object from bright sunlight into a shaded area. We have recently shown that the visual system of the fly found a solution by propagating a corrective luminance-sensitive signal to higher processing stages. Using in vivo two-photon imaging and behavioural analyses we showed that distinct OFF-pathway inputs encode contrast and luminance. The luminance-sensitive pathway is particularly required when processing visual motion in contextual dim light, when pure contrast sensitivity underestimates the salience of a stimulus. Recent work in the lab has addressed the question how two visual pathways obtain such fundamentally different sensitivities, given common photoreceptor input. We are furthermore currently working out the network-based strategies by which luminance- and contrast-sensitive signals are combined to guide appropriate visual behaviour. Together, I will discuss the molecular, cellular, and circuit mechanisms that ensure contrast computation, and therefore robust vision, in fast changing visual scenes.