Kit D. Longden

Octopaminergic Modulation of Temporal Frequency Coding in an Identified Optic Flow-Processing Interneuron

Flying generates predictably different patterns of optic flow compared with other locomotor states. A sensorimotor system tuned to rapid responses and a high bandwidth of optic flow would help the animal to avoid wasting energy through imprecise motor action. However, neural processing that covers a higher input bandwidth itself comes at higher energetic costs which would be a poor investment when the animal was not flying. How does the blowfly adjust the dynamic range of its optic flow-processing neurons to the locomotor state? Octopamine (OA) is a biogenic amine central to the initiation and maintenance of flight in insects. We used an OA agonist chlordimeform (CDM) to simulate the widespread OA release during flight and recorded the effects on the temporal frequency coding of the H2 cell. This cell is a visual interneuron known to be involved in flight stabilization reflexes. The application of CDM resulted in (i) an increase in the cells spontaneous activity, expanding the inhibitory signaling range (ii) an initial response gain to moving gratings (20–60 ms post-stimulus) that depended on the temporal frequency of the grating and (iii) a reduction in the rate and magnitude of motion adaptation that was also temporal frequency-dependent. To our knowledge, this is the first demonstration that the application of a neuromodulator can induce velocity-dependent alterations in the gain of a wide-field optic flow-processing neuron. The observed changes in the cells response properties resulted in a 33% increase of the cells information rate when encoding random changes in temporal frequency of the stimulus. The increased signaling range and more rapid, longer lasting responses employed more spikes to encode each bit, and so consumed a greater amount of energy. It appears that for the fly investing more energy in sensory processing during flight is more efficient than wasting energy on under-performing motor control.

Nutritional State Modulates the Neural Processing of Visual Motion

Food deprivation alters the processing of sensory information, increasing neural activity in the olfactory and gustatory systems in animals across phyla. Neural signaling is metabolically costly, and a hungry animal has limited energy reserves, so we hypothesized that neural activity in other systems may be downregulated by food deprivation. We investigated this hypothesis in the motion vision pathway of the blowfly. Like other animals, flies augment their motion vision when moving: they increase the resting activity and gain of visual interneurons supporting the control of locomotion and gaze. In the present study, walking-induced changes in visual processing depended on the nutritional state-they decreased with food deprivation and recovered after subsequent feeding. We found that changes in the motion vision pathway depended on walking speed in a manner dependent on the nutritional state. Walking also reduced response latencies in visual interneurons, an effect not altered by food deprivation. Finally, the optomotor reflex that compensates for visual wide-field motion was reduced in food-deprived flies. Thus, walking augmented motion vision, but the effect was decreased when energy reserves were low. Our results suggest that energy limitations may drive the rebalancing of neural activity with changes in the nutritional state.

Bimodal optomotor response to plaids in blowflies: mechanisms of component selectivity and evidence for pattern selectivity.

Many animals estimate their self-motion and the movement of external objects by exploiting panoramic patterns of visual motion. To probe how visual systems process compound motion patterns, superimposed visual gratings moving in different directions, plaid stimuli, have been successfully used in vertebrates. Surprisingly, nothing is known about how visually guided insects process plaids. Here, we explored in the blowfly how the well characterized yaw optomotor reflex and the activity of identified visual interneurons depend on plaid stimuli. We show that contrary to previous expectations, the yaw optomotor reflex shows a bimodal directional tuning for certain plaid stimuli. To understand the neural correlates of this behavior, we recorded the responses of a visual interneuron supporting the reflex, the H1 cell, which was also bimodally tuned to the plaid direction. Using a computational model, we identified the essential neural processing steps required to capture the observed response properties. These processing steps have functional parallels with mechanisms found in the primate visual system, despite different biophysical implementations. By characterizing other visual neurons supporting visually guided behaviors, we found responses that ranged from being bimodally tuned to the stimulus direction (component-selective), to responses that appear to be tuned to the direction of the global pattern (pattern-selective). Our results extend the current understanding of neural mechanisms of motion processing in insects, and indicate that the fly employs a wider range of behavioral responses to multiple motion cues than previously reported.

Spike Burst Coding of Translatory Optic Flow and Depth from Motion in the Fly Visual System

Many animals use the visual motion generated by traveling straight-the translatory optic flow-to successfully navigate obstacles: near objects appear larger and to move more quickly than distant objects. Flies are expert at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. We present novel cell types that have local motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes self-motion in the forward-sideslip direction and fires action potentials in spike bursts as well as single spikes. We show that the spike burst coding is size and speed-tuned and is selectively modulated by motion parallax-the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the rate of single spikes is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have properties well suited to the visual navigation of clutter and to encode the flys movements along near cardinal axes of thrust, lift, and forward sideslip.

Central Brain Circuitry for Color-Vision-Modulated Behaviors

Color is famous for not existing in the external world: our brains create the perception of color from the spatial and temporal patterns of the wavelength and intensity of light. For an intangible quality, we have detailed knowledge of its origins and consequences. Much is known about the organization and evolution of the first phases of color processing, the filtering of light in the eye and processing in the retina, and about the final phases, the roles of color in behavior and natural selection. To understand how color processing in the central brain has evolved, we need well-defined pathways or circuitry where we can gauge how color contributes to the computations involved in specific behaviors. Examples of such pathways or circuitry that are dedicated to processing color cues are rare, despite the separation of color and luminance pathways early in the visual system of many species, and despite the traditional definition of color as being independent of luminance. This minireview presents examples in which color vision contributes to behaviors dominated by other visual modalities, examples that are not part of the canon of color vision circuitry. The pathways and circuitry process a range of chromatic properties of objects and their illumination, and are taken from a variety of species. By considering how color processing complements luminance processing, rather than being independent of it, we gain an additional way to account for the diversity of color coding in the central brain, its consequences for specific behaviors and ultimately the evolution of color vision.

Colour Vision: A Fresh View of Lateral Inhibition in Drosophila

A recent study reports a novel form of lateral inhibition between photoreceptors supporting colour vision in the vinegar fly, Drosophila melanogaster.

Sensorimotor Neuroscience: Motor Precision Meets Vision

Visual motion sensing neurons in the fly also encode a range of behavior-related signals. These nonvisual inputs appear to be used to correct some of the challenges of visually guided locomotion.

Asynchronous inputs and NMDA conductances predict excitatory responses in the cortical-cA1 pathway of the hippocampus

In the hippocampus, CA1 place cells are driven by a substantial input from CA3. There is a second pathway to CA1 from the entorhinal cortex. The mode of action of cortex on CA1 through this pathway is not known. The pathway supports CA1 place field activity after CA3 has been lesioned, yet stimulation of the pathway in rat slices results in strong feedforward inhibition that prevents pyramidal cell action potentials. We use a detailed conductance-based model of this pathway to simulate the response to cortical stimulation in slice experiments and in vivo spatial exploration. We find that the presence of NMDA conductances enable CA1 pyramidal cells to integrate cortical inputs over a time scale longer than that which is effective in recruiting the inhibitory response that can suppress action potentials. We then show that this asynchronous response mode supports place field formation in response to experimentally constrained spatially modulated cortical activity. Within this model, the inclusion of GABAB conductances and the hyperpolarisation activated current Ih reduces the strength of the GABAA inputs required to balance the excitatory inputs, and this facilitates place field formation by reducing variability in the inhibitory inputs.