Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands
The compound eye of insects imposes a tradeoff between resolution and sensitivity, which should exacerbate with diminishing eye size. Tiny lenses are thought to deliver poor acuity because of diffraction; nevertheless, miniature insects have visual systems that allow a myriad of lifestyles. Here, we investigate whether size constraints result in an archetypal eye design shared between miniature dipterans by comparing the visual performance of the fruit fly Drosophila and the killer fly Coenosia. These closely related species have neural superposition eyes and similar body lengths (3 to 4 mm), but Coenosia is a diurnal aerial predator, whereas slow-flying Drosophila is most active at dawn and dusk. Using in vivo intracellular recordings and EM, we report unique adaptations in the form and function of their photoreceptors that are reflective of their distinct lifestyles. We find that although these species have similar lenses and optical properties, Coenosia photoreceptors have three- to fourfold higher spatial resolution and rate of information transfer than Drosophila. The higher performance in Coenosia mostly results from dramatically diminished light sensors, or rhabdomeres, which reduce pixel size and optical cross-talk between photoreceptors and incorporate accelerated phototransduction reactions. Furthermore, we identify local specializations in the Coenosia eye, consistent with an acute zone and its predatory lifestyle. These results demonstrate how the flexible architecture of miniature compound eyes can evolve to match information processing with ecological demands.
Paloma T. Gonzalez-Bellido1, Trevor J. Wardill1, and Mikko Juusola1,2
1 Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK
2 State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China
Intrinsic Activity in the Fly Brain Gates Visual Information during Behavioral Choices
The small insect brain is often described as an input/output system that executes reflex-like behaviors. It can also initiate neural activity and behaviors intrinsically, seen as spontaneous behaviors, different arousal states and sleep. However, less is known about how intrinsic activity in neural circuits affects sensory information processing in the insect brain and variability and behavior. Here, by simultaneously monitoring Drosophila’s behavioral choices and brain activity in a flight simulator system, we identify intrinsic activity that is associated with the act of selecting between visual stimuli. We recorded neural output (multiunit action potentials and local field potentials) in the left and right optic lobes of a tethered flying Drosophila, while its attempts to follow visual motion (yaw torque) were measured by a torque meter. We show that when facing competing motion stimuli on its left and right, Drosophila typically generate large torque responses that flip from side to side. The delayed onset (0.1–1 s) and spontaneous switch-like dynamics of these responses, and the fact that the flies sometimes oppose the stimuli by flying straight, make this behavior different from the classic steering reflexes. Drosophila, thus, seem to choose one stimulus at a time and attempt to rotate toward its direction. With this behavior, the neural output of the optic lobes alternates; being augmented on the side chosen for body rotation and suppressed on the opposite side, even though the visual input to the fly eyes stays the same. Thus, the flow of information from the fly eyes is gated intrinsically. Such modulation can be noise-induced or intentional; with one possibility being that the fly brain highlights chosen information while ignoring the irrelevant, similar to what we know to occur in higher animals.
Shiming Tang1,2*., Mikko Juusola1,3*
1 State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China
2 State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
3 Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom
Overexpressing Temperature-Sensitive Dynamin Decelerates Phototransduction and Bundles Microtubules in Drosophila Photoreceptors
shibirets1, a temperature-sensitive mutation of the Drosophila gene encoding a Dynamin orthologue, blocks vesicle endocytosis and thus synaptic transmission, at elevated, or restrictive temperatures. By targeted Gal4 expression, UAS-shibirets1 has been used to dissect neuronal circuits. We investigated the effects of UAS-shibirets1 overexpression in Drosophila photoreceptors at permissive (19°C) and restrictive (31°C) temperatures. At 19°C, overexpression of UAS-shits1 causes decelerated phototransduction and reduced neurotransmitter release. This phenotype is exacerbated with dark adaptation, age and in white mutants. Photoreceptors overexpressing UAS-shibirets1 contain terminals with widespread vacuolated mitochondria, reduced numbers of vesicles and bundled microtubules. Immuno-electron microscopy reveals that the latter are dynamin coated. Further, the microtubule phenotype is not restricted to photoreceptors, as UAS-shibirets1 overexpression in lamina cells also bundles microtubules. We conclude that dynamin has multiple functions that are interrupted by UAS-shibirets1 overexpression in Drosophila photoreceptors, destabilizing their neural communication irreversibly at previously reported permissive temperatures.
Paloma T. Gonzalez-Bellido,1 Trevor J. Wardill,1 Ripsik Kostyleva,2 Ian A. Meinertzhagen,2 and Mikko Juusola1,3
1 Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK
2 Department of Psychology and Neuroscience, Dalhousie University, Halifax, Nova Scotia 3BH 4J1, Canada
3 State Key Laboratory of Cognitive Neuroscience, Beijing Normal University, Beijing 100875, China
Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: I Dynamics
Because of the limited processing capacity of eyes, retinal networks must adapt constantly to best present the ever changing visual world to the brain. However, we still know little about how adaptation in retinal networks shapes neural encoding of changing information. To study this question, we recorded voltage responses from photoreceptors (R1–R6) and their output neurons (LMCs) in the Drosophila eye to repeated patterns of contrast values, collected from natural scenes. By analyzing the continuous photoreceptor-to-LMC transformations of these graded-potential neurons, we show that the efficiency of coding is dynamically improved by adaptation. In particular, adaptation enhances both the frequency and amplitude distribution of LMC output by improving sensitivity to under-represented signals within seconds. Moreover, the signal-to-noise ratio of LMC output increases in the same time scale. We suggest that these coding properties can be used to study network adaptation using the genetic tools in Drosophila, as shown in a companion paper (Part II).
Lei Zheng1, Anton Nikolaev1, Trevor J. Wardill1, Cahir J. O'Kane2, Gonzalo G. de Polavieja3,4, Mikko Juusola1,5*
1 Department of Biomedical Science, University of Sheffield, Sheffield, UK
2 Department of Genetics, University of Cambridge, Cambridge, UK
3 Department of Theoretical Physics, Universidad Autónoma de Madrid, Madrid, Spain
4 Instituto ‘Nicolás Cabrera’ de Física de Materiales, Universidad Autónoma de Madrid, Madrid, Spain
5 State Key Laboratory of Cognitive Neuroscience, Beijing Normal University, Beijing, China
Coding with spike shapes and graded potentials in cortical networks
In cortical neurones, analogue dendritic potentials are thought to be encoded into patterns of digital spikes. According to this view, neuronal codes and computations are based on the temporal patterns of spikes: spike times, bursts or spike rates. Recently, we proposed an action potential waveform code for cortical pyramidal neurones in which the spike shape carries information. Broader somatic action potentials are reliably produced in response to higher conductance input, allowing for four times more information transfer than spike times alone. This information is preserved during synaptic integration in a single neurone, as back-propagating action potentials of diverse shapes differentially shunt incoming postsynaptic potentials and so participate in the next round of spike generation. An open question has been whether the information in action potential waveforms can also survive axonal conduction and directly influence synaptic transmission to neighbouring neurones. Several new findings have now brought new light to this subject, showing cortical information processing that transcends the classical models.
Mikko Juusola 1*, Hugh P.C. Robinson 2, Gonzalo G. de Polavieja 3*
1 Department of Biomedical Science, University of Sheffield, Sheffield, UK
2 Department of Physiology, Development and Neuroscience, University of Cambridge, UK
3 Neural Processing Laboratory, Department of Theoretical Physics, Universidad Autonoma de Madrid, 28049 Madrid, Spain
Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila
At the layer of first visual synapses information from photoreceptors is processed and transmitted towards the brain. In fly compound eye, output from photoreceptors (R1-R6) that share the same visual field is pooled and transmitted via histaminergic synapses to two classes of interneuron, large monopolar cells (LMCs) and amacrine cells (ACs). The interneurons also feed back to photoreceptor terminals via numerous ligand-gated synapses, yet the significance of these connections has remained a mystery. We investigated the role of feedback synapses by comparing intracellular responses of photoreceptors and LMCs in wild-type Drosophila and in synaptic mutants, to light and current pulses and to naturalistic light stimuli. The recordings were further subjected to rigorous statistical and information-theoretical analysis. We show that the feedback synapses form a negative feedback loop that controls the speed and amplitude of photoreceptor responses and hence the quality of the transmitted signals. These results highlight the benefits of feedback synapses for neural information processing, and suggest that similar coding strategies could be used in other nervous systems.
Lei Zheng1, Gonzalo G. de Polavieja2,3, Verena Wolfram1, Musa H. Asyali4, Roger C. Hardie5 and Mikko Juusola*1
1 Department of Biomedical Science, University of Sheffield, S10 2TN, UK
2 Department of Theoretical Physics, Universidad Autónoma de Madrid, 28049 Spain
3 Instituto ‘Nicolás Cabrera’ de Física de Materiales, Universidad Autónoma de Madrid, 28049 Spain
4 Faculty of Engineering and Architecture, Yasar University, Izmir, Turkey
5 Department of Anatomy, University of Cambridge, CB2 3DY, UK
Stimulus History Reliably Shapes Action Potential
Waveforms of Cortical Neurons
Action potentials have been shown to shunt synaptic charge to a degree that depends on their waveform. In this way, they participate in synaptic integration, and thus in the probability of generating succeeding action potentials, in a shape-dependent way. Here we test whether the different action potential waveforms produced during dynamical stimulation in a single cortical neuron carry information about the conductance stimulus history. When pyramidal neurons in rat visual cortex were driven by a conductance stimulus that resembles natural synaptic input, somatic action potential waveforms showed a large variability that reliably signaled the history of the input for up to 50 ms before the spike. The correlation between stimulus history and action potential waveforms had low noise, resulting in information rates that were three to four times larger than for the instantaneous spike rate. The reliable correlation between stimulus history and spike waveforms then acts as a local encoding at the single-cell level. It also directly affects neuronal communication as different waveforms influence the production of succeeding spikes via differential shunting of synaptic charge. Modeling was used to show that slow conductances can implement memory of the stimulus history in cortical neurons, encoding this information in the spike shape.
G.G. de Polavieja1,2* A. Harsch1, I. Kleppe1, H.P.C. Robinson1 and M. Juusola1*
1 Physiological Laboratory, University of Cambridge, Cambridge CB2 3EG, UK
2 Neural Processing Laboratory, Department of Theoretical Physics, Universidad Autonoma de Madrid, 28049 Madrid, Spain
The Rate of Information Transfer of Naturalistic Stimulation by Graded Potentials
We present a method to measure the rate of information transfer for any continuous signals of finite duration without assumptions. After testing the method with simulated responses, we measure the encoding performance of Calliphora photoreceptors.
We find that especially for naturalistic stimulation the responses are nonlinear and noise is nonadditive, and show that adaptation mechanisms affect signal and noise differentially depending on the time scale, structure, and speed of the stimulus. Different signaling strategies for short- and long-term and dim and bright light are found for this graded system when stimulated with naturalistic light changes.
M. Juusola1* and G.G. de Polavieja2*,
1 Physiological Laboratory, University of Cambridge, Cambridge CB2 3DY, UK.
2 Department of Theoretical Physics, Universidad Autonoma de Madrid, 28049 Madrid, Spain.
The contribution of Shaker K+ channels to the information capacity of Drosophila photoreceptors
An array of rapidly inactivating voltage-gated K+ channels is distributed throughout the nervous systems of vertebrates and invertebrates. Although these channels are thought to regulate the excitability of neurons by attenuating voltage signals, their specific functions are often poorly understood. We studied the role of the prototypical inactivating K+ conductance, Shaker, in Drosophila photoreceptors by recording intracellularly from wild-type and Shaker mutant photoreceptors. Here we show that loss of the Shaker K+ conductance produces a marked reduction in the signal-to-noise ratio of photoreceptors, generating a 50% decrease in the information capacity of these cells in fully light-adapted conditions. By combining experiments with modelling, we show that the inactivation of Shaker K+ channels amplifies voltage signals and enables photoreceptors to use their voltage range more effectively. Loss of the Shaker conductance attenuated the voltage signal and induced a compensatory decrease in impedance. Our results demonstrate the importance of the Shaker K+ conductance for neural coding precision and as a mechanism for selectively amplifying graded signals in neurons, and highlight the effect of compensatory mechanisms on neuronal information processing.
J. E. Niven†,M. Vähäsöyrinki‡, M. Kauranen‡, R.C. Hardie§, M. Juusola†* & M. Weckström‡
† Physiological Laboratory, University of Cambridge, Cambridge CB2 3EG, UK
‡ Department of Physical Sciences, Division of Biophysics, University of Oulu, PO Box 3000, 90014 Oulun Yliopisto, Oulu, Finland
§ Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, UK
