Coherent olfactory bulb gamma oscillations arise from coupling independent columnar oscillators.

Spike timing-based representations of sensory information depend on embedded dynamical frameworks within neuronal networks that establish the rules of local computation and interareal communication. Here, we investigated the dynamical properties of olfactory bulb circuitry in mice of both sexes using microelectrode array recordings from slice and in vivo preparations. Neurochemical activation or optogenetic stimulation of sensory afferents evoked persistent gamma oscillations in the local field potential. These oscillations arose from slower, GABA(A) receptor-independent intracolumnar oscillators coupled by GABA(A)-ergic synapses into a faster, broadly coherent network oscillation. Consistent with the theoretical properties of coupled-oscillator networks, the spatial extent of zero-phase coherence was bounded in slices by the reduced density of lateral interactions. The intact in vivo network, however, exhibited long-range lateral interactions that suffice in simulation to enable zero-phase gamma coherence across the olfactory bulb. The timing of action potentials in a subset of principal neurons was phase-constrained with respect to evoked gamma oscillations. Coupled-oscillator dynamics in olfactory bulb thereby enable a common clock, robust to biological heterogeneities, that is capable of supporting gamma-band spike synchronization and phase coding across the ensemble of activated principal neurons.NEW & NOTEWORTHY Odor stimulation evokes rhythmic gamma oscillations in the field potential of the olfactory bulb, but the dynamical mechanisms governing these oscillations have remained unclear. Establishing these mechanisms is important as they determine the biophysical capacities of the bulbar circuit to, for example, maintain zero-phase coherence across a spatially extended network, or coordinate the timing of action potentials in principal neurons. These properties in turn constrain and suggest hypotheses of sensory coding.

First-Arrival Differential Counting for SPAD Array Design.

We present a novel architecture for the design of single-photon detecting arrays that captures relative intensity or timing information from a scene, rather than absolute. The proposed method for capturing relative information between pixels or groups of pixels requires very little circuitry, and thus allows for a significantly higher pixel packing factor than is possible with per-pixel TDC approaches. The inherently compressive nature of the differential measurements also reduces data throughput and lends itself to physical implementations of compressed sensing, such as Haar wavelets. We demonstrate this technique for HDR imaging and LiDAR, and describe possible future applications.

Microscopic robots with onboard digital control.

Autonomous robots-systems where mechanical actuators are guided through a series of states by information processing units to perform a predesigned function-are expected to revolutionize everything from health care to transportation. Microscopic robots are poised for a similar revolution in fields from medicine to environmental remediation. A key hurdle to developing these microscopic robots is the integration of information systems, particularly electronics fabricated at commercial foundries, with microactuators. Here, we develop such an integration process and build microscopic robots controlled by onboard complementary metal oxide semiconductor electronics. The resulting autonomous, untethered robots are 100 to 250 micrometers in size, are powered by light, and walk at speeds greater than 10 micrometers per second. In addition, we demonstrate a microscopic robot that can respond to an optical command. This work paves the way for ubiquitous autonomous microscopic robots that perform complex functions, respond to their environments, and communicate with the outside world.

Cilia metasurfaces for electronically programmable microfluidic manipulation.

Cilial pumping is a powerful strategy used by biological organisms to control and manipulate fluids at the microscale. However, despite numerous recent advances in optically, magnetically and electrically driven actuation, development of an engineered cilial platform with the potential for applications has remained difficult to realize1-6. Here we report on active metasurfaces of electronically actuated artificial cilia that can create arbitrary flow patterns in liquids near a surface. We first create voltage-actuated cilia that generate non-reciprocal motions to drive surface flows at tens of microns per second at actuation voltages of 1 volt. We then show that a cilia unit cell can locally create a range of elemental flow geometries. By combining these unit cells, we create an active cilia metasurface that can generate and switch between any desired surface flow pattern. Finally, we integrate the cilia with a light-powered complementary metal-oxide-semiconductor (CMOS) clock circuit to demonstrate wireless operation. As a proof of concept, we use this circuit to output voltage pulses with various phase delays to demonstrate improved pumping efficiency using metachronal waves. These powerful results, demonstrated experimentally and confirmed using theoretical computations, illustrate a pathway towards fine-scale microfluidic manipulation, with applications from microfluidic pumping to microrobotic locomotion.

Injectable wireless microdevices: challenges and opportunities.

In the past three decades, we have witnessed unprecedented progress in wireless implantable medical devices that can monitor physiological parameters and interface with the nervous system. These devices are beginning to transform healthcare. To provide an even more stable, safe, effective, and distributed interface, a new class of implantable devices is being developed; injectable wireless microdevices. Thanks to recent advances in micro/nanofabrication techniques and powering/communication methodologies, some wireless implantable devices are now on the scale of dust (< 0.5 mm), enabling their full injection with minimal insertion damage. Here we review state-of-the-art fully injectable microdevices, discuss their injection techniques, and address the current challenges and opportunities for future developments.

System design for inferring colony-level pollination activity through miniature bee-mounted sensors.

In digital agriculture, large-scale data acquisition and analysis can improve farm management by allowing growers to constantly monitor the state of a field. Deploying large autonomous robot teams to navigate and monitor cluttered environments, however, is difficult and costly. Here, we present methods that would allow us to leverage managed colonies of honey bees equipped with miniature flight recorders to monitor orchard pollination activity. Tracking honey bee flights can inform estimates of crop pollination, allowing growers to improve yield and resource allocation. Honey bees are adept at maneuvering complex environments and collectively pool information about nectar and pollen sources through thousands of daily flights. Additionally, colonies are present in orchards before and during bloom for many crops, as growers often rent hives to ensure successful pollination. We characterize existing Angle-Sensitive Pixels (ASPs) for use in flight recorders and calculate memory and resolution trade-offs. We further integrate ASP data into a colony foraging simulator and show how large numbers of flights refine system accuracy, using methods from robotic mapping literature. Our results indicate promising potential for such agricultural monitoring, where we leverage the superiority of social insects to sense the physical world, while providing data acquisition on par with explicitly engineered systems.

Fabrication of Injectable Micro-Scale Opto-Electronically Transduced Electrodes (MOTEs) for Physiological Monitoring.

In vivo, chronic neural recording is critical to understand the nervous system, while a tetherless, miniaturized recording unit can render such recording minimally invasive. We present a tetherless, injectable micro-scale opto-electronically transduced electrode (MOTE) that is ~60µm × 30µm × 330µm, the smallest neural recording unit to date. The MOTE consists of an AlGaAs micro-scale light emitting diode (µLED) heterogeneously integrated on top of conventional 180nm complementary metal-oxide-semiconductor (CMOS) circuit. The MOTE combines the merits of optics (AlGaAs µLED for power and data uplink), and of electronics (CMOS for signal amplification and encoding). The optical powering and communication enable the extreme scaling while the electrical circuits provide a high temporal resolution (<100µs). This paper elaborates on the heterogeneous integration in MOTEs, a topic that has been touted without much demonstration on feasibility or scalability. Based on photolithography, we demonstrate how to build heterogenous systems that are scalable as well as biologically stable - the MOTEs can function in saline water for more than six months, and in a mouse brain for two months (and counting). We also present handling/insertion techniques for users (i.e. biologists) to deploy MOTEs with little or no extra training.

Microscopic sensors using optical wireless integrated circuits.

We present a platform for parallel production of standalone, untethered electronic sensors that are truly microscopic, i.e., smaller than the resolution of the naked eye. This platform heterogeneously integrates silicon electronics and inorganic microlight emitting diodes (LEDs) into a 100-µm-scale package that is powered by and communicates with light. The devices are fabricated, packaged, and released in parallel using photolithographic techniques, resulting in ∼10,000 individual sensors per square inch. To illustrate their use, we show proof-of-concept measurements recording voltage, temperature, pressure, and conductivity in a variety of environments.

A 250 µm × 57 µm Microscale Opto-electronically Transduced Electrodes (MOTEs) for Neural Recording.

Recording neural activity in live animals in vivo with minimal tissue damage is one of the major barriers to understanding the nervous system. This paper presents the technology for a tetherless opto-electronic neural interface based on 180 nm CMOS circuits, heterogeneously integrated with an AlGaAs diode that functions as both a photovoltaic and light emitting diode. These microscale opto-electrically transduced electrodes (MOTEs) are powered by and communicate through an optical interface, simultaneously enabling high temporal-resolution electrical measurements without a tether or a bulky RF coil. The MOTE presented here is 250 µm × 57 µm, consumes 1 µW of electrical power, and is capable of capturing and encoding neural signals before transmitting the encoded signals. The measured noise floor is as low as 15 µVRMS at a 15 kHz bandwidth.

A 72 × 60 Angle-Sensitive SPAD Imaging Array for Lens-less FLIM.

We present a 72 × 60, angle-sensitive single photon avalanche diode (A-SPAD) array for lens-less 3D fluorescence lifetime imaging. An A-SPAD pixel consists of (1) a SPAD to provide precise photon arrival time where a time-resolved operation is utilized to avoid stimulus-induced saturation, and (2) integrated diffraction gratings on top of the SPAD to extract incident angles of the incoming light. The combination enables mapping of fluorescent sources with different lifetimes in 3D space down to micrometer scale. Futhermore, the chip presented herein integrates pixel-level counters to reduce output data-rate and to enable a precise timing control. The array is implemented in standard 180 nm complementary metal-oxide-semiconductor (CMOS) technology and characterized without any post-processing.

Dual light field and polarization imaging using CMOS diffractive image sensors.

In this Letter we present, to the best of our knowledge, the first integrated CMOS image sensor that can simultaneously perform light field and polarization imaging without the use of external filters or additional optical elements. Previous work has shown how photodetectors with two stacks of integrated metal gratings above them (called angle sensitive pixels) diffract light in a Talbot pattern to capture four-dimensional light fields. We show, in addition to diffractive imaging, that these gratings polarize incoming light and characterize the response of these sensors to polarization and incidence angle. Finally, we show two applications of polarization imaging: imaging stress-induced birefringence and identifying specular reflections in scenes to improve light field algorithms for these scenes.

A microscale camera using direct Fourier-domain scene capture.

We demonstrate a chip-scale (<1 mm(2)) sensor, the Planar Fourier Capture Array (PFCA), capable of imaging the far field without any off-chip optics. The PFCA consists of an array of angle-sensitive pixels manufactured in a standard semiconductor process, each of which reports one component of a spatial two-dimensional (2D) Fourier transform of the local light field. Thus, the sensor directly captures 2D Fourier transforms of scenes. The effective resolution of our prototype is approximately 400 pixels.

Light field image sensors based on the Talbot effect.

We present a pixel-scale sensor that uses the Talbot effect to detect the local intensity and incident angle of light. The sensor comprises two local diffraction gratings stacked above a photodiode. When illuminated by a plane wave, the upper grating generates a self-image at the half Talbot depth. The second grating, placed at this depth, blocks or passes light depending upon incident angle. Several such structures, tuned to different incident angles, are sufficient to extract local incident angle and intensity. Furthermore, arrays of such structures are sufficient to localize light sources in three dimensions without any additional optics.

Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission.

In the mammalian retina, complementary ON and OFF visual streams are formed at the bipolar cell dendrites, then carried to amacrine and ganglion cells via nonlinear excitatory synapses from bipolar cells. Bipolar, amacrine and ganglion cells also receive a nonlinear inhibitory input from amacrine cells. The most common form of such inhibition crosses over from the opposite visual stream: Amacrine cells carry ON inhibition to the OFF cells and carry OFF inhibition to the ON cells ("crossover inhibition"). Although these synapses are predominantly nonlinear, linear signal processing is required for computing many properties of the visual world such as average intensity across a receptive field. Linear signaling is also necessary for maintaining the distinction between brightness and contrast. It has long been known that a subset of retinal outputs provide exactly this sort of linear representation of the world; we show here that rectifying (nonlinear) synaptic currents, when combined thorough crossover inhibition can generate this linear signaling. Using simple mathematical models we show that for a large set of cases, repeated rounds of synaptic rectification without crossover inhibition can destroy information carried by those synapses. A similar circuit motif is employed in the electronics industry to compensate for transistor nonlinearities in analog circuits.

Amacrine-to-amacrine cell inhibition in the rabbit retina.

We studied the interactions between excitation and inhibition in morphologically identified amacrine cells in the light-adapted rabbit retinal slice under patch clamp. The majority of on amacrine cells received glycinergic off inhibition. About half of the off amacrine cells received glycinergic on inhibition. Neither class received any GABAergic inhibition. A minority of on, off, and on-off amacrine cells received both glycinergic on and GABAergic off inhibition. These interactions were found in cells with diverse morphologies having both wide and narrow processes that stratify in single or multiple layers of the inner plexiform layer (IPL). Most on-off amacrine cells received no inhibition and have monostratified processes confined to the middle of the IPL. The most common interaction between amacrine cells that we measured was "crossover inhibition," where off inhibits on and on inhibits off. Although the morphology of amacrine cells is diverse, the interactions between excitation and inhibition appear to be relatively limited and specific.

Inhibitory feedback shapes bipolar cell responses in the rabbit retina.

Retinal bipolar cells can be divided into on and off types based on the polarity of their response to light. Bipolar activity is further shaped by inhibitory inputs, characterized here by the events that occur immediately after the onset of a light step: 1) in most off bipolar cells, excitatory current decreased, whereas inhibitory current increased. These currents reinforced each other, enhancing the light response. 2) In about half of the on cone bipolar cells, the excitatory current increased, whereas inhibitory current decreased, also reinforcing the light response. Both of these reinforcing interactions were mediated by glycinergic inhibition. 3) In the remaining on cone bipolar cells, excitation and inhibition both increased, but inhibition was delayed so that these cells responded transiently. 4) Finally, in rod bipolar cells, excitation and inhibition both increased so that inhibition suppressed excitation, reducing the light response at all time scales. The suppressive inhibition seen in on cone and rod bipolar cells was mediated by GABA. Thus morphologically diverse bipolar cells receive only four main types of inhibitory input, and the majority of "inhibitory" inputs actually serve to enhance excitation.

Parallel processing in retinal ganglion cells: how integration of space-time patterns of excitation and inhibition form the spiking output.

Our goal was to understand how patterns of excitation and inhibition, interacting across arrays of ganglion cells in space and time, generate the spiking output pattern for each ganglion cell type. We presented the retina with a 1-s flashed square, 600 microm on a side, and measured patterns of excitation and inhibition over an 1,800-microm-wide region encompassing many ganglion cells. Excitatory patterns of on ganglion cells resembled rectified versions of the voltage patterns of on bipolar cells. Inhibitory patterns in on ganglion cells resembled the rectified versions of voltage patterns of off bipolar cells. off ganglion cells received off excitation and on inhibition. Many ganglion cells also received an additional wide field transient inhibition derived from the activity of both on and off bipolar cells. Ganglion cell spiking was suppressed in those space-time regions dominated by inhibition. We classified each ganglion cell type by correlating its space-time patterns with its dendritic morphology. These studies suggest the bipolar and amacrine cell circuitry underlying the interplay between on and off signals that generate spiking patterns in ganglion cells. They reveal a surprising synergistic interaction between excitation and inhibition in most ganglion cells.