Self-sustained green neuromorphic interfaces

The study addresses the challenge of integrating sensing and computation in neuromorphic interfaces due to inherent amplitude mismatch between environmental/physiological signals and the higher driving voltages typically required by memristive devices. While biosystems operate with ultralow-amplitude action potentials (~50–120 mV), most sensors and neuromorphic elements require external power or amplification, limiting compactness, flexibility, and applicability to low-amplitude stimuli. The research question is whether neuromorphic interfaces can be designed to process bio-level signals directly and be self-sustained by harvesting ubiquitous environmental energy. The authors propose leveraging microbially produced protein nanowires to (1) realize memristors that switch at sub-100 mV, (2) harvest electrical energy from ambient humidity, and (3) function as sensing elements, enabling green, flexible, and reconfigurable neuromorphic systems that close the gap to biological integration.

Prior works on neuromorphic electronics and artificial afferent systems have demonstrated memristor-based processing and sensor-driven neuromorphic responses, including devices powered by mechanical or thermoelectric generators. However, these systems often require external energy inputs, specialized sensors, or off-chip components and are limited to specific stimuli due to signal mismatch with memristor thresholds. Biological systems, in contrast, achieve unified sensing and computation through low-amplitude signaling near thermodynamic limits. Previous memristors generally required higher thresholds, and active sensors faced voltage-divider limitations when interfaced with high-resistance energy sources. Protein nanowires from Geobacter sulfurreducens have been reported to support low-voltage memristive switching, harvest energy from humidity, and serve as humidity sensors, suggesting a route to overcome these limitations and enable integrated, self-powered neuromorphic interfaces.

Device components and fabrication: Protein nanowires harvested from Geobacter sulfurreducens were purified, dialyzed against deionized water, stored at 4 °C (final pH ~9). Memristors were fabricated on 25 µm Kapton polyimide: bottom electrode Ti/Pt (3/17 nm), dielectric/top electrode stack Ti/SiO2/Ti/Ag (3/20/2/150 nm), with 20 nm SiO2 as insulator in a vertical Ag–SiO2–Pt structure embedded in ~500 nm protein nanowire film via drop-casting (50 µL/cm2, 150 µg/mL) and thermal drying (80 °C, 1 min). Planar sensors used interdigitated Ti/Au (3/30 nm) electrodes on PI with ~1 µm protein nanowire film. Vertical sensors comprised Au-coated PI electrodes sandwiching ~5 µm protein nanowire film, encapsulated by PDMS layers (~200 µm) with a humidity exposure window. Characterization: Electrical measurements were performed in ambient unless specified. I–V curves via Keysight B1500A/Agilent 4155C; sensor outputs via Keithley 2401/B1500A; RH monitored by hygrometer (REED 8706). Structural analysis via SEM (JEOL JSM-7001F) and TEM (JEOL JEM2200FS). Memristor behavior: Protein nanowire memristors showed low-power threshold switching: Vth ~65 ± 14 mV (N=117), forming-free ~60–95 mV, programming current Icc down to 0.1–10 nA, endurance ~10^4 cycles under pulsed operation, and size-independent switching indicative of filamentary electrochemical metallization (Ag filament formation). Devices lacking protein nanowires did not achieve bio-amplitude switching. Cyclic voltammetry indicated protein nanowires facilitate Ag+/Ag redox, lowering activation conditions for filament nucleation. Mechanical flexibility: Bending tests up to 10,000 cycles (radii 4–0.1 cm) maintained ~90% yield and stable Vth (55–75 mV). Thin device stack and intrinsic flexibility of nanowires (~3 nm diameter) support wearability. Protein nanowire sensors: Vertical devices harvested continuous power from ambient humidity through a vertical moisture gradient, producing steady open-circuit voltage and short-circuit current at RH ~50% and were insensitive to bending. Planar devices produced transient spikes from rapid local RH changes (e.g., breathing) with negligible bending influence. Estimated power outputs (non-optimized): vertical steady ~40 nW/cm2; planar transient 10 nW/cm2. Neuromorphic interfaces—amplitude domain: The vertical energy harvester was paired with a load resistor RL to form an active humidity sensor whose output Vio depended on internal resistance Ri of the protein nanowire film; Vio increased from <30 mV to >100 mV as RH rose 50→60% due to Ri decrease. This drove an artificial neuron comprising a protein nanowire memristor (M) and capacitor Cm (membrane capacitance analog). On dry skin (RH<50%) Vio charged Cm to Vm<10 mV; on sweating skin (RH90%), Vm rose and at ~40 mV triggered memristor turn-on and rapid Cm discharge, producing spiking akin to action potentials. The vertical harvester also powered multifunctional interfaces by combining with passive sensors: a resistive pressure sensor (tactile receptor) and a passive optical sensor, converting stimulus-induced resistance changes into active Vio across RL, charging Cm and eliciting neuronal firing. Neuromorphic interfaces—frequency domain: A wearable integration used a compact planar protein nanowire sensor (~0.3 cm2) to convert respiration into spikes and fed an artificial neuron (M + 10 µF Cm) with a backend LED driver (Op Amp LM321; R1/R2/R3/R4=20/1/100/1 kΩ). A memristor model (Supplementary) simulated responses: at 0.3 Hz (normal), inter-breath intervals allowed discharge, keeping Vm ~15 mV below Vth and no firing; at 1 Hz (abnormal), reduced discharge raised Vm toward Vth, triggering firings. Experiments matched simulations: normal breathing yielded Vm<30 mV and no spikes; fast breathing (1 Hz) produced Vm40 mV and spikes that lit an LED. Reconfigurability: Protein nanowire films can be dissolved under basic conditions (increased solubility at higher pH) and re-deposited, enabling repeated activation/deactivation of memristive function in the same device without altering bio-amplitude switching. A reconfigurable artificial neuron connected six bare Ag–SiO2–Pt structures in series/parallel paths; selectively depositing protein nanowires on different lines tuned firing threshold: path 1 ~50 mV, path 2 ~120 mV, path 3 ~200 mV. Sensors were similarly reconfigurable; output can also be tuned via protein nanowire thickness. Stability and passivation: Protein nanowires exhibit robustness across pH 2–10, detergents, organic solvents, and elevated temperature; thin-film devices maintain performance for months in ambient. Ag electrode oxidation can degrade memristor stability; adding a protective layer (e.g., Pt) improves ambient stability. PDMS-passivated protein nanowire memristors preserved bio-amplitude function in water.

• Protein nanowire memristors operate at bio-amplitudes: threshold voltage Vth = 65 ± 14 mV (N=117) with programming currents as low as 0.1–10 nA, and endurance of ~10^4 cycles; forming-free operation ~60–95 mV; lowest programming power among similar devices (<1 nW).
• Switching mechanism is electrochemical metallization (Ag filament) facilitated by protein nanowires’ ability to promote Ag+/Ag redox; devices without protein nanowires do not show bio-amplitude switching.
• Flexible robustness: ~90% yield and stable Vth (55–75 mV) after 10,000 bending cycles; negligible performance change under radii from 4 to 0.1 cm.
• Protein nanowire sensors harvest/use humidity: vertical devices provide continuous output (~40 nW/cm2) insensitive to bending; planar devices yield respiration-induced spikes (~10 nW/cm2 transient), both sufficient to drive bio-amplitude memristors.
• Self-sustained neuromorphic interfaces: humidity-driven artificial afferent circuit transduces RH changes (e.g., sweating) into action-potential-like spikes (Vm threshold ~40 mV) without external power.
• Multifunctionality via energy harvester + passive sensors: tactile and optical interfaces convert passive sensor resistance changes into active voltages that charge Cm and elicit neuronal firing.
• Frequency-selective processing in a wearable: normal breathing (0.3 Hz) yields Vm ~15–30 mV and no firing; abnormal breathing (1 Hz) raises Vm ~40 mV, triggering spikes and LED alert, matching circuit simulations.
• Reconfigurability: reversible dissolution/re-deposition of protein nanowires enables repeated activation; tunable firing thresholds by selecting array paths—~50 mV (path 1), ~120 mV (path 2), ~200 mV (path 3).
• Stability and compatibility: protein nanowire devices show long-term ambient stability; passivation (e.g., Pt, PDMS) addresses Ag oxidation and supports operation in aqueous environments.

By matching the computation threshold to biological signal amplitudes and harvesting ubiquitous humidity for power, the interfaces overcome the fundamental signal mismatch that has required external power or pre-amplification in prior systems. Protein nanowires uniquely unify sensing, energy harvesting, and low-voltage switching, enabling compact, flexible, and self-sustained neuromorphic interfaces. Demonstrations across amplitude and frequency domains show biologically analogous afferent processing: continuous humidity sensing leading to neuronal firing, multimodal (tactile and optical) perception using the same power source, and respiration-rate detection with frequency-dependent decision-making. The capacity for reconfiguration via simple material exchange allows personalization and adaptation to different physiological signal strengths or frequencies. These capabilities advance neuromorphic biointegration and reduce system complexity and energy demands compared to conventional approaches.

The work introduces fully self-sustained, green neuromorphic interfaces that directly process bio-level signals using protein nanowire-enabled devices. Key contributions include: (1) bio-amplitude memristors with sub-100 mV thresholds and nA-level programming, (2) ambient humidity-powered sensors providing continuous and spiking signals, (3) integrated, multifunctional afferent circuits for humidity, tactile, and optical stimuli, (4) wearable respiration monitoring with frequency-based decision and on-board actuation, and (5) simple reconfigurability to tune neuronal thresholds and sensor outputs. The protein nanowire platform offers sustainable, biocompatible materials with promising stability and modifiability. Future research should elucidate the molecular mechanisms of redox facilitation in switching, optimize energy harvester and sensor architectures for higher power density and selectivity, systematically evaluate long-term biocompatibility and in vivo stability, develop robust passivation for tissue interfaces, and expand to additional neuromorphic functions and modalities for IoT and biomedical applications.

• Mechanistic understanding: The facilitation of Ag+/Ag redox and filament formation by protein nanowires is inferred but requires deeper molecular-level investigation.
• Stability constraints: Ag electrode oxidation can degrade memristor stability under ambient conditions; protective layers (e.g., Pt) are needed to ensure long-term operation.
• Environmental dependence: Energy harvesting and some sensing rely on ambient humidity; performance may vary with environmental conditions and has not been optimized for maximum power output.
• Biocompatibility/in vivo validation: While protein composition suggests compatibility and PDMS passivation supports aqueous operation, comprehensive biocompatibility, immunogenicity, and long-term in vivo stability studies remain to be done.
• Generalizability: Demonstrations are proof-of-concept with limited device scale and specific stimuli; broader scalability, durability under real-world wear, and multimodal interference effects require further assessment.