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A bioinspired flexible organic artificial afferent nerve

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Science  01 Jun 2018:
Vol. 360, Issue 6392, pp. 998-1003
DOI: 10.1126/science.aao0098
  • Fig. 1 An artificial afferent nerve system in comparison with a biological one.

    (A) A biological afferent nerve that is stimulated by pressure. Pressures applied onto mechanoreceptors change the receptor potential of each mechanoreceptor. The receptor potentials combine and initiate action potentials at the heminode. The nerve fiber forms synapses with interneurons in the spinal cord. Action potentials from multiple nerve fibers combine through synapses and contribute to information processing. (B) An artificial afferent nerve made of pressure sensors, an organic ring oscillator, and a synaptic transistor. Only one ring oscillator connected to a synaptic transistor is shown here for simplicity. However, multiple ring oscillators with clusters of pressure sensors can be connected to one synaptic transistor. The parts with the same colors in (A) and (B) correspond to each other. (C) A photograph of an artificial afferent nerve system.

  • Fig. 2 Characteristics of an artificial afferent nerve system with one branch.

    (A) Resistance of a resistive pressure sensor and the corresponding change in the supply voltage of an organic ring oscillator in response to the change of pressure. The pressure sensor and the organic ring oscillator formed a voltage divider between a dc power supply voltage and the ground (fig. S2). (B) Peaks and oscillating frequencies of output voltages of ring oscillators as a function of pressures applied to pressure sensors. (C) Peak values and oscillating frequencies of postsynaptic currents of synaptic transistors depending on pressures. The gate voltage of the synaptic transistor was supplied from the ring oscillator output. (D) Postsynaptic current output of an artificial afferent nerve for three different pressure intensities. The duration of the stimulus application was 4 s for all three cases. (E) Response to three different durations of the pressure stimulus with a constant pressure intensity of 80 kPa. (F) The peak amplitude and frequency of the postsynaptic current depending on the duration of the stimulus application for the fixed amplitude of pressure (80 kPa). All error bars in (A) to (F) show 1 SD. (i) to (iv) correspond to the signals in Fig. 1. Arrows indicate the conversion of the signals by pressure sensors, organic ring oscillators, and synaptic transistors.

  • Fig. 3 Characterization of an artificial afferent nerve system with multiple branches.

    (A) Artificial afferent nerve with two branches of ring oscillators and pressure sensors measured in (B) to (F). (B and C) Postsynaptic currents when only one pressure sensor was pressed with 20 kPa (B) and 80 kPa (C), respectively. (D) Postsynaptic current when pressures of 20 and 80 kPa were simultaneously applied to two pressure sensors. (E) Plot of the sum of currents from (B) and (C). Our synaptic transistor functions as an adder so that (D) and (E) are almost the same. (F) The amplitude of Fourier transform of the cases in (B) to (E). Frequency components corresponding to pressures are maintained after the pressure information is combined by a synaptic transistor. Each transform was done for 4 s of data and normalized to its maximum peak. (G) Artificial afferent nerve with a cluster of two pressure sensors used for movement recognition in (H) and (I). The width of electrodes was 800 μm, and the distance between the two electrodes was 400 μm. (H and I) Postsynaptic currents when an object is moved in the direction of the red arrow (H) and the direction of the blue arrow (I) in (G). (J) Portion of the connections used for braille reading in (K) and (L). Ring oscillators and synaptic transistors were connected to an array of three pixels by two pixels of pressure sensors. A synaptic transistor was connected to either one or two ring oscillators. The complete combinations of connections used are shown in fig. S17, A and B. (K) (Left) Applied pressures on the pressure sensor array. (Right) Peak frequencies of postsynaptic currents from synaptic transistors connected to only one pixel (the synaptic transistors in blue boxes in fig. S17A). The results from all the braille characters are shown in fig. S18A. (L) The smallest Victor-Purpura distance (the metric used to quantify the difference between postsynaptic currents) between the postsynaptic currents of different alphabets. The integration of signals from two pixels by synaptic transistors improves the discrimination among the braille characters.

  • Fig. 4 Hybrid reflex arc.

    (A) Discoid cockroach with an artificial afferent nerve on its back. (B) Hybrid reflex arc made of an artificial afferent nerve and a biological efferent nerve. This experimental setup was used for measurements in (D) to (F). Pressure stimuli from multiple spots can be combined by an artificial afferent nerve and can be converted into postsynaptic currents. Postsynaptic currents are amplified to stimulate biological efferent nerves and muscles to initiate movement. (C) Photograph of reference and stimulating electrodes, a detached cockroach leg, and a force gauge used for (D) to (F). The tibial flexor muscle was dissected to remove its disturbance. (D) Isometric contraction force of the tibial extensor muscle in response to pressure on the artificial afferent nerve in (B). The pressure intensity and duration were 39.8 kPa and 0.5 s, respectively. (E) Summary of the maximum isometric contraction force of the tibial extensor muscle depending on the intensities of pressures. The duration of the stimulus application was 0.5 s for all measurements. (F) Effects of the duration of the pressure stimulus on the maximum isometric contraction force of the tibial extensor muscle. The amplitude of pressure was fixed at 360 Pa.

Supplementary Materials

  • A bioinspired flexible organic artificial afferent nerve

    Yeongin Kim, Alex Chortos, Wentao Xu, Yuxin Liu, Jin Young Oh, Donghee Son, Jiheong Kang, Amir M. Foudeh, Chenxin Zhu, Yeongjun Lee, Simiao Niu, Jia Liu, Raphael Pfattner, Zhenan Bao, Tae-Woo Lee

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Supplementary Text
    • Figs. S1 to S21
    • Tables S1 and S2
    • Caption for Movie S1
    • References

    Images, Video, and Other Media

    Movie S1
    Movements of a cockroach leg in a hybrid reflex arc. The hybrid reflex arc consists of an artificial afferent nerve and a biological efferent nerve as in Fig. 4B. Postsynaptic currents from the artificial afferent nerve were amplified and connected to a detached leg of a cockroach. When we apply a pressure onto the artificial afferent nerve, the cockroach leg was actuated. Isotonic measurements were recorded. In this case, neither the tibial extensor muscle nor the tibial flexor muscle was dissected. Thus, the movements were bidirectional. The summary plots of measurement results are shown in Fig. S21.
     

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