A bionic self-driven retinomorphic eye with ionogel photosynaptic retina

Bioinspired bionic eyes should be self-driving, repairable and conformal to arbitrary geometries. Such eye would enable wide-field detection and efficient visual signal processing without requiring external energy, along with retinal transplantation by replacing dysfunctional photoreceptors with healthy ones for vision restoration. A variety of artificial eyes have been constructed with hemispherical silicon, perovskite and heterostructure photoreceptors, but creating zero-powered retinomorphic system with transplantable conformal features remains elusive. By combining neuromorphic principle with retinal and ionoelastomer engineering, we demonstrate a self-driven hemispherical retinomorphic eye with elastomeric retina made of ionogel heterojunction as photoreceptors. The receptor driven by photothermoelectric effect shows photoperception with broadband light detection (365 to 970 nm), wide field-of-view (180°) and photosynaptic (paired-pulse facilitation index, 153%) behaviors for biosimilar visual learning. The retinal photoreceptors are transplantable and conformal to any complex surface, enabling visual restoration for dynamic optical imaging and motion tracking.


performance.
The observed photoresponse appears somewhat slower compared to conventional photodetectors.It would be insightful if the authors could discuss and provide comments regarding this aspect.
Concerning the second claim related to photothermoelectric properties, there are reservations about the system's practical applicability.The skepticism stems from the notable challenges associated with temperature control in numerous scenarios.
The manuscript lacks the presentation of operational schemes (passive or active matrix operation), which impedes the visualization and understanding of the system's practical functioning.
In the introduction, there seems to be a misunderstanding concerning animal eyes.For example, stating that most biological eyes possess a hemispherical retina with widespectrum perception appears inaccurate.A more nuanced explanation might refer to 'photoreceptor arrays in a curved form.'Furthermore, the term 'wide spectrum perception' seems ambiguous, as the spectral range varies significantly across different species.

Response to the reviewers
Reviewer #1: In this work by X. Luo et al., a self-powered bionic retinomorphic eye is developed using selective photosensitive polypyrrole nanoparticles (PPy-NPs) doping of ionogel pillar.The results demonstrate the capability of the flexible and stretchable device of neuroelectric plasticity.The study is promising for future self-powered photo-synaptic devices.
While the results are scientifically sound and of interest to the readers of Nature Comm., there are several concerns that require addressing before the paper can be considered for publication: Comment 1: Several previous studies have explored self-powered synapses.It would be interesting to the readers to add more details about them in the introduction and a table to compare the performance and capabilities as well as the self-powering mechanism.
Response 1: We greatly appreciate for your valuable suggestion.In recent years, self-powered photosynapses have attracted increasing attention due to their great potential in ultralow-power neuromorphic vision technologies.Up to now, several self-powered photosynapses have been constructed through different mechanisms, as shown in Table R1.It is found that the prevailing self-powered synaptic mechanisms predominantly exploit photovoltaic effects.In comparsion, from the perspective of mechansim, our approach is marked by the pioneering utilization of the photothermoelectric principle, while previous self-powered photosynapses are mostly realized by photovoltic effect.From the perspective of performances, our heterojunction ionogel not only manifests an exceptionally broad photoresponse range but also demonstrates outstanding performance with flexible and self-healable properties.Moreover, to the best of our knowlege, ionogel heterostructure in our work is reported firstly for neuromorphic vision.The Table R1 has been added as Table 1 in the revised supporting information and the comparasion has been described in the revised manuscript.

Changes in the revised manuscript:
In the introduction part, we have added the following sentences in the revised manuscript: "Recently, artificial eyes based on self-powered photosynapses have been constructed, the photoreceptors exhibit a limited light response range........insufficient flexibility".(Page 3, Line 47-50)."which is different from the previous self-powered optical synapses induced by photovoltaic effects (Supplementary Table S1)," (Page 4, Line 68-69).
Comment 2: What incident power is used in fig.2a?
Response 2: Thank you for your careful review.The optical power density used in fig.2a is 7.2 μW/mm 2 .The data also has been added in the revised manuscript (Page 5, Line 94).

Changes in the revised manuscript:
In the main text, we have added the incident power in the revised manuscript: "The optical power density used in fig.2a is 7.2 μW/mm 2 " (Page 5, Line 94).
of short-range plasticity in optical synapses.Based on previous literatures, the majority of two-terminal self-powered optical synapses only exhibit a single form of short synaptic plasticity due to their unidirectional responses to optical stimuli (Nat. Commun. 2023, 14, 1972;Adv. Sci. 2022, 9, 2103494;ACS Appl. Electron. Mater. 2023, 5, 3403), which are constent with our results.Notebly, only a few studies have demonstrated the presence of both PPF and PPD capabilities in photosynapses owing to the bidirectional responses to light stimuli with different wavelengths (Adv. Mater. Technol., 2023, 8, 2201779).The manifestation of these capabilities mostly rely on the optical properties of photoresponsive matter.In our study, the photosensitive materials exhibit the positive response across the entire absorption spectrum, ensuring that our device demonstrates PPF synaptic behavior without requiring an external voltage.Based on our experience and understanding, for these two-terminal self-powered photosynapse devices, it is possible to obtain the PPD function unless an external voltage is applied.However, this power loading normally results in an escalation of dark current, thereby exerting a discernible negative influence on the photoresposibility and PPF index of the device.Therefore, how to design and fabricate the self-powered photosynapse with bidirectional modulation is highly desible and interesting, thanks for your valuable comments.

Changes in the revised manuscript:
In the main text, we have added the fitting formula for the PPF calculation in the revised manuscript: "(  =  0 +  1  −  1 ⁄ +  2  −  2 ⁄ )".(Page 8, Line 154-155).At 530 nm, thermionic electron emission dominates due to the low ligh absorption and higher photon energy (Figure R1a), while at a wavelength of 625 nm, it is primarily driven by the photothermal effect induced by PPy-NPs induced temperature gradients.While the absorption of PPy-gel in Fig. R1b exhibits higher absorption at 625 nm, indicating comparable light responses within both wavelength ranges.R3 (also see Supplementary Fig. 10c), the results show an increase in post-synaptic current and an augmentation in synaptic weights with repeated optical pulses.
Notably, each subsequent stimulation resulted in a progressively extended forgetting duration.
These observed trends in synaptic weight changes align with our previous findings.This phenomenon bears resemblance to the well-known Ebbinghaus forgetting curve often observed in biological vision.
Comment 7: Please elaborate on the ion migration and charge movement mechanism during potentiation and depression under different wavelengths of light to make it clearer to the reader.
Response 7: Thank you for your comment.The ion migration process can be described in detail as follows: In the wavelength range of 585 nm to 970 nm, the dominating factor is the photothermal effect of PPy-NPs.This effect leads to an increase in temperature on the side of the doped PPy-NPs gel due to thermal gradients (see Figure R1b).The temperature difference facilitates the migration of ions towards the undoped side, resulting in the rapid accumulation of positive charges due to the small size of Li+ ions.In the wavelength range of 365 nm to 585 nm, the thermionic effect becomes prominent due to the exceptional UV light absorption of the silver nanoparticle paste used as contact electrodes.This effect causes a significant generation of thermoelectrons on the side of the undoped ionogel (see Figure R1a and c).As a result of Comment 8: The authors claim developing a flexible and stretchable device, however, there is no data related to the stretching capability of the device.Please show the the maximum stretching capability as well as cycling tests to confirm that the device can sustain multiple stretching cycles and thus its reliability as a physically compliant device.
Response 8: Thanks for reviewer's professional comment.We have conducted the tensile and cycling test of the ionogel junction device.As shown in Figure R4a, the ionogel heterojunction exhibits a stretching capability of approximately 180%, which effectively satisfies various application requirments.The stress-strain cycling curves almost overlap with its initial state even after undergoing 200 loadings at a stretch of 50%, indicating its reliable stability (Figure R4b).Meanwhile, the corresponding test data and relevant testing method have been added in the revised supplement information as Supplementary Fig. 11.dimentions, the downscaled device still exhibits photoresponse, the intensity of photocurrent is lower than that of the original device.However, due to the constraints inherent in our present functional materials and fabrication processes, the downscaled sample show a reduced yield.
Failure to accomplish this integration results in reduced yields of salable devices, and therefore increased manufacturing costs.Thus, process integration is one of the biggest manufacturing challenges for realization of large-scale and high density production of downscaled ionogel devices.In the next step, we will develope advanced fabrication techniques into the overall process for high density device manufacture.Reviewer #2: This manuscript introduces a self-driven hemispherical retinomorphic eye (SHR-E) with an elastomeric retina, utilizing ionogel heterojunctions as photoreceptors.
However, several critical aspects need more explicit clarification: Comment 1: The primary claim of this research focuses on 'self-driven' photodetection.
However, it is essential to note that conventional silicon photodetectors also operate at zero operational voltage, and some photodetectors with heterostructures exhibit maximum photoresponse at zero voltage.
Response 1: Thanks for your insightful comment.The previous studies have demonstrated that the conventional silicon or silicon heterostructures-based photodetectors exhibit exceptional photoresponse even at zero voltage (Nature Photonics, 2020, 7, 578-584;Small, 2021, 17, 2100439).In comparison with those silicon-based photodetectors, our heterojunction ionogel photoreceptor exhibits more unique properties, such as high flexibility, self-healing capabilities and excellent conformalability.Meanwhile, the ionogel photoreceptor could be fabricated by solution process method.These characteristics offer significant potential applications in various scenarios, such as humanoid robots and flexible electronics.
Comment 2: It would be beneficial if the authors could display the I-V curves at various light intensity levels to provide a more comprehensive understanding of the device's performance.
Response 2: We greatly appreciate for your valuable suggestion.In order to characterize the current-voltage (I-V) behavior, we performed additional experiments involving current-voltage measurement at different light intensities.As shown in Figure R6, by applying an external voltage, the current values are in the microampere range, which is significantly higher than the nanoampere level observed for photoresponse current in the self-driven mode (see Figure 2a).
Therefore, with the help of power supply, the I-V curves exhibited minimal variation under light exposure at different light intensities.Response 3: Thanks for your professional comment.As an emerging functional material, ionogel exhibit distinct ion conduction mechanism compared to the electron conduction in traditional materials.The conductive property of ionogels normally relies on the migration of ion, which differs from electron migration due to the substantial disparities in volume and mass between ions and electrons (Science 2022, 376, 502-507;Nat. Commun. 2019, 10, 1171).
Consequently, ionic charges exhibit much slower migration speeds than electron charges under equivalent kinetic energy conditions, thereby leading to slower photoresponse compared to conventional photodetectors.We have dicussed this aspect in Page 5, Line 96-98.
Comment 4: Concerning the second claim related to photothermoelectric properties, there are reservations about the system's practical applicability.The skepticism stems from the notable challenges associated with temperature control in numerous scenarios.Changes in the revised manuscript: We have added the following senstence in the revised manscript: "Furthermore, temperature-dependent photocurrent behaviors are observed in our heterostructure (Supplementary Fig. 8).The EPSC is more sensitive to high temperature due to the enhanced activity and accelerated migration rate of ions within the gel at elevated temperature."(Page 6, Line 126-129).
Response 5: Thanks for your invaluable comment.We have made a modification and additions to Methods parts of the manuscript.
Changes in the revised manuscript: In the Method part of revised manuscript, we have made a modification to Visualization system as following: "The experimental visualization setup includes a transimpedance amplifier (TIA), a Beijing Altech USB5631-D data acquisition card, a multi-circuit power supply, a laptop computer, and a Labview program.Supplementary Figure 12 provides a schematic of the system.The power supply in this setup is utilized exclusively for operating the TIA and data acquisition card, while an external power source projects optical pattern onto the array by illuminating a mask with light.A 5x5 array of devices is integrated with a custom printed circuit board (PCB).The data from the 25 pixels is transmitted through the PCB to the TIA for current amplification.The amplified signal is then captured by the data acquisition card and relayed to the computer for visualization.The operation of the data acquisition card and the visualization of the data are managed using Labview software." Comment 6: In the introduction, there seems to be a misunderstanding concerning animal eyes.
For example, stating that most biological eyes possess a hemispherical retina with wide-spectrum perception appears inaccurate.A more nuanced explanation might refer to 'photoreceptor arrays in a curved form.'Furthermore, the term 'wide spectrum perception' seems ambiguous, as the spectral range varies significantly across different species.
Response 6: Thanks for your careful checks and suggestion.According to your suggestion, we have changed the following sentence "most biological eyes possess a hemispherical retina with wide-spectrum perception appears inaccurate" into "most biological eyes possess photoreceptor arrays in a curved form with broadband photoperception".The changes have been highlighted in the revised manuscript.
Changes in the revised manuscript: In the introduction part of revised manuscript, we have made a modification to the relevant discribtion as following: "most biological eyes possess photoreceptor arrays in a curved form with broadband photoperception". in Page 2, Line37-38.
The authors have thoroughly and successfully answered the reviewers' comments and conducted the necessary experiments to address the provided comments.The paper can now be recommended for publication.
Reviewer #2 (Remarks to the Author): I remain cautious about current research in self-driven photodetection.For example, the authors present IV curves under varying lighting conditions, but these curves exhibit linear characteristics that hinder distinct signal differentiation.Notably, minor voltage fluctuations can cause significant changes in photocurrent, even without an increase in light exposure.
Furthermore, the current level merges at a high voltage level, rendering it unsuitable for use as a photodetector.Recently, devices under the names 'bionic eye' or 'neuromorphic devices' have been reported in various forms.Although these devices incorporate multiple characteristics and functionalities, I believe that maintaining at least the basic properties at an appropriate level is essential for the research to hold value.

Reviewer #3 (Remarks to the Author):
The work reports the self-driven ionogel based photoreceptors for artificial retina.
Compositing the polypyrrole nanoparticles (PPy-NPs) into an ionogel induces the self-driven potential due to combination of photothermal effect from PPy-NPs and thermoelectric effect from ionogel.The idea looks interesting but the mechanism of the EPSC needs to be explained in more detail.It is recommended for major revision.Here are the comments for the improvement.
1. Photothermal effects due to PPy-NPs are important in generating photothermal effect.To induce the thermoelectric effect, the spatial gradient of temperature (delta T(x)) is expected to play an important role.Therefore, the authors should explain the source of the EPSC and self-driven potential in more detail with a drawing of heterojunction structure (Fig. 1c).
2. The change in the EPSC with light exposure conditions is assumed to be related to thermoelectric effect.The EPSC is measured across the ionogel.The detailed direction of ion migration, the direction of generated potential and their effect of ionic current should be explained in detail.
3. Was the EPSC the short-circuit current?In my opinion, it is required to measure the opencircuit voltage and short-circuit current to prove that the mechanism of the device is due to thermoelectric effect.The authors should also specify the source of current and how it was measured.4. The authors mentioned that the mechanism is different from the photovoltaic effect.The explanation should be detailed in conjunction with the mechanism explanation.5.There are some minor errors.For example, In Fig. 1a, "Cynapse" should be changed to"Synapse".Response: Thanks for your comment.A self-driven or self-powered photodetector, as a new type of photodetectors, enables photodetection without the external power, has attracted great attention recently (Nature, 2023, 616, 712;Nat. Commun., 2023, 14, 1972;Adv. Funct. Mater., 2021, 31, 2011284).Compared to conventional photodetectors, the optoelectronic synapses can detect and memorize the optical signals simultaneously, thus enabling the implementation of a biological vision and an optogenetic neural network (Nat. Nano., 14, 776, 2019;Nat. Nano., 17, 27, 2022).In our study, the ionogel heterojunction device exhibits self-driven optoelectronic synapse function, which can convent light signals into electric signals and process the signals with the synaptic weight without any external power requirements.With the help of light exposure, the ionogel heterojunction generates a temperature gradient between pure-gel and PPygel, owing to the photothermal effect.This temperature gradient can drive thermodiffusion of mobile ions, resulting in an ion concentration gradient that produces a low electric voltage in the millivolt range.Generally, the process that converting temperature difference into electric voltage is defined as the thermoelectric effect, also known as the Soret effect or ionic Seebeck effect (Science 2020(Science , 368, 1091;;Sci. Adv., 2022, 8, eabq8432).Therefore, our heterojunction device is considered as a self-driven photosynapse instead of photodetection.To understand the I-V behaviors of heterojunction device under an applied voltage (It is noted that we don't need the applied external voltage in our manuscript), here we conducted the current-voltage measurement experiment again under varying light intensities (Fig. R1), the results is very similar to that in the first revision.A plausible explanation for this phenomenon is illustrated as follows: The heterogel normally acts as an ionic conductive material, wherein a temperature gradient within the heterogel induces ion migration from hot side to cold side in absence of external voltage.This thermodiffusion process generates ionic current, with an order of nA.However, when an external large voltage is applied, ion movement driven by electric field becomes dominant, with an order of μA.Therefore, it can be concluded that the ion movement driven by photothermal effect plays a subordinate role during the applied voltage.As a result, when an external voltage is introduced, no appreciable changes in current are seen under varing light illumination., 2023, 35, 2209004;Adv. Funct. Mater., 2022, 32, 2207713).In contrast to conventional Email: iamjqliu@njtech.edu.cnsemiconductor materials that employ electrons and holes as charge carriers, ion gels represent a novel conductor utilizing ions as transport carriers.The dark current of ion gels surges with increasing bias voltage.Therefore, testing the device at low voltage is necessary to achieve low dark current levels.Our device can be tested at zero bias voltage which not only conserves energy but also yields minimal dark current while enhancing optical responsiveness.

Comment 4 :Response 4 :
photodetector.Here the silver paste's nanoparticles exhibit exceptional UV-Vis light absorption and generate a broadband photoelectric response through synergistic action.The photon energy absorbed by silver nanoparticles can releases numerous electrons into the electrolyte, creating an electron-rich region on ionogel side that attracts Li + migration (asymmetric light absorption).

Figure R4 .
Figure R4.The mechanical property of heterojunction ionogel.(a) Tensile stress-strain curve for heterojunction ionogel.Inset: Photograph of original state and maximum strain state.(b) Cyclic stress-strain curves at a fixed strain of 50%.

Professor
Figure R5.The scalability of the ionogel device.a-b, Photograph of a 10×10 device array at 1cm×1cm area and its photocurrent response under UV excitation.c-d, Photograph of a 5×5 device array at 1cm×1cm area and its photocurrent response under UV excitation.

Figure R6 .
Figure R6.I-V curves of the device under 365 nm light irradiation with different intensity.

Response 4 :
We appreciate your comment.To explore the influence of temperature on device performance.Our study involved comprehensive testing of the device's tolerance and response characteristics across different temperature ranges.Specifically, we conducted additional experiments at environmental temperatures of 20 ℃, 30 ℃, and 40 ℃.As shown in FigureR7, temperature-dependent photocurrent behaviors were observed.With the temperature increase, their corresponding ESPC value also enhance.The observed phenomenon can be attributed to the enhanced activity of ions within the gel at the elevated temperature, thereby leading to an accelerated migration rate.

Fig. R1 .
Fig. R1.I-V curves of device under 365 nm light irradiation with different intensity at 0-5 V

Fig. R2 .
Fig. R2.Signal-to-noise ratio curves of the device at different voltages.

Table R1 .
The comparison of self-powered optical synapses.