'Perceiving invisible light through a FILCHED cortical prosthesis' by Rostyslav Sklyar

ARTICLE Received 24 Aug 2012 | Accepted 15 Jan 2013 | Published 12 Feb 2013

DOI: 10.1038/ncomms2497

1 Perceiving invisible light through a somatosensory cortical prosthesis Eric E. Thomson1,2, Rafael Carra1,w & Miguel A.L. Nicolelis1,2,3,4,5

2a 2b 2c

Sensory neuroprostheses show great potential for alleviating major sensory deﬁcits. It is not known, however, whether such devices can augment the subject’s normal perceptual range. Here we show that adult rats can learn to perceive otherwise invisible infrared light through a neuroprosthesis that couples the output of a head-mounted infrared sensor to their somatosensory cortex (S1) via intracortical microstimulation. Rats readily learn to use this new information source, and generate active exploratory strategies to discriminate among infrared signals in their environment. S1 neurons in these infrared-perceiving rats respond to both whisker deﬂection and intracortical microstimulation, suggesting that the infrared representation does not displace the original tactile representation. Hence, sensory cortical prostheses, in addition to restoring normal neurological functions, may serve to expand natural perceptual capabilities in mammals.

1 Department of Neurobiology, Duke University, Box 3209, 311 Research Drive, Bryan Research, Durham, North Carolina 27710, USA. 2 Edmond and Lily Safra International Institute for Neuroscience of Natal (ELS-IINN), Natal 01257050, Brazil. 3 Department of Biomedical Engineering, Duke University, Durham, North Carolina 27710, USA. 4 Department of Psychology and Neuroscience, Duke University, Durham, North Carolina 27710, USA. 5 Center for Neuroengineering, Duke University, Durham, North Carolina 27710, USA. w Present address: University of Sao Paulo School of Medicine, Sao Paulo 01246-000, Brazil. Correspondence and requests for materials should be addressed to M.A.L.N. (e-mail: nicoleli@neuro.duke.edu).

NATURE COMMUNICATIONS | 4:1482 | DOI: 10.1038/ncomms2497 | www.nature.com/naturecommunications

ARTICLE

NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2497

adult rats learned to navigate their IR world as if they had acquired a novel distal sensory modality. Results Behavioural performance. We initially trained six rats on a simple visual discrimination task. Rats were placed in a circular chamber that included three reward ports (Figs 1a,b). On each trial, a visible LED was activated in one of the ports, and rats were rewarded with water for poking their nose in that port. Once they reached criterion on this task (70% correct, after 25±5 days (mean±s.e.m.)), we surgically afﬁxed an IR detector to the rat’s head, and implanted stimulating microelectrodes in the whisker region of S1 cortex (Figs 1c,d). After this surgical procedure, we returned the animals to the same chamber, where they had to learn to perform the same task using IR light, which is invisible to rats (see Methods for details on the task and training)11. To allow the rats to perceive IR light levels, the value of the IR detector output was converted into a pattern of electrical stimulation in S1, with stimulation frequency updated every 50 ms depending on the IR intensity detected (Fig. 1d). Electrical stimulation frequency increased as rats approached, or oriented their heads toward, an IR source (see Supplementary Movie 1). Note that such electrical stimulation in S1 is known to induce some type of tactile sensation in humans12 and monkeys13. It took 26±6 days for all six implanted rats to learn to discriminate among the IR sources at or above the criterion used in the initial visual task (470% correct). While training with their new IR gear, rats underwent clear changes in behavioural strategy.

Port 1 IR LED

Port 2

IR detector

Water port

Visible LED

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Frequency (Hz)

IR level (v)

ost sensory neuroprosthetic systems aim to restore function within the same modality as a pre-existing sensory deﬁcit. For instance, cochlear implants restore auditory function1, and stimulation along the visual pathway can restore visual function2,3. In some cases, however, it might be necessary to augment, rather than simply restore, the usual function of a sensory area4,5. For instance, in people that suffer permanent damage to the visual cortex, we might ask the somatosensory cortex to take over some of the roles of the visual system. Such cross-modal plasticity has been demonstrated in juvenile animals6–8. For example, rewiring experiments in newborn ferrets have shown that when visual inputs are rerouted to the auditory cortex, the auditory cortex acquires many anatomical and functional properties of the visual cortex7,8, and even mediates visually guided behaviour8. Such results suggest that the function of a primary sensory area can dramatically change depending on the type of input it receives from the environment9,10. To date, however, the literature lacks a clear demonstration of such functional plasticity in normal adult mammals. This would require that the adult brain be plastic enough to extract novel information embedded within pre-existing representations, and use this information to generate appropriate behaviours. In the present study, we test whether adult rats can incorporate a novel sensory modality into their perceptual repertoire. Speciﬁcally, we examined whether adult rats could learn to discriminate among infrared (IR) sources after we coupled the output of a head-mounted IR detector to electrical microstimulators in the whisker representation of S1. We discovered that, after training with this sensory prosthetic device,

0 IR level

Time (s)

Figure 1 | Methods. (a) Set-up of the IR behaviour chamber. Three reward ports line the walls of the circular chamber. The proximity of the ports to one another is indicated by the angle y. The rat has an IR detector (red) affixed to its head, and the cone emanating from the detector represents the area within which it will respond to IR stimuli. The red lines emanating from port 3 represent the IR signal emitted from that IR source. (b) Arrangement of each reward port, which includes a recess with a water spout, an IR LED above, and a broad-spectrum visible LED below. (c) Design of stimulating electrodes (see Methods for details). The inset shows how each stimulating electrode pair is configured in the array (scale bar, 300 mm). (d) Example of electrode placement. Cytochrome oxidase-stained barrel field shows the location of four stimulating electrodes. Each penetration is indicated with a red asterisk. Reference line: 500 mm. (e) Coupling IR levels with ICMS. On each trial, the IR light turns on, which activates the IR detector that is mounted on the rat’s head. Processing converts the detected IR level into a stimulation frequency. This value is sent to the microstimulator, which produces the desired current pulses. The inset on the right-hand-side illustrates the structure of each biphasic waveform in the pulse train. 2

NATURE COMMUNICATIONS | 4:1482 | DOI: 10.1038/ncomms2497 | www.nature.com/naturecommunications

ARTICLE

NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2497

each lasting 200 ms: unilateral whisker deflection (via air puffs), ICMS (using current magnitudes that were applied during the task) and both stimuli delivered simultaneously. S1 neurons were clearly not hijacked by ICMS, even after many months of microstimulation. In fact, most (83%) S1 neurons showed quite robust responses to whisker deflection (Fig. 3a,b). The breakdown of all response types is detailed in Fig. 3c. Briefly, of 76 units, 84% (64/76) responded to one or the other stimulus, while 16% (12/76) showed no significant response to either stimulus. The majority (83% (63/76)) showed significant responses to whisker deflection. Of these, 83% (52/63) were multimodal neurons, exhibiting significant responses to ICMS as well. Only one neuron in our sample showed a response to ICMS but not whisker deflection. Among the multimodal S1 neurons, the response to both stimuli delivered simultaneously was highly sublinear (Fig. 3d; P ¼ 4.6 10 17; two-tailed paired t-test). Population responses in S1 increased according to a saturating function of whisker deflection magnitude (Fig. 3e). Response magnitudes also increased with ICMS frequency up to 350 Hz, but dropped off at 400 Hz, likely due to adaptation (Fig. 3f). This neuronal response-profile is akin to an IR receptive-field for the range of IR stimulation frequencies employed in the task.

Discussion In 1969, Bach-y-Rita performed the classic ‘sensory substitution’ experiments, in which visual stimuli were projected onto the skin via mechanical actuators, allowing congenitally blind patients to experience a visual world for the first time4. Here we have applied the logic of sensory substitution directly to the somatosensory cortex, bypassing the body’s periphery, with the goal of building a cortical sensory prosthesis capable of augmenting the subject’s perceptual capability5. Instead of giving a binary, top–down signal instructing the rats where to move17, we connected S1 to a new graded sensory cue available in their environment, and they spontaneously adopted novel foraging behaviours in response. Note that, in principle, this experimental paradigm could use any novel stimulus (for example, magnetic or radio waves) to be represented in S1. We observed that neurons in the stimulated regions of S1 maintained their ability to respond to whisker deflection. This suggests that two different cortical representations (one tactile and one IR) became superimposed on the animal’s S1 cortex, creating a novel bimodal processing region. However, it is important to emphasize that behavioural studies will be needed to determine the consequences, for whisker-based tactile discrimination, of adding this new information to S1. The mechanisms by which animals learn to use this new information source will also be an interesting avenue for future research, as such research should suggest how to accelerate sensory prosthetic acquisition. To investigate the mechanisms of plasticity, including those theories implicating glial cells18, it will be helpful to examine functional and structural changes in cortical and subcortical tactile processing centres as rats learn to discriminate among IR sources. Overall, our behavioural results suggest that animals initially treated S1 electrical stimulation as an unexpected whisker deflection, and eventually treated it as a stimulus originating away from the body in the surrounding environment. However, we are unable, using the methods in this paper, to determine whether the fully trained rats consciously experienced microstimulation as a new distal sensory modality, or simply learned to associate a tactile sensation with an otherwise imperceptible distal sensory cue. This is a question that could presently be addressed with sensory substitution experiments in humans. Indeed, one such study suggests that some subjects experienced tactile stimuli 4

as visual in nature after training with a visual-to-tactile peripheral substitution device19. The next generation of sensory neuroprosthetics research in humans will likely continue to rely on ICMS rather than optogenetics20,21. Indeed, our experimental strategy has been quite different from optogenetic approaches22–25: instead of stimulating a specific cell-type population, we indiscriminately stimulated all S1 neurons in the vicinity of the stimulating electrodes’ tips. Despite the fact that this unusual signal was delivered at extremely high frequencies, and likely spread through most of S126–28, these animals readily learned to exploit this new sensory channel. One potential application of the technology used in this study is in the design of a new generation of motor neuroprostheses that, instead of simply sending a brain-derived motor control signal to move a prosthetic limb, would provide continuous sensory feedback to the user’s brain from the prosthesis29–31. Such closed-loop bidirectional brain–machine–brain interaction could significantly improve reaction time, behavioural accuracy and likely aid the integration of the limb into the user’s internal body image9,30,32,33. However, there is another aspect of the present work that has rarely been explored in the neuroprosthetics literature: the potential to expand or augment a species’ normal perceptual range. In that pursuit, we have implemented, as far as we can tell, the first cortical neuroprosthesis capable of expanding a species’ perceptual repertoire to include the near IR electromagnetic spectrum, which is well outside the rat photoreceptors’ spectral sensitivity. Thus, by taking advantage of this novel paradigm, our rats were able to transcend the limitation of perceiving only those stimuli that can activate their bodies’ native sensory transducers. Methods Behavioural task and training. All experiments were performed on female Long Evans rats B14-weeks-old (B250 g; Harlan Laboratories). Rats were trained in a chamber with three reward ports that were situated 90° apart (Fig. 1a). Each port was fit with a visible broad-spectrum LED, and an infrared LED (Opto Semiconductors Inc., 940 nm peak emittance (range of non-zero emissions was between 825 and 1000 nm), and IR intensity dropped to half-max at 120°) (Fig. 1a). We first trained water-deprived rats to poke in the port whose visible LED was activated. Each trial began when a visible light in one randomly selected port was activated. Rats received water when they broke the photobeam in that port (correct trials). Trials counted as incorrect when the rats poked in a different port, or did not poke at all and let the trial terminate (this was set to occur between 15 and 20 seconds after the onset of the light). On incorrect trials, they received no water, an error tone, and a longer delay to the next trial. For some rats, we delivered air puffs to the face on incorrect trials. Once animals performed above a criterion value (470% correct) 44 days in a row, we implanted an array of stimulating electrodes into S1 (Fig. 1d). The array includes an IR detector attached to the connector (see Fig. 1c and Surgery below). After the animals recovered from surgery, we determined the minimal currents required to evoke a behavioural response in at least two electrode pairs (thresholds were between 1 and 200 mA, see Stimulating Electrodes and Stimulator below for details). We then trained them in the same behavioural chamber, but incrementally replacing visible light with ICMS linked to IR levels from their detector (Fig. 1e). Initially, each trial had the same structure as trials in the initial behavioral task described above, except that the onset of the visible light was preceded by IR-level dependent stimulation (up to 400 Hz) that lasted 0.6–1.5 s. In four of six rats, we began with brief durations of stimulation (600–700 ms) to acclimate them to stimulation. In two of the rats, we started with longer stimulation durations to get estimates of behavioural latency as they learned the task (Fig. 2b). Thus the animals learned that stimulation indicated the presence of the visible light. The stimulation frequency was exponentially proportional to the IR levels (Fig. 1e). We used an exponential function because IR intensity dropped logarithmically from the IR source. We stimulated at high frequencies for two reasons: one, in preliminary experiments we found that using a lower frequency range (that is, 0–100 Hz) yielded less reliable performance; two, we wished to avoid evoking kindling seizures34. Stimulation frequencies were updated every 50 ms based on IR levels, and it took B5 ms for the stimulation frequency to actually change in the rat once the command was sent. Pulse frequency was the only variable that tracked IR levels: current amplitudes were kept the same for each pulse. Once it became clear, based on visual inspection, that the animals were comfortable with stimulation, we added ‘IR-only’ trials in which the IR-dependent

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AC@6<AD6 The sensing organs are exponentially better than any of analogous artificial ones. That is why using them in full scale is a perspective trend to the efficient (advanced) machine perception. On the other hand, limitations of sensing organs could be replaced by the perfect artificial ones with the subsequent training the nervous system on their output signals. An attempt to lay down the foundations of biosensing by natural sensors and in addition to them by the artificial transducers of physical quantities, also with their expansion into space arrays and external/implantable functioning in relation to the nervous system is performed. The advances in nanotechnology are opening the way to achieving direct electrical contact of nanoelectronic structures with electrically and electrochemically active neurocellular structures. The transmission of the sensors’ signals to a processing unit has been maintaining by an electromagnetic transistor/memristor (externally) and superconducting transducer of ionic currents (implantable). The arrays of the advanced sensors give us information about the space and direction dynamics of the signals' spreading.The measuring method and necessary performance data of the sensor for the robot’s orientation in the ambient magnetic field with living being-machine interaction in order to obtain input and output signals from brain and motor nerves to the measurement system and vice versa are introduced. The range of applied sensors differs from an induction sensor to superconducting induction magnetometer. The analytical expressions for arrangements of the head sensors in differential and vector (*D) relative positions are deduced. Sensitivity of the perception method makes it possible to recognize the linear translation of %&!) m and disposal in space of %&!* m*. Interaction between living beings and robotic equipment is given analytical treatment. KeywordsE Magnetic Field, Induction Sensor, SuFET, Nerve Impulses, Interface, Gradiometer, Sensing Area

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(78)

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(77)

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Table. The similar fragments which are highlighted in two attached articles. #

R Sklyar “Machine Perception Through Natural Intelligence”

title- Machine Perception Through Natural Intelligence

abstract- a)

Eric E. Thomson, Rafael Carra, & Miguel A.L. Nicolelis “Perceiving invisible light through a somatosensory cortical prosthesis”

title- Perceiving invisible light through a somatosensory cortical prosthesis

The sensing organs are exponentially better than any of abstract- a) Sensory neuroprostheses show great potential for alleviating analogous artificial ones. That is why using them in full scale is a perspective major sensory defcits. It is not known, however, whether such devices can augment the subject’s normal perceptual range. trend to the efficient (advanced) machine perception.

On the other hand, limitations of sensing organs could be replaced by the perfect artificial ones with the subsequent training the nervous system on their output signals.

b) Here we show that adult rats can learn to perceive otherwise invisible

infrared light through a neuroprosthesis that couples the output of a headmounted infrared sensor to their somatosensory cortex via intracortical microstimulation. c) An attempt to lay down the foundations of biosensing by natural sensors c) Hence, sensory cortical prostheses, in addition to restoring normal and in addition to them by the artificial transducers of physical quantities, neurological functions, may serve to expand natural perceptual capabilities also with their expansion into space arrays and external/implantable in mammals. functioning in relation to the nervous system is performed.

Multiprocessor data fusion is in effect intrinsically performed by animals and Such results suggest that the function of a primary sensory area can dramatically change depending on the type of input it receives from the human beings to achieve amore accurate assessment of the processing environment. [p. 2] environment. [p. 74]

Alternatively, a superconducting field-effect transistor (SuFET) based In the present study, we test whether adult rats can incorporate a novel neurotransducer (SuFETTr) with carbon nanotubes (CNT) or pickup coil (PC) sensory modality into their perceptual repertoire. [p. 2] kind of input circuit for the nerve and neuronic impulse has been designed. [p.67]

A nanoSuFET with a high-temperature superconducting channel is Note that, in principle, this experimental paradigm could use any novel introduced into the nerve fibre or brain tissue for transducing their signals in stimulus (for example, magnetic or radio waves). [p. 4] both directions. As a result, we have achieved SuFETTr that is suitable for ascertaining the variety of values. [p. 67]

The described intelligent system is introducing a new multisensor-brain interface. [p. 74]

As a result living beings control drives by previously translated biosignals. In One potential application of the technology used in this study is in the

The mechanisms by which animals learn to use this new information source will also be an interesting avenue for future research, as such research should suggest how to accelerate sensory prosthetic acquisition. [p. 4] design of a new generation of motor neuroprostheses that, instead of simply

the other variant, biosignals from organs of the senses or brain transduce directly into intelligent or robotic systems which, in such a way, pick up environmental information. [p. 72]

sending a brain-derived motor control signal to move a prosthetic limb, would provide continuous sensory feedback to the user’s brain from the prosthesis. [p. 4]

5) between both sensors and actuators a mutual flow of information exists by means of the explained human- robot interface. It is presumed that the nerve- machine interface will allow the close monitoring of flow data which are restricting to the transducing ability of a biosensor of nerve impulses [p.76]

Such closed-loop bidirectional brain–machine–brain interaction could signifcantly improve reaction time, behavioural accuracy and likely aid the integration of the limb into the user’s internal body image. [p. 4]

Fig. 16 The living being-machine interface in the biorobotic perception system. [p. 73]

3) Recent developments in bioengineering, nanotechnology, and soft However, there is another aspect of the present work that has rarely been explored in the neuroprosthetics literature: the potential to expand or computing make it possible to create a new generation of BCI. There are developing opportunities for combining natural and artificial sensing abilities augment a species’ normal perceptual range. [p. 4] in the synthesized system. [p. 75] Two directions of SuFETTr function enable decoding of these signals by comparing the result of its reaction on some process or organ with an action on them of the simulated electrical or biochemical signal after their reverse transducing through the SuFETTr(s). [p. 67]

In that pursuit, we have implemented, as far as we can tell, the frst cortical neuroprosthesis capable of expanding a species’ perceptual repertoire to include the near IR electromagnetic spectrum, which is well outside the rat photoreceptors’ spectral sensitivity. Thus, by taking advantage of this novel paradigm, our rats were able to transcend the limitation of perceiving only those stimuli that can activate their bodies’ native sensory transducers. [p. 4]