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Cited by 42Nerve injury and regenerationNeuroscience and Neural EngineeringTissue Engineering and Regenerative Medicine

Modality-Specific Axonal Regeneration: Toward Selective Regenerative Neural Interfaces

Open access
Lotfi, Parisa, Garde, Kshitija, Chouhan, Amit K., Bengali, Ebrahim, Romero-Ortega, Mario I.·2011·Frontiers in Neuroengineering
DOI 10.3389/fneng.2011.00011PMC PMC3191531
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Abstract

Regenerative peripheral nerve interfaces have been proposed as viable alternatives for the natural control of robotic prosthetic devices. However, sensory and motor axons at the neural interface are of mixed sub-modality types, which difficult the specific recording from motor axons and the eliciting of precise sensory modalities through selective stimulation. Here we evaluated the possibility of using type specific neurotrophins to preferentially entice the regeneration of defined axonal populations from transected peripheral nerves into separate compartments. Segregation of mixed sensory fibers from dorsal root ganglion neurons was evaluated in vitro by compartmentalized diffusion delivery of nerve growth factor (NGF) and neurotrophin-3 (NT-3), to preferentially entice the growth of TrkA+ nociceptive and TrkC+ proprioceptive subsets of sensory neurons, respectively. The average axon length in the NGF channel increased 2.5-fold compared to that in saline or NT-3, whereas the number of branches increased threefold in the NT-3 channels. These results were confirmed using a 3D "Y"-shaped in vitro assay showing that the arm containing NGF was able to entice a fivefold increase in axonal length of unbranched fibers. To address if such segregation can be enticed in vivo, a "Y"-shaped tubing was used to allow regeneration of the transected adult rat sciatic nerve into separate compartments filled with either NFG or NT-3. A significant increase in the number of CGRP+ pain fibers were attracted toward the sural nerve, while N-52+ large-diameter axons were observed in the tibial and NT-3 compartments. This study demonstrates the guided enrichment of sensory axons in specific regenerative chambers, and supports the notion that neurotrophic factors can be used to segregate sensory and perhaps motor axons in separate peripheral interfaces.

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Crossref · 10.3389/fneng.2011.00011

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  • By delivering growth factors that target distinct neural populations, it might eventually be possible to guide different fiber populations to specific electrodes.

    “By delivering growth factors that target distinct neural populations (e.g., tactile and proprioceptive), it might even be possible to eventually guide different fiber populations to specific electrodes (Lotfi et al., 2011).”

    From Biomimetic approaches to bionic touch through a peripheral nerve interface (2015) · cites this paper as Lotfi et al., 2011

    The Introduction says neuron-specific growth factors could guide axons to compartmentalized electrodes, and identifies NT-3 as promoting proprioceptive axon growth. It identifies NGF as targeting pain fibers, however, and does not show a growth factor guiding tactile fibers to electrodes. The proposed electrode targeting is a future possibility, not a demonstrated result. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Cuff electrodes can be inserted into the gap of a nerve lesion and the nerve allowed to grow through it, rather than wrapping the cuff around a healthy nerve.

    “Cuff electrodes can be inserted into the gap of a nerve lesion and the nerve allowed to grow through it, rather than wrapping the cuff around a healthy nerve (Lotfi et al., 2011; Stoyanova et al., 2013; Thompson et al., 2015).”

    From Foreign Body Reaction to Implanted Biomaterials and Its Impact in Nerve Neuroprosthetics (2021) · cites this paper as Lotfi et al., 2011

    The Discussion (page unavailable) describes a regenerative interface placed between the transected ends of a repaired nerve, supporting the nerve-gap aspect. But it identifies that interface as a REMI and describes cuff electrodes separately as extraneural; it does not say that a cuff is placed in the gap for the nerve to grow through. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Lotfi et al. results indicated preferential neurite outgrowth of subtypes of neurons toward the expected target locations, providing proof-of-concept support for selective neuronal regeneration.

    “The results presented indicated preferential neurite outgrowth of subtypes of neurons toward the expected target locations, providing a proof-of-concept support for this type of approach.”

    From Regenerative Electrode Interfaces for Neural Prostheses. (2016) · cites this paper as [34]

  • Microchannel-based devices guide regenerating axons and parcel outgrowth toward distinct target locations.

    “Microchannel-based devices guide regenerating axons and parcel outgrowth toward distinct target locations.”

    From Regenerative Electrode Interfaces for Neural Prostheses. (2016) · cites this paper as [34]

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Research works printed but not linked: 2

  1. [1]1. Benvenuto, A., Raspopovic, S., Hoff- mann, K. P., Carpaneto, J., Cavallo, G., Di Pino, G., Guglielmelli, E., Rossini, L., Rossini, P. M., Tombini, M., and Micera, S. (2010). Intrafas- cicular thin-film multichannel elec- trodes for sensory feedback: evi- dences on a human amputee. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2010, 1800-1803.
  2. [12]12. Dario, P., Garzella, P., Toro, M., Micera, S., Alavi, M., Meyer, U., Valder- rama, E., Sebatiani, L., Ghelarducci, B., Mazzoni, C., and Pastacaldi, P. (1998). Neural interfaces for regen- erated nerve stimulation and record- ing. IEEE Trans. Rehabil. Eng. 6, 353-363.

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Related

Authors
Lotfi, P., Garde, K., Chouhan, A. K., Bengali, E., & Romero-Ortega, M. I.
Affiliations
The University of Texas at Arlington (US)
ORCID
Venue
Frontiers in Neuroengineering
Publisher
Frontiers Media SA
Published
2011
Volume
4
Pages
11-11
ISSN
1662-6443 (ISSN-L)
DOI
10.3389/fneng.2011.00011
PMC
PMC3191531
OpenAlex
W2070918313
Cited by
42
References
62
Citations by year
2026: 1 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 1 · 2017: 6 · 2016: 1 · 2015: 7 · 2014: 2 · 2013: 3 · 2012: 5
FWCI
1.33
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Neuroengineering (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Defense Advanced Research Projects Agency
  • Advanced Research Projects Agency
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
Keywords
axon regeneration, peripheral nerve regeneration, nerve growth factor, neurotrophin-3, TrkA, TrkC, nociceptors, proprioceptive sensory neurons, dorsal root ganglia, sciatic nerve transection, calcitonin gene-related peptide, axon branching

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