Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats
Background: Vagus nerve stimulation (VNS) improves cognition in humans and rodents, but the effects of a single session of VNS on performance and plasticity are not well understood. Objective: Behavioral performance and hippocampal (HC) electrophysiology/neurotrophin expression were measured in heal...
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| Format: | Article |
| Language: | English |
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Elsevier
2022-09-01
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| Series: | Brain Stimulation |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X22001796 |
| _version_ | 1811182542085160960 |
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| author | Laura K. Olsen Raquel J. Moore Naomi A. Bechmann Victoria T. Ethridge Nathan M. Gargas Sylvia D. Cunningham Zhanpeng Kuang Joshua K. Whicker Joyce G. Rohan Candice N. Hatcher-Solis |
| author_facet | Laura K. Olsen Raquel J. Moore Naomi A. Bechmann Victoria T. Ethridge Nathan M. Gargas Sylvia D. Cunningham Zhanpeng Kuang Joshua K. Whicker Joyce G. Rohan Candice N. Hatcher-Solis |
| author_sort | Laura K. Olsen |
| collection | DOAJ |
| description | Background: Vagus nerve stimulation (VNS) improves cognition in humans and rodents, but the effects of a single session of VNS on performance and plasticity are not well understood. Objective: Behavioral performance and hippocampal (HC) electrophysiology/neurotrophin expression were measured in healthy adult rats after VNS paired training to investigate changes in cognition and synaptic plasticity. Methods: Platinum/iridium electrodes were surgically implanted around the left cervical branch of the VN of anesthetized male Sprague-Dawley rats (N = 47). VNS (100 μs biphasic pulses, 30 Hz, 0.8 mA) paired Novel Object Recognition (NOR)/Passive Avoidance Task (PAT) were assessed 24 h after training and post-mortem tissue was collected 48 h after VNS (N = 28). Electrophysiology recordings were collected using a microelectrode array system to assess functional effects on HC slices 90 min after VNS (N = 19). Sham received the same treatment without VNS and experimenters were blinded. Results: Stimulated rats exhibited improved performance in NOR (p < 0.05, n = 12) and PAT (p < 0.05, n = 14). VNS enhanced long-term potentiation (p < 0.05, n = 7–12), and spontaneous spike amplitude (p < 0.05, n = 7–12) and frequency (p < 0.05, n = 7–12) in the CA1. Immunohistochemical analysis found increased brain-derived neurotrophic factor expression in the CA1 (p < 0.05, n = 8–9) and CA2 (p < 0.01, n = 7–8). Conclusion: These findings suggest that our VNS parameters promote synaptic plasticity and target the CA1, which may mediate the positive cognitive effects of VNS. This study significantly contributes to a better understanding of VNS mediated HC synaptic plasticity, which may improve clinical utilization of VNS for cognitive enhancement. |
| first_indexed | 2024-04-11T09:32:20Z |
| format | Article |
| id | doaj.art-7a7b5be0d1b148bcba1282ec972bf680 |
| institution | Directory Open Access Journal |
| issn | 1935-861X |
| language | English |
| last_indexed | 2024-04-11T09:32:20Z |
| publishDate | 2022-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj.art-7a7b5be0d1b148bcba1282ec972bf6802022-12-22T04:31:49ZengElsevierBrain Stimulation1935-861X2022-09-0115511011110Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male ratsLaura K. Olsen0Raquel J. Moore1Naomi A. Bechmann2Victoria T. Ethridge3Nathan M. Gargas4Sylvia D. Cunningham5Zhanpeng Kuang6Joshua K. Whicker7Joyce G. Rohan8Candice N. Hatcher-Solis9Cognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USA; Oak Ridge Institute for Science and Education, Oak Ridge, TN, USACognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USA; Infoscitex, Inc., Dayton, OH, USACognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USA; Infoscitex, Inc., Dayton, OH, USANaval Medical Research Unit Dayton, Wright-Patterson AFB, OH, USA; Odyssey Systems Consulting Group, Wakefield, MA, USANaval Medical Research Unit Dayton, Wright-Patterson AFB, OH, USA; Odyssey Systems Consulting Group, Wakefield, MA, USACognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USA; Oak Ridge Institute for Science and Education, Oak Ridge, TN, USACognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USACognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USANaval Medical Research Unit Dayton, Wright-Patterson AFB, OH, USACognitive Neuroscience, 711th HPW, AFRL, Wright-Patterson AFB, OH, USA; Corresponding author. Airmen Biosciences Division, 711th Human Performance Wing, Air Force Research Laboratory, Wright-Patterson AFB, OH, 45433, USA.Background: Vagus nerve stimulation (VNS) improves cognition in humans and rodents, but the effects of a single session of VNS on performance and plasticity are not well understood. Objective: Behavioral performance and hippocampal (HC) electrophysiology/neurotrophin expression were measured in healthy adult rats after VNS paired training to investigate changes in cognition and synaptic plasticity. Methods: Platinum/iridium electrodes were surgically implanted around the left cervical branch of the VN of anesthetized male Sprague-Dawley rats (N = 47). VNS (100 μs biphasic pulses, 30 Hz, 0.8 mA) paired Novel Object Recognition (NOR)/Passive Avoidance Task (PAT) were assessed 24 h after training and post-mortem tissue was collected 48 h after VNS (N = 28). Electrophysiology recordings were collected using a microelectrode array system to assess functional effects on HC slices 90 min after VNS (N = 19). Sham received the same treatment without VNS and experimenters were blinded. Results: Stimulated rats exhibited improved performance in NOR (p < 0.05, n = 12) and PAT (p < 0.05, n = 14). VNS enhanced long-term potentiation (p < 0.05, n = 7–12), and spontaneous spike amplitude (p < 0.05, n = 7–12) and frequency (p < 0.05, n = 7–12) in the CA1. Immunohistochemical analysis found increased brain-derived neurotrophic factor expression in the CA1 (p < 0.05, n = 8–9) and CA2 (p < 0.01, n = 7–8). Conclusion: These findings suggest that our VNS parameters promote synaptic plasticity and target the CA1, which may mediate the positive cognitive effects of VNS. This study significantly contributes to a better understanding of VNS mediated HC synaptic plasticity, which may improve clinical utilization of VNS for cognitive enhancement.http://www.sciencedirect.com/science/article/pii/S1935861X22001796Vagus nerve stimulationSynaptic plasticityLong-term potentiationSpontaneous spikingBrain-derived neurotrophic factorNovel object recognition |
| spellingShingle | Laura K. Olsen Raquel J. Moore Naomi A. Bechmann Victoria T. Ethridge Nathan M. Gargas Sylvia D. Cunningham Zhanpeng Kuang Joshua K. Whicker Joyce G. Rohan Candice N. Hatcher-Solis Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats Brain Stimulation Vagus nerve stimulation Synaptic plasticity Long-term potentiation Spontaneous spiking Brain-derived neurotrophic factor Novel object recognition |
| title | Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats |
| title_full | Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats |
| title_fullStr | Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats |
| title_full_unstemmed | Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats |
| title_short | Vagus nerve stimulation-induced cognitive enhancement: Hippocampal neuroplasticity in healthy male rats |
| title_sort | vagus nerve stimulation induced cognitive enhancement hippocampal neuroplasticity in healthy male rats |
| topic | Vagus nerve stimulation Synaptic plasticity Long-term potentiation Spontaneous spiking Brain-derived neurotrophic factor Novel object recognition |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X22001796 |
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