Long-Term Stable Recording of Single-Neuron Spike Activity in the Amygdala in Conscious Rabbits

The development of current technologies for neurophysiological research has made it possible to observe the activity of large numbers of neurons involved in the operation of distributed neural neurons in the whole brain. An important aspect of such studies is the stability of the signal being recorded, which determines the ability to make recordings from a single cell for prolonged periods. The aim of the present work was to assess the possibility of using chronically implanted multiple microwires for stable recording of the activity of individual neurons in the rabbit brain. Experiments were performed on two adult male European rabbits (Orictolagus cuniculus), in which bundles of microwires were implanted in the amygdala. Experimental data were captured over periods of 72 days in rabbit No. 1 and 964 days in rabbit No. 2. Assessment of neuron signal recording quality showed that the recording device used here made high-quality recordings of the activity of single neurons over long periods. Use of an automated algorithm identified stable recordings of single neurons, which in future will provide for multifaceted investigations of changes in the activity of brain cells with complex behavior.

This is a preview of subscription content, access via your institution.

References

  1. Adrian, E. D., “The impulses produced by sensory nerve endings: Part 4. Impulses from pain receptors,” J. Physiol., 62, No. 1, 33–51 (1926).

    CAS  Article  Google Scholar 

  2. Blinkov, S. M., Brazovskaya, F. A., and Putsillo, M. V., An Atlas of the Rabbit Brain, Meditsina, Moscow (1973).

    Google Scholar 

  3. Bondar, I. V., Leopold, D. A., Richmond, B. J., et al., “Long-term stability of visual pattern selective responses of monkey temporal lobe neurons,” PLoS One, 4, No. 12, e8222 (2009).

    Article  Google Scholar 

  4. Bondar, I. V., Vasileva, L. N., Badakva, et al., “Recording quality of neuron signals in the motor cortex of monkeys using chronically implanted multiple microwires,” Zh. Vyssh. Nerv. Deyat., 64, No. 1, 101 (2014).

  5. Chauviere, L., Pothof, F., Gansel, K. S., et al., “In vivo recording quality of mechanically decoupled fl oating versus skull-fixed silicon-based neural probes,” Front. Neurosci., 13, 464 (2019).

    Article  Google Scholar 

  6. Coffey, K. R., Barker, D. J., Gayliard, N., et al., “Electrophysiological evidence of alterations to the nucleus accumbens and dorsolateral striatum during chronic cocaine self-administration,” Eur. J. Neurosci., 41, 1538–1552 (2015).

    Article  Google Scholar 

  7. Cohen, L., Koffman, N., Meiri, H., et al., “Time-lapse electrical recordings of single neurons from the mouse neocortex,” Proc. Natl. Acad. Sci. USA, 110, 5665–5670 (2013), https://doi.org/10.1073/pnas.1214434110.

    CAS  Article  PubMed  Google Scholar 

  8. Dhawale, A. K., Poddar, R., Wolff, S. B. E., et al., “Automated long-Term recording and analysis of neural activity in behaving animals,” eLife, 6 (2017).

  9. Fraser, G. W. and Schwartz, A. B., “Recording from the same neurons chronically in motor cortex,” J. Neurophysiol., 107, No. 7, 1970–1978 (2012), https://doi.org/10.1152/jn.01012.2010.

    Article  PubMed  Google Scholar 

  10. Fyhn, M., Hafting, T., Treves, A., et al., “Hippocampal remapping and grid realignment in entorhinal cortex,” Nature, 446, No. 7132, 190–194 (2007).

    CAS  Article  Google Scholar 

  11. Guan, S., Wang, J., Gu, X., et al., “Elastocapillary self-assembled neurotassels for stable neural activity recordings,” Sci. Adv., 5, No. 3 (2019).

  12. Hong, J. H., Koyano, K. W., Russ, B. E., and Leopold, D. A., “Comparing experience-dependent changes in stimulus response selectivity of macaque AM and AF face patch neurons,” in: The Annual Meeting of Society for Neuroscience Abstract, Online (2017).

  13. Hubel, D. and Wiesel, T., “Receptive fields of single neurones in the cat’s striate cortex,” in: The Central Nervous System: the Visual Pathway from Retina to Striate Cortex (1959), pp. 574–591.

  14. Koyano, K. W., Russ, B. E., and Leopold, D. A., “Recording from face patch AM neurons of a macaque monkey using implanted microwire bundles,” in: The Annual Meeting of the Japan Neuroscience Society Abstract (2016), pp. 1–142.

  15. Krüger, J., Caruana, F., Volta, R. D., and Rizzolatti, G., “Seven years of recording from monkey cortex with a chronically implanted multiple microelectrode,” Front. Neuroeng., 3, 6 (2010).

    PubMed  PubMed Central  Google Scholar 

  16. Kuraoka, K. and Nakamura, K., “Responses of single neurons in monkey amygdala to facial and vocal emotions,” J. Neurophysiol, 97, No. 2, 1379–1387 (2007).

    Article  Google Scholar 

  17. Kuraoka, K., Konoike, N., and Nakamura, K., “Functional differences in face processing between the amygdala and ventrolateral prefrontal cortex in monkeys,” Neuroscience, 304, 71–80 (2015).

    CAS  Article  Google Scholar 

  18. Lanzilotto, M., Livi, A., Maranesi, M., et al., “Extending the cortical grasping network: Pre-supplementary motor neuron activity during vision and grasping of objects,” Cereb. Cortex, 26, 4435–4449 (2016).

    Article  Google Scholar 

  19. Lewicki, M. S., “A review of methods for spike sorting: the detection and classification of neural action potentials,” Network, 9, No. 4, R53–78 (1998).

  20. Logothetis, N. K., Pauls, J., Augath, M., et al., “Neurophysiological investigation of the basis of the fMRI signal,” Nature, 412, No. 6843, 150–7 (2001).

  21. McMahon, D. B. T., Russ, B. E., Elnaiem, H. D., et al., “Single-unit activity during natural vision: Diversity, consistency, and spatial sensitivity among AF face patch neurons,” J. Neurosci., 35, No. 14, 5537–5548 (2015).

    CAS  Article  Google Scholar 

  22. Mosher, C. P., Zimmerman, P. E., and Gothard, K. M., “Neurons in the monkey amygdala detect eye contact during naturalistic social interactions,” Curr. Biol., 24, No. 20, 2459–2464 (2014).

    CAS  Article  Google Scholar 

  23. Okun, M., Lak, A., Carandini, M., and Harris, K. D., “Long term recordings with immobile silicon probes in the mouse cortex,” PLoS One, 11, No. 3, e0151180 (2016).

  24. Park, S. H., Russ, B. E., McMahon, D. B. T., et al., “Functional subpopulations of neurons in a macaque face patch revealed by single-unit fMRI mapping,” Neuron, 95, No. 4, 971–981 (2017).

  25. Pavlova, I. V. and Rysakova, M. P., “Effects of administration of an agonist and an antagonist of γ receptors into the amygdala of rabbits on the motor and cardiac components of conditioned-reflex fear,” Zh. Vyssh. Nerv. Deyat., 63, No. 6, 730 (2013).

  26. Porada, I., Bondar, I., Spatz, W. B., and Krüger, J., “Rabbit and monkey visual cortex: more than a year of recording with up to 64 microelectrodes,” J. Neurosci. Meth ., 95, No. 1, 13–28 (2000).

  27. Renshaw, B., “Central effects of centripetal impulses in axons of spinal ventral roots,” J. Neurophysiol., 9, 191–204 (1946).

    CAS  Article  Google Scholar 

  28. Shvyrkova, N. A. and Andrushko, S. V., “Activity of neurons in the sensorimotor area of the cerebral cortex of rabbits in zoosocial behavior,” Zh. Vyssh. Nerv. Deyat., 40, No. 1, 52–58 (1990).

    CAS  Google Scholar 

  29. Stosiek, C., Garaschuk, O., Holthoff, K., and Konnerth, A., “In vivo twophoton calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. USA, 100, No. 12, 7319–7324 (2003).

    CAS  Article  Google Scholar 

  30. Strumwasser, F., “Long-term recording from single neurons in brain of unrestrained mammals,” Science, 127, No. 3296, 469–470 (1958).

  31. Thompson, L. T. and Best, P. J., “Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats,” Brain Res., 509, No. 2, 299–308 (1990).

    CAS  Article  Google Scholar 

  32. Tinbergen, N. and Lorenz, K., “Taxis und Instinkthandlung in der Eirollbewegung der Graugans,” Z. Tierpsychol., 2, 1–29 (1938).

    Google Scholar 

  33. Tolias, A. S., Ecker, A. S., Siapas, A. G., et al., “Recording chronically from the same neurons in awake, behaving primates,” J. Neurophysiol., 98, No. 6, 3780–90 (2007).

    Article  Google Scholar 

  34. Vasileva, L. N., Badakva, A. M., Miller, N. V., et al., “Long-term recording of single neurons and criteria for its assessment,” Zh. Vyssh. Nerv. Deyat., 64, No. 6, 693–701 (2014).

    Google Scholar 

  35. Verzeano, M., “Activity of cerebral neurons in the transition from wakefulness to sleep,” Science, 124, No. 3217, 366–367 (1956).

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to I. V. Bondar.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 70, No. 4, pp. 528–542, July–August, 2020.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vasileva, L.N., Bondar, I.V. Long-Term Stable Recording of Single-Neuron Spike Activity in the Amygdala in Conscious Rabbits. Neurosci Behav Physi 51, 322–331 (2021). https://doi.org/10.1007/s11055-021-01075-5

Download citation

Keywords

  • chronic recording
  • microelectrodes
  • neurons
  • stable recording
  • rabbit
  • neurophysiology
  • visual stimuli
  • auditory stimuli
  • conscious animals
  • amygdala