Electrophysiology and Morphology of Human Cortical Supragranular Pyramidal Cells in a Wide Age Range

Overview

Journal bioRxiv

Date 2024 Jun 25

PMID 38915496

Authors

Pal Barzo

Ildiko Szots

Martin Toth

Eva Adrienn Csajbok

Gabor Molnar

Gabor Tamas

Affiliations

Soon will be listed here.

Abstract

The basic excitatory neurons of the cerebral cortex, the pyramidal cells, are the most important signal integrators for the local circuit. They have quite characteristic morphological and electrophysiological properties that are known to be largely constant with age in the young and adult cortex. However, the brain undergoes several dynamic changes throughout life, such as in the phases of early development and cognitive decline in the aging brain. We set out to search for intrinsic cellular changes in supragranular pyramidal cells across a broad age range: from birth to 85 years of age and we found differences in several biophysical properties between defined age groups. During the first year of life, subthreshold and suprathreshold electrophysiological properties changed in a way that shows that pyramidal cells become less excitable with maturation, but also become temporarily more precise. According to our findings, the morphological features of the three-dimensional reconstructions from different life stages showed consistent morphological properties and systematic dendritic spine analysis of an infantile and an old pyramidal cell showed clear significant differences in the distribution of spine shapes. Overall, the changes that occur during development and aging may have lasting effects on the properties of pyramidal cells in the cerebral cortex. Understanding these changes is important to unravel the complex mechanisms underlying brain development, cognition and age-related neurodegenerative diseases.

References

Petanjek Z, Judas M, Kostovic I, Uylings H . Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. Cereb Cortex. 2007; 18(4):915-29. DOI: 10.1093/cercor/bhm124. View

Petanjek Z, Judas M, Simic G, Rasin M, Uylings H, Rakic P . Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A. 2011; 108(32):13281-6. PMC: 3156171. DOI: 10.1073/pnas.1105108108. View

Connors B . Intrinsic neuronal physiology and the functions, dysfunctions and development of neocortex. Prog Brain Res. 1994; 102:195-203. DOI: 10.1016/S0079-6123(08)60540-3. View

McCormick D, Prince D . Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol. 1987; 393:743-62. PMC: 1192421. DOI: 10.1113/jphysiol.1987.sp016851. View

HUTTENLOCHER P, De Courten C, Garey L, Van Der Loos H . Synaptogenesis in human visual cortex--evidence for synapse elimination during normal development. Neurosci Lett. 1982; 33(3):247-52. DOI: 10.1016/0304-3940(82)90379-2. View

Jacobs B, Driscoll L, Schall M . Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol. 1997; 386(4):661-80. View

Popescu I, Le K, Ducote A, Li J, Leland A, Mostany R . Increased intrinsic excitability and decreased synaptic inhibition in aged somatosensory cortex pyramidal neurons. Neurobiol Aging. 2020; 98:88-98. PMC: 8436770. DOI: 10.1016/j.neurobiolaging.2020.10.007. View

Rakic P . Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci. 2009; 10(10):724-35. PMC: 2913577. DOI: 10.1038/nrn2719. View

Beaulieu-Laroche L, Toloza E, van der Goes M, Lafourcade M, Barnagian D, Williams Z . Enhanced Dendritic Compartmentalization in Human Cortical Neurons. Cell. 2018; 175(3):643-651.e14. PMC: 6197488. DOI: 10.1016/j.cell.2018.08.045. View

10.

Craik F, Bialystok E . Cognition through the lifespan: mechanisms of change. Trends Cogn Sci. 2006; 10(3):131-8. DOI: 10.1016/j.tics.2006.01.007. View

11.

Etherington S, Williams S . Postnatal development of intrinsic and synaptic properties transforms signaling in the layer 5 excitatory neural network of the visual cortex. J Neurosci. 2011; 31(26):9526-37. PMC: 6623153. DOI: 10.1523/JNEUROSCI.0458-11.2011. View

12.

Guet-McCreight A, Chameh H, Mahallati S, Wishart M, Tripathy S, Valiante T . Age-dependent increased sag amplitude in human pyramidal neurons dampens baseline cortical activity. Cereb Cortex. 2022; 33(8):4360-4373. DOI: 10.1093/cercor/bhac348. View

13.

Huguenard J, Hamill O, Prince D . Developmental changes in Na+ conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol. 1988; 59(3):778-95. DOI: 10.1152/jn.1988.59.3.778. View

14.

McAllister A . Cellular and molecular mechanisms of dendrite growth. Cereb Cortex. 2000; 10(10):963-73. DOI: 10.1093/cercor/10.10.963. View

15.

Elston G, Fujita I . Pyramidal cell development: postnatal spinogenesis, dendritic growth, axon growth, and electrophysiology. Front Neuroanat. 2014; 8:78. PMC: 4130200. DOI: 10.3389/fnana.2014.00078. View

16.

Nusser Z, Lujan R, Laube G, Roberts J, Molnar E, Somogyi P . Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 1998; 21(3):545-59. DOI: 10.1016/s0896-6273(00)80565-6. View

17.

Kuzawa C, Chugani H, Grossman L, Lipovich L, Muzik O, Hof P . Metabolic costs and evolutionary implications of human brain development. Proc Natl Acad Sci U S A. 2014; 111(36):13010-5. PMC: 4246958. DOI: 10.1073/pnas.1323099111. View

18.

van Blooijs D, van den Boom M, van der Aar J, Huiskamp G, Castegnaro G, Demuru M . Developmental trajectory of transmission speed in the human brain. Nat Neurosci. 2023; 26(4):537-541. PMC: 10076215. DOI: 10.1038/s41593-023-01272-0. View

19.

Kang H, Kawasawa Y, Cheng F, Zhu Y, Xu X, Li M . Spatio-temporal transcriptome of the human brain. Nature. 2011; 478(7370):483-9. PMC: 3566780. DOI: 10.1038/nature10523. View

20.

Zhu J . Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca2+ action potentials in adult rat tuft dendrites. J Physiol. 2000; 526 Pt 3:571-87. PMC: 2270034. DOI: 10.1111/j.1469-7793.2000.00571.x. View