Abstract
Postnatal inhibitory neuron development affects mammalian brain function, and failure of this maturation process may underlie pathological conditions such as epilepsy, schizophrenia, and depression. Furthermore, understanding how physiological properties of inhibitory neurons change throughout development is critical to understanding the role(s) these cells play in cortical processing. One subset of inhibitory neurons that may be affected during postnatal development is somatostatin-expressing (SOM) cells. A subset of these cells is labeled with green-fluorescent protein (GFP) in a line of mice known as the GFP-positive inhibitory neurons (GIN) line. Here, we studied how intrinsic electrophysiological properties of these cells changed in the somatosensory cortex of GIN mice between postnatal ages P11 and P32+. GIN cells were targeted for whole-cell current-clamp recordings and ranges of positive and negative current steps were presented to each cell. The results showed that as the neocortical circuitry matured during this critical time period multiple intrinsic and firing properties of GIN inhibitory neurons, as well as those of excitatory (regular-spiking [RS]) cells, were altered. Furthermore, these changes were such that the output of GIN cells, but not RS cells, increased over this developmental period. We quantified changes in excitability by examining the input–output relationship of both GIN and RS cells. We found that the firing frequency of GIN cells increased with age, while the rheobase current remained constant across development. This created a multiplicative increase in the input–output relationship of the GIN cells, leading to increases in gain with age. The input–output relationship of the RS cells, on the other hand, showed primarily a subtractive shift with age, but no substantial change in gain. These results suggest that as the neocortex matures, inhibition coming from GIN cells may become more influential in the circuit and play a greater role in the modulation of neocortical activity.
Highlights
The second and third postnatal weeks are a period of massive developmental change within the rodent neocortex
In order to fully understand how the firing dynamics of GFP-positive inhibitory neurons (GIN) cells and RS cells changed during development, we examined the input–output relationship of both cell types from P11 to P32+
Our data demonstrated that multiple intrinsic physiological characteristics of L2/3 GIN and RS cells in somatosensory cortex changed across the developmental time period investigated here (P11– P32+)
Summary
The second and third postnatal weeks are a period of massive developmental change within the rodent neocortex. Recent in vivo recordings from superficial SOM cells in mouse somatosensory cortex have found that activity in SOM cells is suppressed during both passive whisker deflection and during active whisking states (Gentet et al, 2012) This loss of dendritic inhibition may function to allow excitatory inputs on the distal dendrites to summate and propagate to the soma more effectively. Understanding the normal trajectory of GIN cell maturation serves several purposes It helps clarify the physiological role(s) these cells can play during different stages of postnatal development by indicating how intrinsic properties of GIN cells change over age, how readily these cells are excited and what their firing characteristics are once activated. These results suggest that as the neocortical circuit develops, GIN cells may increasingly participate in sensory processing within somatosensory cortex
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