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[Preprint]. 2023 Jun 19:2023.06.02.543448.
doi: 10.1101/2023.06.02.543448.

Inter and Intralaminar Excitation of Parvalbumin Interneurons in Mouse Barrel Cortex

Kate S Scheuer  1 , Anna M Jansson  2 , Xinyu Zhao  3 , Meyer B Jackson  2
Affiliations

Inter and Intralaminar Excitation of Parvalbumin Interneurons in Mouse Barrel Cortex

Kate S Scheuer et al. bioRxiv. .

Update in

Abstract

Parvalbumin (PV) interneurons are inhibitory fast-spiking cells with essential roles in directing the flow of information through cortical circuits. These neurons set the balance between excitation and inhibition, control rhythmic activity, and have been linked to disorders including autism spectrum and schizophrenia. PV interneurons differ between cortical layers in their morphology, circuitry, and function, but how their electrophysiological properties vary has received little attention. Here we investigate responses of PV interneurons in different layers of primary somatosensory barrel cortex (BC) to different excitatory inputs. With the genetically-encoded hybrid voltage sensor, hVOS, we recorded voltage changes simultaneously in many L2/3 and L4 PV interneurons to stimulation in either L2/3 or L4. Decay-times were consistent across L2/3 and L4. Amplitude, half-width, and rise-time were greater for PV interneurons residing in L2/3 compared to L4. Stimulation in L2/3 elicited responses in both L2/3 and L4 with longer latency compared to stimulation in L4. These differences in latency between layers could influence their windows for temporal integration. Thus PV interneurons in different cortical layers of BC show differences in response properties with potential roles in cortical computations.

Keywords: barrel cortex; genetically-encoded voltage sensor; parvalbumin interneuron.

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Conflict of interest statement

Conflict of interest statement: The authors declare no competing financial or non-financial interests.

Figures

Figure 1.
Figure 1.
Identifying individual responsive PV interneurons. Gradient contrast image taken with the Kiralux camera (A) and fluorescence image taken with the CCD-SMQ camera (B) of a BC slice. Black stars indicate the tip of the stimulating electrode, and dashed lines indicate layer boundaries in A-E. C. SNR heatmap of slice in A and B. Gray pixels near the top have signals below the baseline noise and were excluded from analysis. The electrode is outlined in black on the lower left edge in C-E. D. K-means cluster map. K-means clustering of SNR was performed on pixels with SNR > baseline (colored in C). The data were best fitted with two clusters, with averages of 4.8 and 9.2. The yellow cluster with higher average SNR is likely to contain responsive PV interneurons, while the purple cluster with lower average SNR probably contains processes and unresponsive neurons. E. SNR heatmap overlaid with identified responsive PV interneurons outlined in black or red (color choice based on ease of view and not cell properties). F. Traces of fluorescence versus time for the PV interneurons outlined and numbered in E show clear depolarization in response to stimulation (triangle). G. Expanded portion of a trace (12 msec) shaded in F illustrating response parameters. Amplitude (red) is the maximum change in fluorescence; latency (purple) is the time from stimulation to half-maximal change in fluorescence; half-width (green) is the time between half-maximal change in fluorescence from depolarization to repolarization; rise-time (blue) is the time between half-maximal and maximal change in fluorescence; decay-time (gold) is the time from peak to half-maximal fluorescence.
Figure 2.
Figure 2.
PV interneuron response half-width and amplitude do not vary with distance. Neither half-width (A, R = 0.006, p = 0.854) nor amplitude (B, Pearson’s product-moment correlation: R = 0.042, p = 0.170) are significantly correlated with distance from the stimulating electrode. This is consistent with single-cell responses, as half-width would be expected to increase, and amplitude would decrease with distance for a population response. Each point on the scatterplot corresponds to one PV interneuron. Linear regression best fit lines are shown in blue. N = 1086 cells from 52 slices.
Figure 3.
Figure 3.
PV interneuron responses in BC. Gradient contrast (A) and fluorescence (B) images of two different slices of BC. L2/3 through L5 are visible within the fields of view. The tip of the stimulating electrode (black or white star) is visible in L2/3 (left) or L4 (right) in A-C. Dashed lines separate layers. C. SNR heatmaps for the slices shown in A and B. Warmer colors correspond to higher SNR regions more likely to contain responsive PV interneurons (color scales and ranges – lower right).
Figure 4.
Figure 4.
Amplitude, rise-time, and half-width of PV interneurons residing in different layers. L2/3 PV interneuron responses (blue) had higher amplitudes (A), longer rise-times (B), and broader half-widths (C) than responses from PV interneurons in L4 (purple). Decay-time (D) did not differ based on PV interneuron residence layer. Stimulation layer did not significantly impact amplitude, half-width, rise-time, or decay-time.
Figure 5.
Figure 5.
PV interneuron response latency depends on stimulation layer. A. Raw latencies for PV interneuron responses to stimulation in L2/3 (orange) or L4 (green). B. Regardless of residence layer, responses elicited by L2/3 stimulation (orange) have longer distance-normalized latencies than those elicited by L4 stimulation (green, t = (50) = 4.244, p < 0.001).
Figure 6.
Figure 6.
Summary of PV interneuron response differences. Amplitude, distance-normalized latency, rise-time, and half-width vary based on cortical layer. PV interneurons (teal circles) residing in L2/3 had higher amplitudes, slower rise-times, and broader half-widths compared to those in L4. Distance-normalized latencies of responses to stimulation of excitatory cells (purple triangles) in L2/3 were longer than those of responses to stimulation in L4.
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