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. 2024 Jun 13;19(6):e0289901.
doi: 10.1371/journal.pone.0289901. eCollection 2024.

Inter and intralaminar excitation of parvalbumin interneurons in mouse barrel cortex

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

Inter and intralaminar excitation of parvalbumin interneurons in mouse barrel cortex

Katherine S Scheuer et al. PLoS One. .

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 and control rhythmic activity. 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 in many L2/3 and L4 PV interneurons simultaneously, with stimulation applied to either L2/3 or L4. A semi-automated procedure was developed to identify small regions of interest corresponding to single responsive PV interneurons. 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 respond in a layer specific and input specific manner, and these differences have potential roles in cortical computations.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. A flowchart illustrates the steps of analysis used to identify responsive neurons in maps of activity (ΔF/F) and signal-to-noise ratio (Fig 2).
The sequence of steps illustrates the multiple criteria employed in identifying ROIs as single PV interneurons for analysis.
Fig 2
Fig 2. Identifying individual responsive PV interneurons.
A. Gradient contrast image of a BC slice (with Kiralux camera). B. Fluorescence image of the same slice (with the CCD-SMQ camera). Black star indicates the tip of the stimulating electrode, and dashed lines indicate layer boundaries in A-E. The electrode is visible in A and B and is outlined in black in C-E. C. SNR heatmap of evoked responses from the same slice, with SNR coded as color according to the scale lower left. A few pixels near the top have signals below the baseline noise and were excluded from analysis (grey). D. K-means cluster map using the method outlined in Fig 1, based on pixels with SNR > baseline (other than gray in C). In this example the data were best fitted with two clusters with averages of 4.8 and 9.2. The yellow higher SNR cluster contains responsive PV interneurons, while the purple lower SNR cluster contains processes and unresponsive neurons. ROIs are outlined in black. E. An SNR heatmap from the same experiment generated by different software overlaid with identified responsive PV interneurons (33 ROIs containing 2–7 pixels, average 3.18). ROIs are outlined in black or red, with red numbers to indicate traces in F. F. Traces of fluorescence versus time for the PV interneurons outlined and numbered in red in E show clear depolarization in response to stimulation (triangle above and dashed vertical line). G. A segment of 20 msec from trace 9 in F (shaded) is expanded to illustrate response parameters analyzed here. Amplitude (red) is the maximum change in fluorescence; latency (purple) is the time from stimulation to half-maximal change; half-width (green) is the time between half-maximal changes from depolarization to repolarization; rise-time (blue) is the time between half-maximal and maximal change; decay-time (olive) is the time from peak to half-maximal fluorescence.
Fig 3
Fig 3. PV interneuron response half-width and amplitude do not vary with distance.
A. Half-width was uncorrelated with distance from stimulating electrode (R = 0.006, p = 0.854). B. Amplitude was uncorrelated with distance (R = 0.042, p = 0.170; Pearson’s product-moment correlation for both A and B). These results support the interpretation of single-cell responses, as half-width would be expected to increase, and amplitude would decrease with distance for population responses. Each point corresponds to one ROI identified by the procedure described in Methods. Linear regression best fit lines are shown in blue. N = 1086 cells from 52 slices.
Fig 4
Fig 4. 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 of evoked responses from the slices shown in A and B. Warmer colors correspond to higher SNR and more responsive PV interneurons (color scales and ranges–lower right).
Fig 5
Fig 5. 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. All boxplots are nonparametric.
Fig 6
Fig 6. PV interneuron response latency depends on stimulation layer.
A. Raw latencies (not divided by distance) and B. Normalized latencies (to distance) for PV interneuron responses to stimulation in L2/3 (orange) or L4 (green). Regardless of residence layer, responses elicited by L2/3 stimulation (orange) have longer distance-normalized latencies than those elicited by L4 stimulation (green, F(1,51) = 16.478, p < 0.001). Both boxplots are nonparametric.
Fig 7
Fig 7. 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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