Representation of the body in the lateral striatum of the freely moving rat: Fast Spiking Interneurons respond to stimulation of individual body parts

Abstract

Numerous studies have shown that certain types of striatal interneurons play a crucial role in selection and regulation of striatal output. Striatal Fast-Spiking Interneurons (FSIs) are parvalbumin positive, GABAergic interneurons that constitute less than 1% of the total striatal population. It is becoming increasingly evident that these sparsely distributed neurons exert a strong inhibitory effect on Medium Spiny projection Neurons (MSNs). MSNs in lateral striatum receive direct synaptic input from regions of cortex representing discrete body parts, and show phasic increases in activity during touch or movement of specific body parts. In the present study, we sought to determine whether lateral striatal FSIs identified by their electrophysiological properties, i.e., short-duration spike and fast firing rate (FR), display body part sensitivity similar to that exhibited by MSNs. During video recorded somatosensorimotor exams, each individual body part was stimulated and responses of single neurons were observed and quantified. Individual FSIs displayed patterns of activity related selectively to stimulation of a discrete body part. Most patterns of activity were similar to those exhibited by typical MSNs, but some phasic decreases were observed. These results serve as evidence that some striatal FSIs process information related to discrete body parts and participate in sensorimotor processing by striatal networks that contribute to motor output.

Statement of significance: Parvalbumin positive, striatal FSIs are hypothesized to play an important role in behavior by inhibiting MSNs. We asked a fundamental question regarding information processed during behavior by FSIs: whether FSIs, which preferentially occupy the sensorimotor portion of the striatum, process activity of discrete body parts. Our finding that they do, in a selective manner similar to MSNs, begins to reveal the types of phasic signals that FSI feed forward to projection neurons during striatal processing of cortical input regarding a specific sensorimotor event. These findings suggest new avenues for testing feed-forward inhibition theory as applied to striatum in naturalistic conditions, such as whether FSI decreases facilitate excitation of MSNs related to the current movement while FSI increases silence MSNs unrelated to the current movement.

Keywords: Dorsolateral striatum; Electrophysiology; Fast Spiking Interneurons; Parvalbumin.

Figure 1

a) & (b) overlaid single spike waveforms of an example MSN and example FSI. (c) & (d) corresponding inter-spike interval histograms for the example MSN and FSI. (e) & (f) overlaid averaged waveforms of 26 presumed FSIs and 57 presumed MSNs. Red dashed lines: measurements used for cluster analysis.

Figure 2

a) & (b) three-dimensional scatter plots of entire distribution of recorded waveforms along the three dimensions used in cluster analysis: FR, valley duration, valley to peak duration from two perspectives. Yellow dots: 17 neurons classified as FSIs (with FR> 2 spikes/sec), dark red dots: neurons classified as MSNs. Remaining neurons belong to minor clusters.

Figure 3

Rasters and peri-event time histograms (PETHs) centered on the onset of body part stimulation (represented by black vertical dashed line at time 0) displaying firing of body part responsive FSIs. Black dots represent the offset of body part stimulation. (a) raster-PETH displaying firing of a responsive FSI that exhibits clear increase in firing during downward passive head movement, (b) lack of modulation for same neuron during upward head movement. (c) Another FSI exhibits clear decrease related to upward paw movement, but (d) a lack of modulation during upward head movement. e) FSI showing increased FR during upward head movement, (f) and no modulation during whisker stimulation. (g) Another FSI showing large decrease in FR during upward head movement, (h) but no change during left paw lifts.

Figure 4

Box plot displaying mean absolute fold change in FR of FSI with respect to baseline, plotted separately for unrelated body parts versus related body parts. * indicates significant difference (p = 0.01) in magnitude of FR from Baseline to Test for Related but not Unrelated (ns = not significant) categories (absolute FR fold change value of 1 = no change).

Figure 5

Diagram of locations where FSIs responsive and non-responsive to body part stimulation were recorded. Red dots mark locations of responsive FSIs, whereas black dots mark locations of non-responsive FSIs.