Short-Latency Activation of Striatal Spiny Neurons via Subcortical Visual Pathways

Effects of light flash stimulation on spontaneous activity of a spiny neuron (representative example). A, Top, All-amplitude histogram generated from a 9 s segment of recording. Thresholds for detection of up-state transitions are indicated. Bottom, A sample of the smoothed trace from the same recording. Up threshold (dotted line), down-state onsets (triangles), 200 ms interval for amplitude measurement (black bar), and up-state latency (lat.) are indicated (for definitions, see Materials and Methods). B, C, Left, Time-resolved probability distribution for the neuron to depolarize from the down-state membrane potential (y-axis) during no-light epochs (B) (n = 34 random sample from 236) and light epochs (C) (n = 30); black depicts a high probability, the lightest gray shade represents one trial; timescale is the same as in C. Right, Amplitude distributions of depolarizations from the down state. Note that, after a light flash, stronger depolarizations were measured in this neuron (6.5 vs 2.3 mV; Wilcoxon's rank sum test, p < 0.01). D, The distribution of up-state latencies reveals shortened latencies after light flash stimulation (255 ms; compared with 312 ms for no light; Wilcoxon's rank sum test, p < 0.05).

Typical effects of BIC ejection into the SC on spontaneous and visual-evoked neural activity. A, Immediate effects of BIC ejection into the SC on fluctuations in neural activity in the striatum (top), cortex (middle), and superior colliculus (bottom). B, Before BIC (left), the spiny neuron showed no visual response, only the normal spontaneously occurring up states. Note the absence of a VEP in the LFP recorded from the SC (bottom trace). After BIC (right), when a strong negative deflection marked the VEP in the SC, light stimulation evoked a short-latency up transition in the spiny neuron.

Time course of visual responsiveness induced by BIC ejection into the SC in dopamine-intact and AMPT-treated animals. A–D, Medians of up-state latencies (A, B) and early depolarization amplitudes measured from the down state (C, D) are shown as mean ± SEM across neurons. Time on the x-axis is given in relation to BIC ejection (dotted line at 0). Dashed lines, No-light epochs; solid lines, light epochs in neurons from AMPT-treated (n = 7) and untreated animals (n = 7). The asterisks above each subplot indicate significant differences between no-light and light epochs at 5 min after BIC ejection (Wilcoxon's signed rank test, p < 0.05). Note the similar time course and magnitude of visual responses in the AMPT-treated and untreated group after BIC (Wilcoxon's rank sum test, p > 0.1). Also, note the tendency to smaller early depolarization amplitudes in light as well as no-light epochs of the AMPT-treated group before and >15 min after BIC.

Effects of BIC on visual responsiveness of the SC and a spiny neuron in single trials. Time on the x-axis is given in relation to BIC ejection (dashed line at 0). A, Time-resolved membrane potential distribution. Grayscale indicates the probability for the neuron to be at a respective membrane potential (y-axis); black depicts a high probability, and white depicts a low probability. Colored circles indicate point of early depolarization amplitude achieved during the first 200 ms after the light flash; a red circle indicates that the SC was visually responsive at the time (see C). B, Up-state latencies of light responses. Note the consistently short latencies when the SC was responsive (red circles). C, Amplitudes of the collicular VEP. Amplitudes after BIC exceeding the 99th percentile of no-light responses (indicated by the horizontal dotted line) were considered as significant visual responses (red circles). D, The EEG power at 1 Hz. Note the decrease after BIC ejection. E, F, Scatter plots of up-state latencies (E; from B) and early depolarization amplitudes (F; from A) versus the amplitude of the VEP (from C). The vertical dotted lines represent the 99th percentile of SC no-light responses. Only data points of significant collicular VEPs after BIC were included in the regression fits (red circles). Correlation coefficients (R²) were statistically significant (p < 0.05).

Changes in visual sensitivity of primary visual cortex and striatal spiny neurons are not correlated. The left panels show a typical example of a mean cortical VEP before (gray) and after (black) BIC ejection; lighter shades indicate SEM. The right panels show distribution of up-state latencies measured simultaneously (except in C) in a striatal spiny neuron in box plots; median (central line), quartiles (bar limits), range (error bars), and outliers (+) are indicated. The asterisks indicate that latencies are significantly shorter than in light epochs before BIC (p < 0.05, Wilcoxon's rank sum test). A, BIC ejection into the SC induces visual responses in spiny neurons but also affects the cortical VEP. B, BIC ejected into the visual cortex increases the VEP recorded through the adjacent LFP electrode but fails to induce visual responsiveness in the striatal spiny neuron. C, The cortical VEP (gray) recorded before the penetration of the neuron is suppressed after MUS ejection onto the cortex (black). Nevertheless, BIC ejection into the SC still induces visual responses in the spiny neuron.