Error correction and fast detectors implemented by ultrafast neuronal plasticity

We experimentally show that the neuron functions as a precise time integrator, where the accumulated changes in neuronal response latencies, under complex and random stimulation patterns, are solely a function of a global quantity, the average time lag between stimulations. In contrast, momentary leaps in the neuronal response latency follow trends of consecutive stimulations, indicating ultrafast neuronal plasticity. On a circuit level, this ultrafast neuronal plasticity phenomenon implements error-correction mechanisms and fast detectors for misplaced stimulations. Additionally, at moderate (high) stimulation rates this phenomenon destabilizes (stabilizes) a periodic neuronal activity disrupted by misplaced stimulations.

Figure 1

Experimental measurements of the response latency of a single neuron at 10, 15, 20, 30, 40, and 50 Hz (increasing frequency from bottom to top line). Fluctuations in the neuronal response latency at 10 and 30 Hz are exemplified by the zoom-in (gray areas, bottom and top respectively).

Figure 2

(a) Experimental measurements of momentary changes in the neuronal response latency under stimulation at 30 Hz, where stimulations 50, 100, 150 were given at 10, 20, and 50 Hz (indicated by upper, middle, and lower arrow, respectively). (b) A single neuron was stimulated at a frequency of 20 Hz [gray (lower) line] and 30 Hz [black (upper) line], where at stimulation number 150 a different frequency in the range [8, 70] Hz was given, resulting in a latency leap Δ$L$ = $L$(150)−$L$(149). Arrows correspond to latency leaps indicated in (a). (c) The neuronal response latency under stimulation at 10 Hz [black (lower) line], 30 Hz [gray (upper) line], and at 30 Hz where the frequency changed to 10 Hz every $m$ = 2 [dark blue (lower) jittered line], 5 [dark green (middle) jittered line], 10 [dark red (upper) jittered line] stimulations, and respectively at periodic stimulations 15 [light blue (lower) smooth line], 21.4 [light green (middle) smooth line], and 25 [light red (upper) smooth line] Hz. The right panel shows a zoom-in of the gray area. (d) The neuronal response latency under stimulation at 10 Hz (red smooth line) and at random time lags between stimulations in the range [35, 165] ms (blue jittered line).

Figure 3

(a) The neuronal response latency stimulated with random time lags in [50, 150] ms (blue) and the accumulated probability $P_{+}$ = $P$(Δ$L$·Δτ>0) (purple). (b) A zoom-in [gray area in (a)] of Δ$L$ (pink circles) and the corresponding Δτ (aqua squares). For most steps Δ$L$·Δτ>0, with an exception at step 309 (black arrow), in this trial. (c) Schematic of a chain consisting of five neurons, where neuron 1 is stimulated by a random stimulation pattern. (d) The accumulated response latency for the first Ni neurons along the chain, where the lines are ordered from bottom to top from $i$ = 1 to $i$ = 5. (e) Top panel: accumulated probabilities $P_{+}$, $P_{-}$ and $P_0$ for $N$1 in (d). Bottom panel: accumulated $P_{+}$ for $N$1 [blue (lower) full line], $N$3 [green (middle) full line], and $N$5 [purple (upper) full line] in (d), and the theoretically predicted $P_{+}$ for $N$3 [purple (lower) dashed line] and $N$5 [green (upper) dashed line]. (f) Schematic of a neuronal circuit consisting of nine neurons and strong (weak) [above-threshold (subthreshold)] stimulations represented by full (dashed) lines. The rightmost neuron receives two weak stimulations via two delay routes with an initial difference of ε ms (red wide dashed line). (g) Experimental results for an initial ε = 12.5 ms. The leftmost neuron is stimulated at random time lags in the range [27.3, 39.3] ms with the exception of 100 ms preceding stimulation 160. The time lag between two stimulations arriving at the rightmost neuron, Δ$S$ (blue), results in an evoked spike solely for stimulation 160 (red circle).

Figure 4

(a) Experimental measurements of the response latency at 6 ms (166.7 Hz) with the exception of 10 ms (100 Hz) preceding the tenth stimulation. (b) A reversed scenario to (a), 10 ms (100 Hz) with the exception of 6 ms (166.7 Hz) preceding the tenth stimulation. (c) Top box: Stimulations at a fixed rate (blue), and their corresponding evoked spikes for moderate ($M$, red) and high ($H$, green) stimulation frequencies. Evoked spikes are shown as a function of stimulation number. Middle box: Similar to the top box, however the fifth stimulation is given at a higher rate, earlier than expected under a fixed stimulation rate (dashed vertical line). Bottom box: Similar to the top box, however the fifth stimulation is given at a lower rate, later than expected.