Experiential modification of the trigeminal reflex blink circuit

Abstract

To characterize the organization and plasticity of the trigeminal reflex blink circuit, we interacted blink-evoking supraorbital (SO) and infraorbital (IO) nerve stimuli in alert rats. Stimulation of either trigeminal branch produced a short-lasting inhibition followed by a longer-lasting facilitation of blinks evoked by stimulating the other nerve. When IO stimulation evoked a smaller blink than SO stimulation (IO < SO), SO stimulation facilitated subsequent IO-evoked blinks more than IO stimulation facilitated SO-evoked blinks. When IO > SO, IO and SO stimulation exerted equivalent facilitation of subsequent reflex blinks. To investigate whether the blink circuit obeyed rules analogous to those governing the associative and spike timing-dependent plasticity exhibited by individual synapses, we compared the effects of 3600 simultaneous IO and SO pairings, asynchronous IO and SO pairings, or synchronous IO and SO pairings separated by 20 ms on temporal interactions between IO and SO inputs to the blink circuit. Simultaneous pairing of a weak IO and a strong SO strengthened the IO input to the blink circuit, whereas asynchronous pairing weakened the stronger input. When the pairing pattern made an afferent input arrive after blink circuit activity, it weakened that afferent input. Analogous to synaptic modifiability, the results revealed that blink-evoking stimuli acted as a "presynaptic input" and blink circuit activity acted as a "postsynaptic spike." These mechanisms may create the maladaptive reorganization of trigeminal inputs in diseases such as hemifacial spasm.

Figure 1.

Temporal interaction of SO- and IO-evoked blinks. A, SO stimulus (▴) presented 60 ms before IO stimulus (▵). B, SO stimulus (▴) presented 20 ms before IO stimulus (▵). C, SO stimulus and IO stimulus presented simultaneously (▴). D, IO stimulus (▵) presented 20 ms before SO stimulus (▴). E, IO stimulus (▵) presented 60 ms before SO stimulus (▴). Each trace is the rectified OOemg of a single trial from the same rat.

Figure 2.

Temporal interactions between SO- and IO-evoked blinks as a function of relative control blink size. A, Mean (±SEM) normalized R1 OOemg amplitudes of the SO-evoked blink as a function of the interstimulus interval by which the IO stimulus preceded the SO stimulus when the control IO-evoked blink was smaller (IO < SO; ○) or larger (IO > SO; ·) than the control SO-evoked blink (left side of graph). Mean (±SEM) normalized R1 OOemg amplitudes of the IO-evoked blink as a function of the interstimulus interval by which the SO stimulus preceded the IO stimulus when the control IO-evoked blink was smaller (IO < SO; ▿) or larger (IO > SO; ▾) than the control SO-evoked blink (right side of graph). B, Mean normalized SO-evoked blink amplitude (SO Blink Amplitude) when preceded by an IO stimulation as a function of mean normalized IO-evoked blink amplitude (IO Blink Amplitude) when preceded by an SO stimulus for interstimulus intervals from 20 to 80 ms when the control IO-evoked blink was smaller (IO < SO; ○) or larger (IO > SO; ·) than the control SO-evoked blink. The solid line is the unity line. Each data point is the average of at least 30 trials.

Figure 3.

Temporal interactions between SO- and IO-evoked blinks before and after repeated simultaneous pairing of IO and SO stimuli. A, D, Mean (±SEM) normalized R1 OOemg amplitude of the SO-evoked blink (Relative SO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) repeated simultaneous pairing of IO and SO stimuli when the control IO-evoked blink was smaller (IO < SO; A) or larger (IO > SO; D) than the control SO-evoked blink. B, E, Mean normalized SO-evoked blink amplitude (Relative SO Blink Amplitude) when preceded by an IO stimulation as a function of mean normalized IO-evoked blink amplitude (Relative IO Blink Amplitude) when preceded by an SO stimulus for interstimulus intervals from 20 to 80 ms when the control IO-evoked blink was smaller (IO < SO; B) or larger (IO > SO; E) than the control SO-evoked blink before (○) and after (·) simultaneous SO and IO pairing. The solid line is the unity line. C, F, Mean (±SEM) normalized R1 OOemg amplitude of the IO-evoked blink (Relative IO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) simultaneous IO and SO pairing when the control IO-evoked blink was smaller (IO < SO; C) or larger (IO > SO; F) than the control SO-evoked blink. Each point is the average of data from at least 30 trials.

Figure 4.

Temporal interaction of IO and SO stimuli 1 d after simultaneous IO and SO pairing. A, Mean normalized SO-evoked blink amplitude when preceded by an IO stimulation as a function of mean normalized IO-evoked blink amplitude when preceded by an SO stimulus for interstimulus intervals from 20 to 80 ms when the control IO-evoked blink was smaller than the control SO-evoked blink (IO < SO). B, Mean normalized SO-evoked blink amplitude (Relative SO Blink Amplitude) when preceded by an IO stimulation as a function of mean normalized IO-evoked blink amplitude (Relative IO Blink Amplitude) when preceded by an SO stimulus for interstimulus intervals from 20 to 80 ms when the control IO-evoked blink was larger than the control SO-evoked blink (IO > SO). Data points are before pairing on day 1 (○), immediately after simultaneous pairing on day 1 (·), and before pairing on day 2 (▿). The solid line is the unity line. Each point is the mean of data from at least 20 trials from three rats.

Figure 5.

Temporal interactions between SO- and IO-evoked blinks before and after pairing in which the IO preceded the SO by 20 ms. A, C, Mean (±SEM) normalized R1 OOemg amplitude of the SO-evoked blink (Relative SO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) repetitive IO 20 SO pairing when the control IO-evoked blink was smaller (IO < SO; A) or larger (IO > SO; C) than the control SO-evoked blink. B, D, Mean (±SEM) normalized R1 OOemg amplitude of the IO-evoked blink (Relative IO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) repetitive IO 20 SO pairing when the control IO-evoked blink was smaller (IO < SO; B) or larger (IO > SO; D) than the control SO-evoked blink. Each point is the average of data from at least 10 trials.

Figure 6.

Temporal interactions between SO- and IO-evoked blinks before and after pairing in which the SO preceded the IO by 20 ms. A, C, Mean (±SEM) normalized R1 OOemg amplitude of the SO-evoked blink (Relative SO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) repetitive SO 20 IO pairing when the control IO-evoked blink was smaller (IO < SO; A) or larger (IO > SO; C) than the control SO-evoked blink. B, D, Mean (±SEM) normalized R1 OOemg amplitude of the IO-evoked blink (Relative IO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) repetitive SO 20 IO pairing when the control IO-evoked blink was smaller (IO < SO; B) or larger (IO > SO; D) than the control SO-evoked blink. Each point is the average of data from at least 10 trials.

Figure 7.

Temporal interactions between SO- and IO-evoked blinks before and after asynchronous IO and SO pairing. A, D, Mean (±SEM) normalized R1 OOemg amplitude of the SO-evoked blink (Relative SO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) asynchronous IO and SO pairing when the control IO-evoked blink was smaller (IO < SO; A) or larger (IO > SO; D) than the control SO-evoked blink. B, E, Mean normalized SO-evoked blink amplitude (Relative SO Blink Amplitude) when preceded by an IO stimulation as a function of mean normalized IO-evoked blink amplitude (Relative IO Blink Amplitude) when preceded by an SO stimulus for interstimulus intervals from 20 to 80 ms when the control IO-evoked blink was smaller (IO < SO; B) or larger (IO > SO; E) than the control SO-evoked blink before (○) and after (·) repetitive asynchronous SO and IO pairing. The solid line is the unity line. C, F, Mean (±SEM) normalized R1 OOemg amplitude of the IO-evoked blink (Relative IO Blink Amplitude) as a function of the interstimulus interval between the IO and SO stimuli before (Pre; ○) and after (Post; ·) repetitive asynchronous IO and SO pairing when the control IO-evoked blink was smaller (IO < SO; C) or larger (IO > SO; F) than the control SO-evoked blink. Each point is the average of data from at least 20 trials.