Multiple forms of learning yield temporally distinct electrophysiological repetition effects

Abstract

Prior experience with a stimulus leads to multiple forms of learning that facilitate subsequent behavior (repetition priming) and neural processing (repetition suppression). Learning can occur at the level of stimulus-specific features (stimulus learning), associations between stimuli and selected decisions (stimulus-decision learning), and associations between stimuli and selected responses (stimulus-response learning). Although recent functional magnetic resonance imaging results suggest that these distinct forms of learning are associated with repetition suppression (neural priming) in dissociable regions of frontal and temporal cortex, a critical question is how these different forms of learning influence cortical response dynamics. Here, electroencephalography (EEG) measured the temporal structure of neural responses when participants classified novel and repeated stimuli, using a design that isolated the effects of distinct levels of learning. Event-related potential and spectral EEG analyses revealed electrophysiological effects due to stimulus, stimulus-decision, and stimulus-response learning, demonstrating experience-dependent cortical modulation at multiple levels of representation. Stimulus-level learning modulated cortical dynamics earlier in the temporal-processing stream relative to stimulus-decision and stimulus-response learning. These findings indicate that repeated stimulus processing, including the mapping of stimuli to decisions and actions, is influenced by stimulus-level and associative learning mechanisms that yield multiple forms of experience-dependent cortical plasticity.

Figure 1.

Task schematic and levels of repetition. (A) During study, each target word was presented with the same decision cue 3 times, and subjects pressed 1 of 2 buttons to indicate a “yes” (Y) or “no” (N) response. At test, studied target words were presented again either with the same cue (Within-Task) or a different cue (AT), and Novel target words were presented for the first time. Of the AT trials, half required the same response as at study (AT-RR), and half required a different response (AT-RS). (B) The 4 test conditions differed according to repetition at the stimulus, stimulus–decision, and stimulus–response levels.

Figure 2.

Stimulus-locked ERP repetition effects. Grand average stimulus-locked waveforms averaged into 12 electrode regions as indicated on scalp map. Zero on the time axis (ms) marks target word onset.

Figure 3.

ERP repetition effects. (A) Stimulus-locked repetition effects displayed at representative left centro-parietal and medial centro-parietal electrode regions. (i) Stimulus repetition effect: stimulus repetition modulated the negative peak from 400 to 450 ms across all electrode regions with amplitude reduction for all repeated trials (W, AT, AT-RR, and AT-RS) compared with Novel trials (N). Bar graph represents mean amplitudes from 400 to 450 ms collapsed across all electrode sites. Topographical map represents mean amplitude difference between Novel and all repeated trials from 400 to 450 ms. (ii) Stimulus–decision repetition effect: stimulus–decision repetition modulated ERPs from 550 to 600 ms across all electrode regions and reflected more positive amplitudes for Within-Task compared with all other trial types. Bar graph represents mean amplitudes from 550 to 600 ms collapsed across all electrode sites. Topographical map represents mean amplitude difference between Within-Task and all other trial types (Novel and AT trials) from 550 to 600 ms. (iii) Stimulus–response repetition effect: stimulus–response repetition modulated ERPs from 450 to 500 ms with reduced negativity for AT-RR compared with AT-RS trials. During this time window, amplitude reductions were present for both of the conditions containing response repetition (Within-Task and AT-RR) compared with both of the conditions without response repetition (Novel and AT-RS) across medial electrodes. Bar graph represents mean amplitudes from 450 to 500 ms collapsed over all medial electrodes. Topographical map represents mean amplitude difference between AT-RS and AT-RR trials from 450 to 500 ms. Zero on the time axis (ms) marks target word onset. ERP amplitude differences relative to Novel trials is denoted ***P < 0.005, **P < 0.01, and *P < 0.05. (B) Stimulus–response conflict effects evident in response-locked ERPs displayed at right and left fronto-central electrode regions. (i) In the preresponse period (from −300 to −250 ms prior to response onset), amplitudes on AT-RS trials were more positive than all other trial types over right fronto-central electrodes. Bar graph represents mean amplitude during the preresponse period in the right fronto-central electrode region. Topographical map represents mean amplitude difference between AT-RS and AT-RR trials during the preresponse period. (ii) In the postresponse period (from 250 to 400 ms postresponse), amplitudes on AT-RS trials were more negative than all other trial types over left fronto-central electrodes. Bar graph represents mean amplitude during the postresponse period in the left fronto-central electrode region. Topographical map represents mean amplitude difference between AT-RS and AT-RR trials during the postresponse period. Zero on the time axis (ms) marks response onset. ERP amplitude differences relative to AT-RS trials is denoted *P < 0.05. Novel (N); Within-Task (W); Across-Task (AT); Across-Task Response Repeat (AT-RR); and Across-Task Response Switch (AT-RS). In all figures, error bars reflect within-subject standard error.

Figure 4.

Repetition-related spectral power changes occurred in the beta frequency range (≈12–30 Hz). (A) Time–frequency plots demonstrating an early (∼100–300 ms) beta power increase following the presentation of Novel trials (displayed at a representative fronto-central electrode). (B) Mean beta power from 100 to 300 ms was greater for Novel trials than for all repeated trials (W, AT-RR, and AT-RS). (C) Beta power increases for Novel trials compared with all repeated trials peaked at 153 ms.